Advances in the Study of Behavior, Volume 33 (Advances in the Study of Behavior)

Advances in THE STUDY OF BEHAVIOR VOLUME 33 Advances in THE STUDY OF BEHAVIOR Edited by Peter J. B. Slater Jay S. R...

Author: Peter J.B. Slater | Jay S. Rosenblatt | Charles T. Snowdon | Timothy J. Roper | Marc Naguib

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Advances in

THE STUDY OF BEHAVIOR VOLUME 33

Advances in THE STUDY OF BEHAVIOR Edited by

Peter J. B. Slater Jay S. Rosenblatt Charles T. Snowdon Timothy J. Roper Marc Naguib

Advances in THE STUDY OF BEHAVIOR Edited by Peter J. B. Slater School of Biology University of St. Andrews Fife, United Kingdom

Jay S. Rosenblatt

Timothy J. Roper

Institute of Animal Behavior Rutgers University Newark, New Jersey

School of Biological Sciences University of Sussex Sussex, United Kingdom

Charles T. Snowdon

Marc Naguib

Department of Psychology University of Wisconsin Madison, Wisconsin

Department of Animal Behavior University of Bielefeld Bielefeld, Germany

VOLUME 33

This book is printed on acid-free paper. Copyright ß 2003, Elsevier Inc.

All Rights Reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the Publisher. The appearance of the code at the bottom of the first page of a chapter in this book indicates the Publisher’s consent that copies of the chapter may be made for personal or internal use of specific clients. This consent is given on the condition, however, that the copier pay the stated per copy fee through the Copyright Clearance Center, Inc. (222 Rosewood Drive, Danvers, Massachusetts 01923), for copying beyond that permitted by Sections 107 or 108 of the U.S. Copyright Law. This consent does not extend to other kinds of copying, such as copying for general distribution, for advertising or promotional purposes, for creating new collective works, or for resale. Copy fees for pre-2003 chapters are as shown on the title pages. If no fee code appears on the title page, the copy fee is the same as for current chapters. 0065-3454/2003 $35.00 Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone: (+44) 1865 843830, fax: (+44) 1865 853333, e-mail: [email protected]. You may also complete your request on-line via the Elsevier homepage (http://elsevier.com), by selecting ‘‘Customer Support’’ and then ‘‘Obtaining Permissions.’’

Elsevier Academic Press 525 B Street, Suite 1900, San Diego, California 92101-4495, USA 84 Theobald’s Road, London WC1X 8RR, UK http://www.academicpress.com International Standard Book Number: 0-12-004533-8 PRINTED IN THE UNITED STATES OF AMERICA 03 04 05 06 07 08 9 8 7 6 5 4 3

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1

Contents

Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

ix xi

Teamwork in Animals, Robots, and Humans CARL ANDERSON AND NIGEL R. FRANKS I. II. III. IV. V. VI. VII. VIII. IX. X.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Social Insect Teams . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other Animal Teams. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Robot Teams . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Human Teams . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Team Size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Testing for Teamwork . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Misconceptions About Teamwork . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 5 17 21 25 28 30 35 39 41 41

The ‘‘Mute’’ Sex Revisited: Vocal Production and Perception Learning in Female Songbirds KATHARINA RIEBEL I. II. III. IV. V. VI.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vocal Perception Learning in Female Songbirds . . . . . . . . Vocal Production Learning in Female Songbirds . . . . . . . . Female Vocal Learning in Non-Oscine Birds . . . . . . . . . . . Sex Differences in Learning? . . . . . . . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

49 51 63 72 73 77 79

Selection in Relation to Sex in Primates JOANNA M. SETCHELL AND PETER M. KAPPELER I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II. Causes, Mechanisms, and Consequences of Sexual Selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v

87 88

vi

CONTENTS

III. IV. V. VI.

Relevance of Primates to Sexual Selection . . . . . . . . . . . . . Relevance of Sexual Selection to Primates . . . . . . . . . . . . . The Male Perspective: The ‘‘Copulatory Imperative’’ . . . . The Female Perspective: Biasing and Confusing Paternity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VII. Conflict Between the Sexes . . . . . . . . . . . . . . . . . . . . . . . . . . VIII. Conclusions and Future Directions . . . . . . . . . . . . . . . . . . . . IX. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

92 96 96 118 140 142 147 148

Genetic Basis and Evolutionary Aspects of Bird Migration PETER BERTHOLD I. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II. The Broad Palette of Theories on Control Mechanisms and Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . III. The Discovery of Circannual Rhythms: The Challenge to Genetic Studies . . . . . . . . . . . . . . . . . . . . IV. The Search for and Selection of Bird Species Suitable for Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V. Genetic Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VI. Quantitative Genetic Analysis. . . . . . . . . . . . . . . . . . . . . . . . VII. The Distribution and Key Role of Partial Migration . . . . . VIII. A New Theory of the Evolution, Control, and Adaptability of Avian Migration. . . . . . . . . . . . . . . . . . . . . . IX. Rapid Changes Due to Selection and Microevolution . . . . X. Outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . XI. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

175 176 179 180 183 200 209 211 213 221 223 225

Vocal Communication and Reproduction in Deer DAVID REBY AND KAREN MCCOMB I. II. III. IV. V.

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Reproductive Calls in Solitary Deer . . . . . . . . . . . . . . . . . . . Reproductive Calls in Gregarious Species . . . . . . . . . . . . . . Research in Progress and Future Directions . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

231 233 234 256 260 261

CONTENTS

vii

Referential Signalling in Non-Human Primates: Cognitive Precursors and Limitations for the Evolution of Language ¨ HLER KLAUS ZUBERBU I. II. III. IV. V. VI. VII.

Language Evolution. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Neural Basis of Language . . . . . . . . . . . . . . . . . . . . . . . Linguistic Capacities in Non-Human Primates . . . . . . . . . . Mental Processes Underlying Call Comprehension . . . . . . The Mind of the Signaler . . . . . . . . . . . . . . . . . . . . . . . . . . . Communication and Social Intelligence . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

265 266 267 271 291 297 299 300

Vocal Self-Stimulation: From the Ring Dove Story to Emotion-Based Vocal Communication MEI-FANG CHENG I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II. Early Fascination with the Female Nest Coo: Tinkering with the Neural Substrate . . . . . . . . . . . . . . . . . . III. Search for Female Vocal-Endocrine Links: Feedback Mechanisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. What Does the Female Nest Coo ‘‘Mean’’ to the Male? . V. Vocal-Endocrine Links: Cross-Species Comparisons . . . . . VI. Affective States in Acoustic Communication . . . . . . . . . . . VII. Emotional Referent in Vocal Communication: Role of Vocal Self-Stimulation. . . . . . . . . . . . . . . . . . . . . . . VIII. The Forebrain Pathways in the Non-Vocal Learner . . . . . IX. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

309

326 341 344 346

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

355

Contents of Previous Volumes . . . . . . . . . . . . . . . . . . . . . . .

365

310 313 320 321 323

Contributors Numbers in parentheses indicate pages on which the authors’ contributions begin.

CARL ANDERSON (1), School of Industrial and Systems Engineering, Georgia Institute of Technology, Atlanta, Georgia 30332-0205, USA PETER BERTHOLD (175), Max Planck Research Centre for Ornithology, Vogelwarte Radolfzell, Schlossallee 2, D-78315 Radolfzell, Germany MEI-FANG CHENG (309), Biopsychology Program, Department of Psychology, Rutgers University, Newark, New Jersey, USA NIGEL R. FRANKS (1), School of Biological Sciences, University of Bristol, Bristol BS8 1UG, United Kingdom PETER M. KAPPELER (87), Abteilung Verhaltensforschung und ¨ kologie, Deutsches Primatenzentrum, 37077 Go¨ttingen, Germany O KAREN MCCOMB (231), Experimental Psychology, University of Sussex, Brighton BN1 9QG, United Kingdom DAVID REBY (231), Experimental Psychology, University of Sussex, Brighton BN1 9QG, United Kingdom KATHARINA RIEBEL (49), Behavioural Biology, Institute of Biology, Leiden University, Leiden, The Netherlands JOANNA M. SETCHELL (87), Centre International de Recherches Medicales, BP 769 Franceville, Gabon ¨ HLER (265), School of Psychology, University of KLAUS ZUBERBU St. Andrews, St. Andrews, KY 16 9JP, Scotland, United Kingdom

ix

Preface

The aim of Advances remains as it has been since the series began: to serve the increasing number of scientists who are engaged in the study of animal behavior by presenting their theoretical ideas and research to their colleagues and to those in neighboring fields. We hope that the series will continue its ‘‘contribution to the development of cooperation and communication among scientists in our field,’’ as its intended role was phrased in the Preface to the first volume in 1965. Since that time, traditional areas of animal behavior research have achieved new vigor by the links they have formed with related fields and by the closer relationship that now exists between those studying animal and human subjects. Scientists studying behavior today range more widely than ever before: from ecologists and evolutionary biologists, to geneticists, endocrinologists, pharmacologists, neurobiologists, not forgetting the ethologists and comparative psychologists whose prime domain the subject is. It is our intention not to focus narrowly on one or a few of these fields, but to publish articles covering the best behavioral work from a broad spectrum. The skills and concepts of scientists in such diverse fields necessarily differ, making the task of developing cooperation and communication among them a difficult one. But it is one that is of great importance, and one to which the Editors and publishers of Advances in the Study of Behavior are committed. We will continue to provide the means to this end by publishing critical reviews, by inviting extended presentations of significant research programs, by encouraging the writing of theoretical syntheses and reformulations of persistent problems, and by highlighting particularly penetrating research that introduces important new concepts. The present volume is mainly focussed on birds and mammals. Several of these contributions are on their vocal communication, but these illustrate very well how one field within the study of behavior can benefit from many different approaches and can, in turn, illuminate a variety of aspects of the subject as a whole. Reby and McComb are concerned with the structure and function of vocal displays in deer, Cheng present ideas on the emotional significance of communication based on her studies of vocal self-stimulation in doves, while Riebel points to a relatively neglected issue in the the much-explored world of bird song learning: production and perception by females. In his chapter, Zuberbu¨hler describes playback experiments on monkeys that give insight into their cognitive capacities and discusses the extent to which these might act as pre-adaptations for xi

xii

PREFACE

language. The other three chapters explore a wide range: Anderson and Franks provide an interesting new framework exploring how animals, humans, and robots work in teams; Setchell and Kappeler review the impact of sexual selection on primates; Berthold describes his impressive body of work on bird migration and, in particular, genetic influences upon it. With this volume, we welcome Dr. Marc Naguib to the editorial team, and Dr. Jane Brockmann will be joining us with the next. Their skills and expertise will be invaluable to us, and they will help to ensure the continued broad geographical and intellectual spread of the series so that, as it moves into its fifth decade, it will continue to have the high impact on the field that it has had since it first appeared in 1965.

ADVANCES IN THE STUDY OF BEHAVIOR, VOL. 33

Teamwork in Animals, Robots, and Humans Carl Anderson1 and Nigel R. Franks2

1

school of industrial and systems engineering georgia institute of technology atlanta, georgia 30332-0205, usa 2

school of biological sciences university of bristol bristol, bs8 1ug uk

I. Introduction Teamwork is common in our own social interactions but is not restricted to humans. Animals, from ants to whales, may also work in teams. When part of certain multi-robot systems, robots may also use teamwork. However, do we really have the same notion of a team in each of these cases? Do the same definitions, concepts, and issues apply when considering these three seemingly disparate types of agents: animals, robots, and humans? In this article, we consider what it means fundamentally to work as a team. Anderson and Franks (2001) recently redefined teamwork for animal societies and found that a definition developed primarily from studies of social insects also applied more generally to other social animals including vertebrates such as lions, hyenas, and whales. In other words, the crucial issues when a pod of humpback whales hunts cooperatively (Sharpe, 2000; Clapham, 2000) appear to be the very same as when a small group of army ants retrieves a prey item as a team (Franks, 1986, 1987; Franks et al., 1999, 2001). This, in itself, was a surprising result. What was more surprising, however, was that when Anderson and McMillan (200x) made a similar comparison between social insect teams and certain types of human teams (those that are selforganized), the same conclusions held. Despite the vast differences between humans and social insects, and the differences between their societies, certain aspects of their cooperative activity show strong commonalities. Taken together, these observations strongly suggest that there are certain underlying and possibly fundamental principles in the organization of work. 1 Copyright 2003 Elsevier Inc. All rights reserved. 0065-3454/03 $35.00

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CARL ANDERSON AND NIGEL R. FRANKS

The goals of this article are as follows. First, we will demonstrate that a single, generic definition of teamwork applies in vastly different social systems. Robots may also use teamwork when part of certain multi-robot systems. Second, we will specify how one recognizes and tests whether a particular instance of highly cooperative activity really is teamwork. How might we rigorously and objectively distinguish between teamwork and other closely related phenomena, such as groupwork? Third, we will broaden the scope from humans and non-human animals to a third major system of interacting ‘‘agents’’ in which teamwork is claimed—robotics. How do roboticists view teamwork in their systems, and, once again, are we dealing with the same issues and concepts of teamwork? Our fourth and final aim is to highlight and to clarify a number of common misconceptions about teamwork. Researchers in one field, based on the examples they usually encounter, may make certain claims about teams which, when one compares teams across fields, are not universally true. Thus, by discrediting some of these claims with revealing examples from other fields, we will draw out some of the truly generic features of teams. Throughout, we clarify key concepts with illustrative examples. However, readers will notice a certain bias towards social insects. Teamwork has never been doubted in multirobot systems and human societies, whereas it has previously been disputed and dismissed in insect societies. A contributory factor is that so few examples were known. Even in Anderson and Franks’ (2001) recent review, only a handful of candidate social insect teams were known (see also Anderson and McShea, 2001b). Now, however, we are in the position to illustrate a much larger, more significant, and informative collection of examples. Admittedly, our bias in favor of social insects also reflects our enthusiasm for these animals; they are a major research focus for both of us. The organization of this chapter is as follows: First, we consider the structural organization of tasks, that is, a classification of task types (Section I). Then we examine teamwork in insect societies (Section II), in other (non-human) animal groups (Section III), in robotics (Section IV), and in humans (Section V). Section VI discusses team size, Section VII how one might test for teamwork, and Section VIII misconceptions about teamwork. Finally, there is a general discussion and conclusions followed by a summary (Sections IX and X). A. Task Types Before we can proceed, it is necessary to outline our general approach and perspective, which permits a meaningful comparison of work organization across vastly different systems. Our approach, first outlined

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TEAMWORK IN ANIMALS, ROBOTS, AND HUMANS

in Ratnieks and Anderson (1999) and developed further in Anderson and Franks (2001) and Anderson et al. (2001), is to focus on the structure of the task itself, rather than focusing on the individuals tackling a task. Tasks may sometimes be broken down into meaningful subunits or ‘‘subtasks.’’ For example, in the honey bee (Apis mellifera), nectar foragers collect nectar and transfer it to receiver bees back at the nest. The latter bees store the material in the comb (Seeley, 1995; Ratnieks and Anderson, 1999). Here there are two distinct subtasks, ‘‘collection’’ and ‘‘storage,’’ clearly delineated by the act of transfer. (This is a partitioned task; see later.) Other tasks have a different structure. For instance, when collectively retrieving a large prey item, Formica wood ants are notoriously uncoordinated; several ants may pull together in order to overcome frictional forces from over the ground, but they may, in fact, sometimes pull against each other (Sudd, 1963, 1965). Here there is no division of labor, and there are no subtasks—each individual has the same role, simply to pull. (This is a group task; see later.) It is from ideas such as these that a scheme of four fundamental task types based upon the interrelationship between subtask types was devised (Anderson and Franks, 2001; Anderson et al., 2001). The characteristic features of all four types are briefly outlined here, with a more detailed and definitional summary appearing in Table I.

TABLE I Characteristics of the Four Task Types*

Task type

Number of individuals

Individual Group Partitioned Team

Single Multiple Multiple Multiple

a

Division Divided of into labor? subtasks? No No Yes Yes

Concurrent activity necessary?

No No No Yes Yes or Noa Yes or Nob Yes Yes

Subtask organization

Overall task complexityc

— — Sequential Concurrent

Low Medium High High

Tasks can be partitioned without a division of labor (e.g., when an individual periodically switches between two or more of the subtasks) (Jeanne, 1986; Ratnieks and Anderson, 1999). b Task partitioning requires concurrent activity when direct transfer occurs (i.e., when material is handed directly to another individual), but not necessarily when only indirect transfer (caching) is involved. c Specified in detail in Anderson et al. (2001). * This table defines the different task types; for instance, a team task requires two or more individuals (column 2) performing two or more subtasks (column 3) concurrently (columns 5 and 6). After Anderson and Franks, 2001; Anderson et al., 2001.

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1. Individual task. A task that a single individual can successfully complete without help from other individuals. For instance, for a lone hunter such as a domestic cat, capturing a mouse might represent an individual task, a task it can complete alone. 2. Group task: A task that necessarily requires multiple individuals to perform the same activity concurrently. Here there are no subtasks and there is no division of labor. In short, individuals must do the same thing at the same time or the task cannot be completed. For instance, Myrmecocystus mimicus honeypot ants perform highly stereotyped displays during territorial combats with neighboring colonies (Ho¨lldobler, 1976). Workers convey the size and strength of their colony to their enemy by effectively forming a line of displaying ants along the boundary. This colony-strength (honest) signal only functions with the concurrent action of multiple individuals. 3. Partitioned task: A task that is split into two or more subtasks that are organized sequentially (Jeanne, 1986; reviewed in Ratnieks and Anderson, 1999; Anderson and Ratnieks, 2000). Nectar ‘‘collection’’ (subtask 1) and ‘‘storage’’ (subtask 2) in A. mellifera are two such examples. Partitioned tasks often take the form of some material or product that is passed from individual to individual (or even to some group) in a relay fashion. These task types are particularly easy to divide into subtasks, as it is the very act of transfer that delineates them. 4. Team task: A task that necessarily requires multiple individuals to perform different subtasks concurrently (Anderson and Franks, 2001). That is, there is a crucial division of labor and crucial concurrency. In short, different individuals must do different things at the same time or the task cannot be completed. For example, in the ant Pheidole pallidula, a polymorphic species that has both majors and minors, intruders are killed using teamwork. A group of workers will immobilize or ‘‘pin down’’ the intruder until a major arrives and decapitates it (Detrain and Pasteels, 1992). In this example, the task, ‘‘kill the intruder,’’ involves the following two subtasks: ‘‘immobilize the intruder,’’ a group subtask (that is, a subtask that is like a group task) and ‘‘decapitate the intruder,’’ an individual subtask (a subtask that is effectively an individual task). Only when both subtasks are performed concurrently can the task be completed; hence, it is a team task.


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By focusing on the structure of the tasks, rather than on the individuals (or ‘‘agents’’) who tackle them and the cognitive abilities required to complete each subtask, we have created a common framework with which we can make comparisons across systems. We thus focus solely on the cooperative behavior and the interdependencies among individuals’ contributions. Based upon a task’s structural organization, it would then be possible to use the metric detailed in Anderson et al. (2001) to quantify a task’s complexity. This potentially allows one, for instance, to rank different tasks from different systems objectively, to correlate a particular task’s complexity with organization size or evolutionary history, or to follow how a particular task is sometimes tackled in a more complex, collaborative manner than at other times. The above approach works on one level, task structure per se, and is individual independent. However, we may also wish to consider how a particular set of individuals must work to complete the task. That is, what may represent a difficult team task for one set of individuals—for example, a group of ants—may represent an easy individual task for an animal such as a human. Therefore, suggesting that a set of individuals can complete a certain task only in a certain way (e.g., as a team) is only meaningful and valid with regard to the constraints of the individuals tackling it. These issues, that the same task may represent a different task type to different individuals, and that a task may be tackled in one way at some times and in a different manner at other times, are discussed later (Section IX).

II. Social Insect Teams In this section, we will first outline the reason Anderson and Franks (2001) felt it necessary to redefine social insect teams, which had been dismissed in all but a tiny minority of insect societies. This also introduces a number of key issues and insights about teamwork. This discussion is followed by a detailed examination of proposed social insect teams. A. Why Redefine Teams? In their important and highly influential monograph Caste and Ecology in the Social Insects, Oster and Wilson (1978, p. 151) include a threeparagraph subsection entitled ‘‘The nonexistence of teams.’’ We quote their text in full, italicizing two sentences of particular importance.

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The relation of the members of an insect society to one another can be characterized as one of impersonal intimacy. With the exception of the dominance orders of primitively organized forms such as paper wasps and bumble bees, eusocial insects do not appear to recognize one another as individuals. Their classificatory ability is limited to the discrimination of nestmates from aliens, members of one caste as opposed to another, and the various growth stages among immature nestmates. A consequence of this lower grade of discrimination is that members of colonies do not form cliques and teams. Groups assemble to catch prey, excavate soil, and other functions requiring mass action; and odor trails and other sophisticated techniques have evolved that permit the rapid recruitment of nestmates to the work sites. But the participants are entirely changeable. There is no evidence that they come and go as teams. The lack of team organization is not necessarily the outcome of the limited brain power of social insects. It can be shown that at a very general level processes are less efficient when conducted by redundant teams than when conducted with redundant parts not organized into teams. This disparity can be overcome or reversed, as in fact it is in human beings, only if the degree of coordination among its members of the teams or between the teams is sufficiently great to compensate for the shortcomings inherent in the system redundancy.

We agree with all of this material except, crucially, the two italicized sentences. Insect societies are certainly a case of impersonal intimacy, and after twenty-five further years of research there is very little evidence that social insects can recognize each other as individuals (but see Tibbetts, 2002). Oster and Wilson, however, suggest that this is a necessary requirement for teamwork (the first italicized sentence). But why should this be? Suppose you are tying a parcel with string and need help. You ask the nearest person to put their finger on the point to be tied while you tie a bow. The task is completed and the person leaves. It is not necessary for you to know the person’s name, or to recognize them during the operation or in the future. All that matters is that you coordinate your respective subtasks, ‘‘putting finger on joint’’ and ‘‘tying the bow,’’ in the appropriate manner to complete the task. As Oster and Wilson indicate in the second and third paragraphs, this is exactly the way that insect societies operate. They are inherently redundant, but that is their secret to success. Let us suppose that in our Pheidole pallidula example above, a group of minors have pinned down an intruder. A major that has been recruited, or happens to come across such an individual, does not need to recognize those ants holding the intruder down. All it must do is recognize that this is an immobilized intruder and perform the correct action: decapitate the individual. Thus, the sentence ‘‘But the participants are entirely interchangeable’’ is significant. This is


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exactly why such teamwork, and other coordinated activity in insect societies, is so adaptive. They do not need to work with certain individuals; anyone in the vicinity who has the ability to perform the required subtask(s) will suffice. Groups of individuals that came and went as a team would seem to be maladaptive. Any member that was lost would mean the functional demise of the whole team until a specific replacement could be found. Twelve years after the publication of this monograph, Ho¨lldobler and Wilson (1990) published their Pulitzer prize-winning book The Ants. By this time, the concept of teams, which had now become accepted to some degree, had changed significantly. Until recently, there has been no evidence for the existence of teams, which can be defined as members of different castes that come together for highly coordinated activity in the performance of a particular task. A team would not consist of particular ants, but rather of interchangeable members of particular castes. . .An exceptional case of team organization has been reported by Franks (1986) in the group retrieval of prey by Eciton burchelli. . .Teamwork needs closer study in Eciton and other ant species that employ group transport. . . (Ho¨lldobler and Wilson, 1990, p. 343).

This issue of redundancy had been clearly recognized and addressed. However, in our minds, this definition is still overly restrictive in that it specifies that members of different castes must cooperate in a team. This has two important implications: (1) Teams could not occur in societies with monomorphic workers, and (2) even in a polymorphic society, there must be a mix of castes. Can teams occur in monomorphic societies? Yes. Your parcel-tying helper could help you with your task, even if she were your clone. Our examples of social insect teams (detailed below) in Aphaenogaster, Leptothorax, Myrmicaria, Protomognathus, and Apis—all monomorphic genera (Oster and Wilson, 1978)—each involving similar-sized and similarskilled individuals, illustrate this same point. Must teams involve a mix of castes? No. Such a restriction would mean that a high school baseball team was not a team unless it contained a specialized pitcher, catcher, and so on. This is clearly not the case. A professional team on the other hand will likely contain such specialists because they will tend to enhance team performance. Similarly, in insect societies, natural selection favors certain castes specializing in certain subtasks in some situations (as in Pheidole pallidula, in which only the majors are capable of decapitation); but as an abstract concept—‘‘team’’—interindividual differences are not strictly necessary. An additional complication with Oster and Wilson’s (1978) implication here is that species such as Dorylus driver ants, which have

8


continuous size variation rather than discrete castes, would be difficult or impossible to classify as a team. How does one distinguish ‘‘particular castes’’ here? As we argue below (originally in Franks et al., 1999, 2001), Dorylus workers do sometimes work as a team. If we have labored these two points, it is for an important reason: Under Anderson and Franks’ (2001) definition, a team is simply the set of individuals that tackles a team task. There are no further assumptions or restrictions about caste, individual recognition, or other aspects of team membership. In the following subsections, we review the existence of teams in insect societies. Although Anderson and Franks (2001) attempted such a review for social insects while redefining what it meant to work as a team, only very few examples were known then. Here, we list many new examples and demonstrate that such highly collaborative activity may be more widespread than originally thought. We also take this opportunity to include greater detail about some of these examples than is standard. This is because some of the literature is fragmented, sometimes old (dating to 1879 in one case), and can be very hard to track down. B. OECOPHYLLA There are two living species of Oecophylla ants, O. longinoda, which is found in Africa, and O. smaragdina, which ranges from India to Australia (Ho¨lldobler and Wilson, 1983). These ants are known colloquially as weaver ants because they live in trees and bind or ‘‘weave’’ living leaves together to form their nests (Ho¨lldobler and Wilson, 1977, 1983, 1990; Fig. 1a). To achieve this complex task, it seems that three subtasks are needed. First, ants must ‘‘pull the leaves together’’ (subtask 1). This is easier said than done. If the distance between the two leaves is small, a single ant may be able to bridge the gap and start pulling. If this is the case, it may be that many workers will line up in parallel, a group task, and pull together. However, usually the gaps are much larger, several ant lengths or more, and so the ants form a striking structure, a pulling chain (a type of ‘‘selfassemblage’’; Anderson et al., 2002). A pulling chain is a chain of ants, each ant using their mandibles to hold onto the petiole or ‘‘waist’’ of the ant in front. While the first ant holds onto the leaf to be pulled, the last ant in the chain uses its tarsal claws to hook onto the other leaf. As it walks backward, it closes the gap so that the feet of the ant in front reach the leaf and hook on. This contraction of the chain closes the gap. Once the gap is closed, many workers then hold the leaves in place. As such, it is reasonable to consider this first subtask a group subtask.


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Fig. 1. a. Oecophylla smaragdina workers constructing a nest using teamwork (copyright Turid Ho¨ldobler-Forsyth, with permission). b. Myrmicaria opaciventris ants stimulate a Caternautellia rugosa nymph for honeydew (courtesy Alain Dejean, with permission). (See Section II.C.) c. Two Eciton burchelli ants, one sub-major (leading) and one minor (following), act as a team to retrieve part of a scorpion’s tail (courtesy Nigel R. Franks).

While the leaves are being held together, the second main subtask, glueing the leaves together, must be performed. However, this too is a sophisticated behavior, a team subtask in itself. To glue the seam together, one worker will take one of the colony’s own larvae and move it over the area to be glued while gently squeezing it (subtask 2). Such squeezing stimulates the larva to produce silk (subtask 3). In most ants, such silk would be used by a larva to spin its own cocoon; in Oecophylla, this silk now functions as glue.

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It is clear that Oecophylla appear to use highly sophisticated teamwork to form their nests. A pulling chain is used to bring the leaves together, usually a group subtask, while at the same time, they must be bonded using larval silk. This latter component is a team in itself—a team within a team—in which a larva produces the glue, an individual subtask, while the worker moves this living ‘‘glue-gun’’ over the area to be glued, another individual subtask (Table II; Anderson et al., 2001). All three components must be performed simultaneously for the task to be completed. C. MYRMICARIA Many species of ants protect and tend to other insects—for example, aphids—in order to collect honeydew, the excess sugar-laden plant sap that the insects have tapped from the plant (Wheeler, 1910; Beattie, 1985; Ho¨lldobler and Wilson, 1990). One such example, one that seems to involve teamwork, centers on the tending of the heteropteran Caternautellia rugosa (Fig. 1b). When a large ant such as a Camponotus brutus worker tends to one of these nymphs, the ant can carry out all the attendant tasks, including stimulating the nymph’s dorsal glands while collecting the honeydew from the nymph’s anus, by itself. For smaller ants, such as Myrmicaria opaciventris (Dejean et al., 2000; A. Dejean, personal communication), these two subtasks, ‘‘stimulation’’ and ‘‘collection,’’ must TABLE II Task Structure of Some Proposed Social Insect Teams* Task structure and example

Task and subtasks

Team T ¼ I1 þ I2

Individual

Individual

Aphaenogaster foraging from plants Dorylus and Eciton prey retrieval (when there is a single follower) Myrmicaria honeydew collection (with several worker stimulating nymph’s dorsal glands) Pheidole militicida seed opening Protomognathus (¼Harpagoxenus) americanus and Leptothorax (¼Myrafant) duloticus slave raids

T¼ I1 T¼ I2 T¼ I1 I2 T¼ I2 T¼ I2

Obtain capsule from plant; ¼ Gnaw peduncle; I2 ¼ Twist capsule Retrieve prey; I1 ¼ Front-running; ¼ Following Collect honeydew; ¼ Collect honeydew; ¼ Stimulate dorsal glands Open seed; I1 ¼ Hold seed; ¼ Gnaw end of seed Steal brood; I1 ¼ Guard entrance; ¼ Capture brood

(continued)


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TABLE II (continued) T¼IþG

Team Individual

Group

Apis social encapsulation

Dorylus and Eciton prey retrieval (when there is group of followers) Myrmicaria honeydew collection (with several worker stimulating nymph’s dorsal glands) Pheidole and Pheidologeton silenus intruder decapitation

T ¼ Encapsulate beetles; I or G ¼ Guard beetle; G or I ¼ Build propolis corral T ¼ Retrieve prey; I ¼ Front-running; G ¼ Following T ¼ Collect honeydew; I ¼ Collect honeydew; G ¼ Stimulate dorsal glands T ¼ Kill the intruder; I ¼ Decapitate the intruder; G ¼ Immobilize the intruder

Team T ¼ G1 + G2

Group

Group

Apis social encapsulation Pheidologeton diversus predation

T ¼ Encapsulate beetles; G1 ¼ Guard beetle; G2 ¼ Build propolis corral T ¼ Overcome prey; G1 ¼ Immobilize prey; G2 ¼ Kill prey

Team Group

Team

Individual

T1 ¼ G + T2, where T2 ¼ I1 + I2

Individual

Oecophylla nest construction

T1 ¼ Build nest; G ¼ Pull leaves together; T2 ¼ Glue leaves together; I1 ¼ Move larva over seam; I2 ¼ Produce silk

*The hierarchical structures of the tasks are shown in the first column with each box representing a task or subtask. The particular tasks and subtasks are detailed more explicitly in the second column; T,I, and G represent team, individual and group (sub)tasks respectively. Subscripts are used when there is more than one (sub)task of the same type.

be performed by at least two individuals working concurrently, one or more stimulating the nymph while the other(s) collect(s) the honeydew. In the words of Dejean and his colleagues (2000, p. 450), ‘‘one to three workers waited for the honeydew secretion while others moved to the

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nymph’s side or even climbed onto their bodies in order to palpate the dorsal glands.’’ Thus, it seems that the Myrmicaria ants can only achieve the goal, to collect the honeydew, while working as a team. D. ECITON and DORYLUS Prey retrieval by Eciton burchelli army ants (Franks, 1986, 1987) was the first accepted example of a social insect team (Section II.A; Anderson and Franks, 2001). In these teams, there are two subtasks—front running, involving a single ant at the front carrying the prey, and following, involving one or more ants, also carrying the prey but from the rear. The role of the front-runner is to get the prey item moving. As larger individuals achieve this more easily, it is perhaps not surprising that front-runners tend to be submajors. Submajors are rare in Eciton colonies (they make up just 3% of the workforce), but they represent 25% of all individuals—that is, porters— involved in prey retrieval (Franks, 1986, 1989). This more inclusive term is needed because it is individuals working alone who often transport prey items, not groups or teams. Once a submajor starts moving the prey item along the foraging column, other individuals join in and help. Sometimes there is just a single follower (Fig. 1c). At other times, several individuals, usually smaller ones, may help. At first sight, the distinction between the two subtasks, front-running and following, might seem trivial. To show that it is not, consider prey retrieval groups, such as those in Formica wood ants (mentioned earlier). These ill-coordinated groups are notoriously inefficient, with different ants trying to take the lead (Sudd, 1963, 1965). However, army ants straddle the items they carry and both front-runners and followers face in the same direction. This means that the front-runner remains the front-runner and all of the ants work well together. In principle, two army ants might straddle the same item but face and pull in opposite directions, but this is never observed. This implies that the group has a distinct structure in which cooperation is maximized by a simple division of labor between the one at the front and the one or more at the rear (Anderson and Franks, 2001). Moreover, given the distribution of castes in the foraging column— that is, the individuals available to form the team—(Franks et al., 2001) found that the front-runner was especially large and the followers were especially small. In short, they have a particularly skewed distribution of team members. Such teamwork is not restricted to Eciton. These army ants, which live only in Central and South America, have an ecological counterpart, Dorylus, in Africa. Dorylus have a similar prey retrieval team structure to Eciton. One difference though is that Dorylus do not have discrete castes, but vary in size continuously across a very broad range. The


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same structure is also found: (1) single front-runners and one or more followers, and (2) especially large front-runners and especially small followers are also found (Franks et al., 2001). The evidence that such a defined team structure in Eciton (Franks, 1986, 1987) and Dorylus (Franks et al., 1999) has a very important consequence: The teams are ‘‘superefficient.’’ In general, we might define superefficiency as N individuals completing a task more than N times faster or more efficiently than one individual (Franks, 1986; Balch and Arkin 1994; Balch et al., 1995). In short, superefficiency is a case of the ‘‘whole being more than the sum of the parts.’’ However, such is the effect in these ants that an item carried by a team cannot be divided up in any way so that all of the fragments can be carried away by the original team members. Franks (1986) suggests that the reason for this group-level property is that rotational forces disappear. Anyone who has carried a long plank of wood or a ladder by themselves will understand. Either it involves a careful balancing act, or it drags on the floor, making it harder to move. Compare that to how much easier it is when another person holds the end of the item. This does not necessarily arise from a sharing of the weight per se, although that will certainly help. Even if the helper simply stops the item from rotating and dragging, it makes moving the item far easier. Similar principles apply to team transport in army ants, which Franks et al. (2001) liken to a penny-farthing bicycle—an old bicycle which has a very large wheel at the front and a tiny wheel at the rear. The analogy with a penny-farthing bicycle reveals how a team of two can be more than the sum of its parts. The tiny castor-like rear wheel on a penny-farthing bicycle transforms the properties of the machine out of all proportion to its size. Similarly, the synergism between a large ant and a small one in a team boosts the performance of both—again, because rotational forces are balanced and disappear. E. APIS Teamwork is not confined to ants. The following example comes from the Cape honey bee (Apis mellifera capensis), a species native to South Africa. Honey bee colonies may become infested by hundreds of small hive beetles (Aethina tumida). These small round beetles, each about half the size of a bee, have the ability to withdraw their legs and head into their tough ‘‘shell.’’ Hence, the bees have a hard time getting rid of them, especially as the beetles may hide in cracks in the nest. However, the bees have evolved a rather impressive way of dealing with them: They imprison them in sticky corrals, a behavior which has been termed ‘‘social encapsulation’’ (Neumann et al., 2001a,b). The bees use propolis, a sticky

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tree resin that the workers usually collect to seal cracks in the nest, to make a prison around the beetles. Some of these prisons completely seal their captives inside. Construction can take up to four days and seal in a single individual or as many as two hundred beetles (Neumann et al., 2001a,b). The key point, however, is that the bees use teamwork to achieve this; while some bees make the prison, others guard the beetles and stop them from escaping (Neumann et al., 2001a,b; Ratnieks, 2001; Randerson, 2001). Both guarding and building may be individual or group subtasks, and all four combinations have been observed (P. Neumann, personal communication). This behavior serves at least two purposes. First, it confines the beetles and can prevent them from reproducing, a particular problem because the beetles can be very fecund (Lundie 1940, cited in Neumann et al., 2001a). Second, if the infestation is very high and the best strategy for the colony is to abscond (desert the nest and start a new parasite-free home elsewhere), such teamwork can give the colony time to prepare for its departure. Interestingly, this teamwork is only seen in the South African race of the honey bee; other races do not appear to have evolved this shrewd strategy, and so infestations are more of a problem. Ratnieks (2001) suggests that this teamwork is a social analogue of antiparasite defense in multicellular organisms; that is, the host organism (read colony) uses special blood cells (cf. bees and propolis) to engulf or encyst (encapsulate) parasitic larvae that manage to elude the host’s primary defenses. F. PROTOMOGNATHUS and LEPTOTHORAX Slave-Making Ants Of the ten thousand or so known ant species, only a tiny minority, about fifty species, are slave-makers (D’Ettorre and Heinze, 2001). Slave-makers are ants that raid the nests of other ant species and steal their brood. These stolen brood eclose into workers that essentially become domestic slaves for the colony. Interestingly, two of these slave-maker species hint at teamwork. During a raid, host workers tend to grab their brood and flee the nest. However, in the slave-maker species Protomognathus (¼Harpagoxenus) americanus and Leptothorax (¼Myrafant) duloticus, a member of the raiding party acts as a guard at the nest entrance (Alloway, 1979; Foitzik et al., 2001). The guard prevents host workers from escaping with brood, thus ensuring there is brood to steal while other ants from the slave-making nest steal the brood. Structurally, this is a team task, ‘‘steal brood,’’ with two individual subtasks—‘‘guard entrance’’ and ‘‘capture brood.’’


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G. PHEIDOLE The Pheidole pallidula example discussed earlier is not the only instance of teamwork (sensu stricto Anderson and Franks, 2001) in this genus. Wilson and Ho¨lldobler (1985, p. 18) describe very similar behavior in P. embolopyx: ‘‘The minors seized the legs and spread-eagled enemy worker ants, while the majors attacked the body directly and were more effective at cutting them into pieces.’’ And, in yet another species, ‘‘Worker P. punctulata were seen holding down an [Oecophylla] longinoda worker while their soldiers ‘jointed’ [i.e., chopped into pieces] its limbs and body with their mandibles’’ (Way, 1953, p. 681). (See Eisner et al., 1976, for a possible parallel among termites.) From these two vague descriptions, it is not possible to tell whether the cutting (or ‘‘jointing’’) subtask involves one or more majors acting simultaneously; that is, whether it is an individual or group subtask. More detailed descriptions are clearly needed. In P. militicida, teamwork appears to serve a different purpose. The minors open the seeds of the [Tridens] pulchellus and desvauxii by gnawing at the pointed end of the seed. Sometimes the seed is held by one minor and gnawed open by another, but a more common method involves only one minor, who places the blunt end of the seed on the floor of the nest and, with the seed held in a vertical position gnaws at its pointed end (Creighton and Creighton, 1959, p. 7).

This is a perfect example of a task that is sometimes tackled by teams, with one worker ‘‘holding’’ and another ‘‘gnawing,’’ and sometimes by individuals, when one worker holds and gnaws simultaneously. This aspect, that a task may be of a different task type depending upon which animals are working on it, is covered in detail later (Section VIII). H. PHEIDOLOGETON The following, a rather anecdotal example of prey capture and dismemberment in Pheidologeton silenus ants, is similar to that of Pheidole: ‘‘Minors pinned down prey, which were then torn apart by the mandibles of both minors and non-minors. . .(C. Kugler, 1978, personal communication)’’ (Moffett, 1988, p. 359). From this scant description, the task structure is not entirely clear. However, like army ants, P. silenus is a group hunter with column and swarm raids. It is likely that both ‘‘minors pin down prey’’ and ‘‘minors and majors tear apart prey’’ are group subtasks, with the latter subtask involving a mix of castes. Moffett’s (1987) account is also suggestive of such a scenario in P. diversus. In both species, it cannot be ruled out that the latter subtask could be conducted as an

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individual subtask by a media (an intermediate-sized ant) or major. However, more detailed observations and descriptions are needed to further categorize and analyze the task structure. A description that exactly mirrors that of the Pheidole, hinting strongly that teams do exist in this genus, is the following: . . .when a hapless Malaysian Diacamma ant blunders directly into the midst of the marauder’s [Pheidologeton diversus] trail, agile minors push forward to pin it to the ground. . .With the adversary defenseless, a major arrives and kills it with repeated crushing blows (Moffett, 1986, p. 286).

I. APHAENOGASTER An old reference that hints at another team task, but unfortunately whose text is so vague that it is neither clear which Aphaenogaster ant species or plant (shepherd’s purse, Capsella bursa-pastoris, or chickweek, Alsine media) is being referred to, is the following. These ants climb plants to tear off green fruits to take back to the nest. This can be an individual task—an ant may ‘‘seize the peduncle of the [shepherd’s purse] capsule between its mandibles and, fixing its hind legs firmly as a pivot, twist the peduncle round and round until it is broken off’’ (Heim, 1898, p. 414), but these ants may also sometimes work as teams involving two individual subtasks. We may frequently see two ants combine for the purpose of breaking the peduncle of a capsule. While one is gnawing the peduncle the other will twist it off; but it seems that their mandibles are never strong enough to sever the peduncle by cutting alone (Heim, 1898, p. 414).

J. A Cautionary Note When ascertaining whether an insect society, or indeed any society, employs teamwork, we must be cautious; just because a description appears to be of a team task, it is not necessarily so. For example, Hogue (1972, p. 95) states, ‘‘A major worker of [Eciton] hamatum locked onto its prey with its large mandibles. Workers this size restrain the prey while smaller individuals cut it to pieces.’’ At first sight, this seems remarkably similar to some of our previous examples. However, Nigel R. Franks, having spent many years studying army ants in the tropics, believes that this behavior probably does not occur and is not indicative of a team. Similarly, the seed harvester ant Pogonomyrmex barbatus clears roadways free of plants leading from its nest and the disk around the nest itself by cutting them down. McCook (1879, p. 23; McCook, 1909, Fig. 35) cites occasional


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division of labor in this operation: ‘‘In two or three cases there appeared to be a division of labor; that is to say, while the cutter at the roots kept on with her work, another climbed the grass blade and applied the power at the opposite end of the lever. This position may have been quite accidental, but it certainly had the appearance of a voluntary cooperation.’’ We find it hard to believe this in fact was a deliberate act and that two were cooperating in any meaningful sense. As may be obvious from the previous subsections, many of the data and observations are rather anecdotal and have not been collected with such a perspective in mind (excepting Apis, Dorylus, Eciton, and Oecophylla). Thus the crucial detail that would discern which subtasks exist is missing. This is especially true of old references, as in McCook (1879, 1909) above, in which researchers tended to anthropomorphize greatly. In essence, they were seeking to ascribe human-like behavior and qualities to social insects. The crucial issue of how we should rigorously and objectively test for teamwork is addressed in Section VII.

III. Other Animal Teams Cooperative hunting, in which several individuals work together to capture a prey that is usually then shared, occurs in a variety of vertebrate animal societies (reviewed in Ellis et al., 1983; Hector, 1986; and Bednarz, 1988, for raptors; and in Dugatkin, 1997, more generally; see also Boesch, 1994). Note that cooperative hunting does not necessarily involve a division of labor and therefore might only classify as groupwork. The following, however, do suggest a definite and necessary division of labor among concurrently-acting individuals, and hence may be considered examples of teams. But more detailed, dedicated experiments (as outlined in Section VII) are necessary before their status as true teams can be confirmed. A. Birds In African crowned eagles (Spizaetus coronatus) studied in Kibale Forest, Uganda, one bird will distract its prey (various species of monkeys) by flying in the midst of a monkey troop or sitting on a prominent perch where it is easily seen (Leland and Struhsaker, 1993). While most of the members of the troop flee, male monkeys will often jump up and down, vocalize, and perform other threatening displays. It is at this point, while certain males are preoccupied in display, that the bird’s mate swoops down

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and attempts to capture one of these males. The two subtasks thus appear to be ‘‘distraction’’ and ‘‘prey capture,’’ and each is an individual subtask. Whereas African crowned eagles employ a distract-and-ambush strategy, other birds employ a slightly different strategy—flush-andambush (Bednarz, 1988), in which one or more birds flush prey into the open where they are captured more easily by other team members. Aplomado falcons (Falco femoralis), which also hunt in pairs, are a case in point. Hector (1986, p. 251) states, ‘‘When attacking prey in trees, females tended to fly close to the ground then ascend abruptly into the inner branches. At this point, prey species, [3 species of dove], quickly took flight. The male falcons then dove and attempted mid-air captures. In ensuing chases, females left cover and followed the fleeing prey while males attacked with repeated dives and ascents.’’ These were probably not chance behavioral differences between the males and females because ‘‘different pairs consistently showed the same division of labor in hunts’’ (Hector, 1986, p. 254). Galapagos hawks (Buteo galapagoensis) and Harris hawks (Parabuteo unicinctus) exhibit similar behavior, but the attack may come from one or two individuals and the flushing is performed by a group (Bednarz, 1988; Faaborg and Bednarz, 1990). For instance, when Harris hawks are chasing black-tailed jackrabbits (Lepus californicus) and desert cottontails (Sylvilagus auduboni), the prey may seek refuge from its group of attackers in a bush. While the hawks surround the bush, one or two birds flushed the prey from the bush, where it is then pounced upon by the waiting teammates. Here then, one subtask, ‘‘surrounding bush,’’ is most often a group subtask whereas the ‘‘flushing prey’’ subtask may be an individual or sometimes a group subtask (Bednarz, 1988). B. Cetaceans In the ocean, the problem of catching prey is often not flushing it from hiding but concentrating it to a sufficiently high density so that the capture probability is significantly raised. When Alaskan humpback whales (Megaptera novaengliae) hunt Pacific herring (Clupea pallasi), they appear to work as a team in which there are two subtasks: prey herding (a group subtask) and bubble blowing (an individual subtask) (Ingebrigtsen, 1929; Jurasz and Jurasz, 1979; and Hain et al., 1982, all cited in Clapham, 2000). The pod initiates an attack by rushing the prey while issuing loud calls. The herring swim upwards in an attempt to escape but at the same time another whale, the bubble blower, swims in a circle above the school and deploys a curtain of air which both traps the prey and channels them to the surface, whereupon all the whales feed upon them. Interestingly, this strategy not


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only involves precise spatiotemporal coordination between the herders and bubble blower, but the bubble blower, vocalizer(s), and herders all appear to specialize in their subtasks (Sharpe, 2000, personal communication). Killer whales (Orcinus orca) also hunt cooperatively (Martinez and Klinghammer, 1970; Simila¨ and Ugarte, 1993; Baird and Dill, 1995; Baird, 2000). In one attack on a Dall’s porpoise reported by Baird and Dill (1995, p. 1306), ‘‘two whales alternately engaged the porpoise in a high speed chase.’’ Presumably, the two concurrent subtasks ‘‘chase’’ and ‘‘rest’’ were necessary to catch this fast-swimming prey (however, see Section VII.A). Baird and Dill (1995) also report several cases in which harbor seals (Phoca vitulina) hid from killer whales in underwater crevices and caves. To prevent the prey’s escape while the whales surfaced for air, the whales seemingly coordinated their time below water so that at least one whale was always guarding the prey. Baird and Dill (1995) also report several cases in which female whales would attack seals while adult males prolonged their dive, possibly to prevent the prey’s escape from below. Finally, Baird (2000, p. 142) cites Guinet’s (1992) study in the Crozet Archipelago in which ‘‘individuals maintained specific foraging positions relative to other individuals, both within and between years and between different bays.’’ Bottlenose dolphins also exhibit division of labor when hunting. Wu¨rsig (1986) cites Tayler and Saaymen’s (1972) study in which some bottlenose dolphins (Tursiops aduncus) herded fish to shore while others prevented escape. Wu¨rsig (1986) himself reports a case in which a group of five bottlenose dolphins coordinated their attack so that three offshore and two nearshore dolphins arrived at the prey synchronously. Finally, Bel’kovich et al. (1998) provide quantitative data on the frequency of what they term the ‘‘wall method’’ in which groups of dolphins drive prey towards the shore or towards one or more other individuals that are waiting. Dolphins sometimes also form alliances of two or three males to control the movement of females. When recapturing a fleeing female, ‘‘rather than chasing directly behind the female, the males often angled off to either side, effectively cutting the distance if she changed direction.’’ (Connor et al., 1992, p. 987). Interestingly, fish may also employ similar cooperative strategies when they hunt— specifically yellowtails (Serriola lalanderi) attacking jack mackerel (Trachurus symmetricus) and Cortez grunts (Lythrulon flaviguttatum) (Schmitt and Strand, 1982 cited in Wu¨rsig, 1986, and Dugatkin, 1997). C. Carnivores Griffin (1984, 1992) describes a hunt by lionesses (Panthera leo) that he observed in Kenya that appeared to involve teamwork. Five lionesses were hunting wildebeest (Connochaetes taurinus) that had separated into two

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groups. Two lionesses sat in conspicuous positions atop two mounds but posed no threat to the prey while, without being seen, a third lioness slinked along a ditch so as to position herself between the two herds. A fourth lioness rushed out of the forest towards one of the herds, which charged towards the other herd and the waiting, hidden fifth lioness. As the herd jumped the ditch, this lioness caught her prey, which was then shared among the lionesses. Although not conclusive proof of teamwork, it certainly has the appearance of an intentional coordination (Griffin, 1984) and a successful strategy involving division of labor among the lionesses. Similarly, Alcock (1979, p. 320) reports that ‘‘sometimes a lioness or two will leave the other members of a group lying in ambush. They will then circle conspicuously around a herd of game animals and drive them back towards their fellow ambushers.’’ Most significant, however, is Stander’s (1992) study of lioness hunts in Namibia. He was able to recognize individual lionesses through their markings, tags, and radio transmitters. He found that some individuals habitually took up the same relative position in different hunts; that is, some individuals appeared to be ‘‘wingers,’’ individuals who always tended to go around the prey and approach it from the front or side, while others act repeatedly as ‘‘centers,’’ individuals who habitually chased prey directly from behind. Teamwork in capturing young animals, in spite of their mothers’ best efforts to protect them, may occur with both jackals (Canis aureus) and hyenas (Crocuta crocuta); one individual distracts the mother while another captures the youngster (S. Harris, personal communication). Relay running, as in the aforementioned killer whales, is known in wolves (Canis lupus; Mech, 1970, pp. 230–231) and also in African wild dogs (Lycaon pictus; McFarland, 1985). Additionally, in the latter species, ‘‘a dog at the rear sometimes will cut corners in an attempt to head off prey’’ during a chase (McFarland, 1985, pp. 136–137). It is worth stressing that such a relay strategy, in which one or more individuals can somehow rest, only works if the prey’s path is non-linear and there are corners to cut. Finally, Godwin and Johns (2002) describe a novel reason for team formation in carnivores: defending captured prey from interlopers of other species. They witnessed two African wild dogs working together to protect their impala kill from a hyena; while one dog approached the hyena from the front, the other dog darted in and bit the hyena on the rump. D. Primates Highly cooperative and coordinated hunting in chimpanzees (Pan troglodytes) has been observed at Gombe National Park, Tanzania, and more frequently in the Taı¨ National Park, Ivory Coast (Boesch, 1994a,b;


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Stanford, 1999). In both cases, one or more individuals act as drivers, forcing the prey towards waiting teammates. For instance, Boesch (1994a; p. 1143) reports, ‘‘I once saw Frodo slowly driving the colobus down the slope in a region of high forest, while Beethoven and Prof chased them by climbing up under their line of retreat, whereas Evered, looking up at this progression in the trees, ran fast on the ground to get ahead of their advance and climbed into a tree into their path. As at Taı¨, the oldest male was taking up the more demanding role.’’ These chimpanzees appear to use facultative hunting strategies. When trees are short the hunting chimpanzees are more opportunistic, while when trees are tall ‘‘they adopt a more planned and collaborative hunting strategy because red colobus monkeys maintain larger distances from them’’ (Boesch, 1994a). Primates may form teams for other reasons. In a much-cited example of male coalitions in olive baboons (Papio anubis), Packer (1977) describes how two lower-ranking males will collaborate to gain access to estrous females. The troop’s dominant male usually escorts such females. One lowranking male keeps the alpha male busy by causing a fight while the other male goes off with the female. Later, the males switch subtasks. This is clearly an instance of a team. Both subtasks, ‘‘keeping the dominant male occupied’’ and ‘‘mating with the female,’’ must be performed concurrently, with the task being ‘‘to achieve a mating for one of the members of the team.’’

IV. Robot Teams As in the sociobiology literature, definitions of teams and teamwork in artificial intelligence and multirobot systems literature are scarce. Hexmoor and Beavers (2001) state that ‘‘to our knowledge all multi-robot experiments use the term team loosely as multiple robots that collectively perform a task and no analysis is offered.’’ Indeed, here we attempt such an analysis. Singh (1998, p. 303), however, does provide a more concrete team definition: ‘‘Multiagent systems that are viewed as having different members playing specific roles and usually cooperating to achieve some higher end.’’ Thus, like that of animal societies (Sections II and III), a team consists of two or more individuals (‘‘multiagent systems’’), involves division of labor (‘‘playing specific roles’’), and has some mutual goal (‘‘cooperating to achieve some higher end’’). Hexmoor and Beavers (2001) also recognize that team members ‘‘share a joint persistent goal’’ and further add that ‘‘the team persists so long as the achievement goal persists,’’ an important issue that is developed later (Sections V.B and IX). Interestingly, Singh (1998, p. 303) recognizes that a team may contain components which themselves are teams: ‘‘When a team is opened up with

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the design stance, we find not mere mechanisms, but other agents, some of which may be teams.’’ This is another a conclusion at which Anderson et al. (2001) arrive in their analysis. Unfortunately, the studies by Singh (1998) and Hexmoor and Beaver (2001) are atypical and it is clear that when one surveys multirobot literature the term ‘‘team’’ is indeed used loosely, ambiguously, and inconsistently. In their review, Cao et al. (1997, p. 17) state that one of the major aims for the emerging field of collective robotics is to develop ‘‘robust definitions and metrics for various forms of cooperation.’’ Our aim in this section, therefore, is to provide a critique of teams and teamwork in the multirobot literature (how have roboticists really used the term?) and to analyze whether our earlier task type classification scheme is relevant to cooperative, multirobot systems. In short, we ask whether the same fundamental issues of teamwork and groupwork identified in animal societies (Sections II and III) also apply to robots. A. Examples Many studies in multirobot systems involve collectively moving an object, usually a box but sometimes a light or furniture, to some target point (Kube and Zhang, 1994; Parker, 1994; Rus et al., 1995; Mataric´ et al., 1995; Brown and Jennings, 1995; reviewed by Cao et al., 1997). However, only some of these systems involve division of labor. Those without division of labor are thus groups rather than teams (sensu stricto Anderson and Franks, 2001; Section II.A). In some cases, a single individual can move the box. Hence, this is a task that could be an individual task—and is such a task when all but one of the robots breaks down—but the robots, when possible, tackle it as a group (Parker, 1999). In other cases, however, the box is so heavy that two or more robots must work in concert to move it (e.g., Kube et al., 1993). In this situation, it is inherently a group task for those particular robots (an important distinction clarified in Section VIII). We now wish to concentrate on illustrative examples that we consider to be teams. Gerkey and Mataric´ (2001) describe what they term a cooperative ‘‘pusher-watcher’’ scheme. Two robots, pushing at either end of one face of a box, must manipulate the object towards a goal. However, as the box is relatively large, they cannot see the goal. Therefore, a third robot is positioned between the goal and the box and issues orders to the other two robots in terms of their required relative velocities. (Gerkey and Mataric´ [2001], state that that they took inspiration from humans moving furniture.) This is clearly a team; there is a group subtask, ‘‘move box,’’ performed by the two pushers and an individual ‘‘direct movement’’ subtask performed by the watcher.


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In Brown and Jennings’s (1995) pusher/steerer scheme, there are just two robots, one on either side of the box. The robot nearest the goal is the only robot that knows the required path, and its sole job is to steer. The other robot’s role is to push both the box and the first robot. Brown and Jennings (1995) liken this to a car, the rear wheels providing the force to move the passenger compartment, while only the front wheels steer. In some runs, the two robots switched subtasks so that they could perform a parallel parking movement that allowed them to navigate sharper turns and narrower free spaces. Under Anderson and Franks’ (2001) definitions (Section II; Table I), this is clearly a team with two individual subtasks, ‘‘push’’ and ‘‘steer.’’ In an interesting twist (pun intended), rather than push an object, Donald et al. (1999) describe a cooperative robot system in which objects are pulled by a rope. Three robots are required. Two of the robots (A and B) are joined by a 5-m length of rope. Their role is to wrap the rope around the object so that it crosses itself once. Using the tension and friction of the rope, these two robots can then move in various ways to rotate or translate the object as desired. The tricky part is that in order for the rope to be crossed, one of the robots must ‘‘step’’ over the rope. However, when the rope is on the floor, there is the potential for it to slip under the object. Hence teamwork is required. The whole sequence is as follows. Robot A remains stationary. Robot B keeps the rope taut and circles almost completely around the object. Robot C, the only robot capable of grasping the rope, moves forward and holds the rope (leading directly to A) against the corner of the object. Robot A moves forward allowing B to step over the now-slack rope (which is still held against the object by C). The rope is made taut again and robot C lets go. Here there are two main subtasks—an individual ‘‘grasping’’ subtask (performed by C) and a team subtask involving two individual subtasks: ‘‘wrapping rope’’ (performed by B) and ‘‘tension manipulation’’ (performed by A). Box manipulation is not the only area of cooperative, multiple robot systems that seems to involve teams; robots also play football (soccer) in teams, another large area of robotics research (Kitano et al., 1997; Balch, 1997). As in human football, a goalkeeper primarily protects the goal, while others in the team try to move the ball forward towards, and ideally into, the opponent’s goal. Here there is crucial division of labor, even if individuals may occasionally switch between subtasks (cf. our baseball example earlier, Section II.A). A final example (see also Section VII) includes exploration of a novel building with two robots, one mobile robot carrying a light and a second, stationary robot (with a camera) who interprets the building’s configuration from the shadows cast (Langer et al., 1995).

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B. Why Use Groups and Teams? Even though there is little consistency in the use of the term ‘‘team,’’ there is a very strong consensus and recognition of the benefits of when and why groups and teams are useful, more so than in other fields. Why design a group or team of robots to complete a task rather than a single, more complex robot? We should stress that the following reasons are general and applicable to teams in all fields. We find the following four major reasons for using groups and teams (Kube et al., 1993; Cao et al., 1997; Hexmoor and Beavers, 2001; Dudek et al., 2002): 1. Lack of Ability: A single individual may not have the capabilities to complete the task and thus requires help from another individual (e.g., Camponotus and Myrmicaria in Section II.C; see also Section VIII). An example is pushing boxes that are too heavy for an individual to move alone (Section IV.A). 2. Efficiency: A group or team may be able to complete the task more quickly, effectively, or efficiently than an individual; this is particularly so when the task is spatial. For instance, fire fighting may be more effective if a set of robots can space themselves around the fire (Kube et al., 1993). At the lowest payoff level, we may find that N individuals complete the task N times quicker than a single individual; consider a set of non-interacting robots collecting randomly-strewn trash (this may not, in fact, be a group or team at all, but several individuals working in series-parallel [sensu Oster and Wilson, 1978]). This may be useful if there is some time constraint for the task (e.g., to complete the task as quickly as possible or within a certain time frame) (a TIME_LIM task sensu Balch, 2002). At the next payoff level, interactions among individuals may generate superefficiency (cf. Eciton in Section II.D). For instance, interacting trash-collecting robots that actively avoid each other will tend to spread themselves across the area and complete the task more quickly than noninteracting robots (Balch and Arkin, 1994; Balch et al., 1995). At the highest payoff level, a team makes use of differences among individuals (known as heterogeneous systems in robotics), and members focus on the subtasks at which they are particularly adept. 3. Redundancy and Fault Tolerance: Groups and teams may be relatively fault-tolerant, especially in homogeneous systems with distributed control (Quinn et al., 2002). If a single, complex robot (rather than a group or team) fails, the task cannot be completed. When redundancy is built into the system, however, and this is


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especially true of groups, failure of individuals may immediately be compensated for by others. This could be particularly important in difficult terrain, for example, on the surface of Mars or in a minefield where some individuals are likely to fail or are very difficult to replace, or with unreliable equipment in general. In heterogeneous systems, for example, highly specialized teams involving individual subtasks and also slave/master systems, failure of a key individual (e.g., the watcher in Gerkey and Mataric´’s 2001 study, above) may mean failure of the whole system. 4. Cost: Individuals in a group or team may be simpler, and therefore cheaper, to design and produce than a single robot that must complete the whole task itself (Castano and Will, 2002). First, simple interactions among individuals with the right set of feedbacks may result in the desired group-level behavior. In this way, the complexity of the system is self-organized and emergent, and not within the individuals themselves (Franks et al., 1991; Bonabeau et al., 1997; Camazine et al., 2001; Anderson, 2002). Such systems are often scalable, robust, and constantly seeking new solutions (Kube and Bonabeau, 2000; Anderson and Bartholdi, 2001; Dudek et al., 2002). Second, the members of a specialized team may be easier and cheaper to design per se—compare the cost and design issues in a task-specialized screwdriver versus a generalist tool such as a Swiss-army penknife, which includes a screwdriver capability (McShea and Anderson, 2003). We conclude that we do find that the same issues of teamwork, such as number of individuals, division of labor, and concurrent action, do apply to multirobot systems. Our fundamental task types and their associated definitions can be used to classify and distinguish robot system behavior in a meaningful, logical, and consistent manner. Finally, roboticists have an especially clear understanding of the pros and cons of teamwork, lessons that other fields may use. Indeed, as Cao et al. (1997, p. 1) claim, ‘‘The constructive, synthetic approach inherent in cooperative mobile robots can possibly yield insights into fundamental problems in the social sciences (organization theory, economics, cognitive psychology) and life sciences (theoretical biology, animal ethology).’’

V. Human Teams We now turn our attention to human teams. Teamwork in human organizations has received enormous attention in recent years, and many authors suggest that a team-based architecture is the key to an efficient,

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adaptive modern day company (Katzenbach and Smith, 1993; Applebaum et al., 1999, and references therein). In this study, however, we focus on whether the notion of teamwork, as viewed by management theorists, matches that of biologists and roboticists. C. Anderson and E. McMillan (2003) recently examined the parallels between insect teams and self-organizing human teams. Here, we summarize and build upon their findings. A. What Constitutes Human Teamwork? Table III lists some team definitions from the management literature. A number of common attributes are apparent. First, a team consists of a small number of individuals, usually defined as ‘‘two or more.’’ Second, there is a strong notion that these individuals are interdependent and must coordinate their activities—thereby implicitly suggesting group or teamwork (sensu stricto Anderson and Franks, 2001). Third, the members of a team work together towards a common objective or goal. Larson and LaFasto’s (1989, p. 19) definition is probably the most succinct. A team has two or more people; it has a specific or recognizable goal to be obtained; and coordination of activity among the members is required for the attainment of the team goal or objective.

Larson and LaFasto (1989) further qualify their definition by excluding situations in which the team’s accomplishment is merely additive, the sum of individual matches and performance, as in a Davis Cup Tennis Match. (A doubles tennis match, however, in which a pair of players on one half of the court must work together to cover the court and return the ball would count as teamwork [Anderson and McMillan, 2003].) Thus, for Larson and LaFasto (1989), Katzenbach and Smith (1993), and perhaps Shonk (1982, 1992) too, a team is more than the sum of its parts and requires coordinated, cooperative action—in other words, like social insect and robot teams, human teams accomplish results that individual members working alone could not. The similarity between Anderson and Franks’ (2001) definition and these management-based definitions, particularly Larson and LaFasto’s, is striking to say the least. At this level of analysis, the fundamental issues of teamwork are similar in ants and humans, despite a 104 to 105 fold difference in average, individual brain volume (ants: Jaffe and Perez, 1989; humans: Milner, 1990). Of course, human teams do have other attributes that are not greatly relevant in ants and robots: the notion of mutual accountability, the notion of team identity, issues of trust, leadership and so on. However, such issues are not the major, common attributes of


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TABLE III Various Team Definitions from the Management Literature (Arranged Chronologically) 1. ‘‘A team is ‘two or more people who must coordinate their activities to accomplish a common goal’ [Plovnick et al., 1975]. The common goal and the required coordination make them a team. It is not enough for people to want to coordinate because it would be nice. Coordination must be required to accomplish the task in order to be a team [Shonk, 1982]’’ (Shonk, 1992, p. 1). 2. ‘‘A team has two or more people; it has a specific or recognizable goal to be attained; and coordination of activity among the members of the team is required for the attainment of the team goal or objective’’ (Larson and LaFasto, 1989, p. 19). 3. ‘‘A group of people is not a team. A team is a group of people with a high degree of interdependence geared toward the achievement of a goal or completion of a task’’ (Parker, 1990, p. 16). 4. ‘‘A team is two or more people working together to achieve common goals’’ (Mackay, 1993, p. 26). 5. ‘‘A team is a collection of individuals who exist within a larger social system such as an organization, who can be identified by themselves and others as a team, who are interdependent, and who perform tasks that affect other individuals and groups’’ (Stewart et al., 1999, p. 3 citing Guzzo and Dickson, 1996). 6. ‘‘A team is a small number of people with complementary skills who are committed to a common purpose, performance goals, and approach for which they hold themselves mutually accountable,’’ and that there is ‘‘the need for any team to produce something of incremental performance value that is more than the sum of each member’s efforts’’ (Katzenbach and Smith, 1993, pp. 45, 89).

teamwork as listed in the definitions in Table III. However, even in Anderson and McMillan’s (2003) more detailed analysis, which appears in Table IV, it is clear that most of their attributes are common. B. Self-Organizing Teams While most readers would probably expect some form of leadership in a human team, this is not always so. They may be self-organized (Stacey, 1996; McMillan-Parsons, 1999; McMillan, 2000; Anderson and McMillan, 2003). By this, we mean teams that are informal and temporary, form spontaneously around specific issues, and in which no member of the team has an organizational or leadership role. Consider the immediate, unplanned cooperation when friends, neighbours and family members help to excavate a trapped person after an earthquake; in a self-organized team most or all individuals make decisions and may ‘‘lead’’ spontaneously as circumstances dictate (see McMillan, 2000; McMillan-Parsons, 1999, for detailed management examples). Essentially, self-organized teams constitute a tight social network with adaptive, emergent properties. On an organizational and decision-making basis, rather than being hierarchical

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TABLE IV Comparison of Likely Attributes of Human and Insect Teams Team Attributes

Human Teams

Insect Teams

Definable membership of two or more Team consciousness or identity Common, overall purpose or goal Members interact, communicate, and influence each other Members have complementary skills and abilities Activity is coordinated Team has ability to act as one The members consider themselves mutually accountable There are performance goals Team members evaluate themselves Team evaluates itself There are emergent properties

Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

Yes No Yes Yes Yes Yes Yes No No Yes No Yes

After Anderson and Mcmillan, 2003.

and command-and-control driven, they are flat and decentralized. Acknowledging that these human teams are only a subset of human team diversity, we propose that self-organizing teams come closest to a truly common, fundamental team-type, equally applicable to social insects, robots, and humans. The way that human teams form is also instructive. They form in response to an issue or an activity that motivates people to take action and create an informal and temporary team (Stacey, 1996). The team would not exist without an impetus that was considered important and worthwhile. Significantly, Anderson and Franks (2001, p. 538) arrive at the same conclusion. ‘‘Teams in social insects only form in immediate response to the stimulus of a team task.’’ For instance, an encounter with a large forage item that cannot be moved alone or the need for an urgent nest repair. Multirobot systems are only now starting to approach this stage of organizational flexibility and response; that is, that an individual robot may recognize a task that needs doing, that it requires cooperation, and that it has the ability to recruit assistance from other robots (T. Balch, personal communication). More research is needed in this area.

VI. Team Size Team size is an interesting aspect of teamwork. Multirobot systems typically involve less than 20 individuals (T. Balch, personal communication) but those that classify as teams (sensu stricto Anderson and Franks,


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2001) are much smaller, generally consisting of just two or three members. In management, companies may consist of hundreds of thousands of employees yet their teams also tend to be small, often with just 3 to 15 members (Peters and Waterman, 1982; Katzenbach and Smith, 1993; Anderson and McMillan, 2003). Similarly, although insect societies span more than five orders of magnitude, their teams are also small. (Teams, however, are typically expected and found only in larger insect societies; Anderson and McShea, 2001a.) Although no quantitative data exist, from the descriptive natural history (Section II) we predict the median team size is probably just two. There are examples of larger teams, for instance Pheidole and Pheidologeton intruder decapitation squads, and especially Oecophylla nest construction teams which may contain many tens of individuals in their pulling chains (group subtasks). However, what may be key is the number of functional components or subtasks (Table II)—just two or three in all known social insect and other animal teams. It would be very instructive to conduct a rigorous, quantitative comparison of team size in all these fields. Why should teams be so consistently small? Some companies claim teams of up to fifty members, but these are dismissed outright by Katzenbach and Smith (1993) on the basis that they do not contain the strong personal interaction and collaboration needed in a team. Also, human face-to-face conversations typically fragment into dyads and subgroups when there are more than four participants (Dunbar, 1996). In both cases, might individuals be less able, comfortable, or efficient in dealing with such a large social network when the individual links of that network require such close attention and cooperation? Thus, it is possible that teams are generally small because teamwork necessarily requires such close coordination of activity. The more heterogeneous the team and the more subtasks there are, the harder it is to form an effective team—hence the above comment about the number of functional components. (Another possibility is that it is easier for a selfish individual to ‘‘cheat’’ somehow in larger teams.) One strategy that may overcome such difficulties is to use the work itself or other cues as both a collation and filter of individual performance; that is, use ‘‘cooperation without communication’’ (Brown and Jennings, 1995; Cao et al., 1997; Dudek et al., 2002). For example, in Eciton prey retrieval or robot box-pushing teams, a new individual attempting to join the team may have little or no knowledge of the other members, but can assess their overall performance from the speed and motion of the prey item or box. Such ‘‘filtering,’’ though ‘‘the sensory capabilities of even the lower animals exceeds present robotic capabilities’’ (Parker, 1999), may allow roboticists to design much larger teams in the future.

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VII. Testing for Teamwork Given our numerous, proposed teams, how does one rigorously test whether a particular instance really is a team? In this section, we suggest how this might be achieved. First, however, using some borderline cases, we wish to illustrate some of the difficulties associated with such testing. A. Borderline Cases Tasks do not always fall neatly in the four different task types (Section I.A; Table I). Borderline cases exist. Given the complexities of animal behavior and the complex interrelationships between (sub)task types—for instance, that a team task may contain partitioned subtasks, and vice versa (Anderson and Franks, 2001)—perhaps this is inevitable. These borderline cases, however, can be instructive. Here, we deliberately seek out such cases to explore the conceptual boundaries of teamwork and provide some additional clarification as to what is, and is not, teamwork (at least from our perspective). 1. The boundary between task partitioning and teamwork Parker (1990: p. 17; his team definition appears in Table III) suggests that a relay race constitutes teamwork. However, we consider this a partitioned task under our definitions (Section I.A). After each of the first three runners in a relay has passed the baton to the next runner, their job is complete; they do not need to participate any longer and yet the task can still be completed successfully. It is thus clear that these subtasks are sequential. However, let us now consider a pair of killer whales, A and B, alternately chasing prey (Baird and Dill, 1995; Section III.C). If A tires out the prey first, and then lets B take over, if A never participates again in the chase or capture, this is likely a partitioned task. However, if A later takes over to give B a rest—and importantly, it is crucial that while B is chasing, A must rest to regain strength—then necessary concurrency is introduced and this unit can be called a team. Thus, one must pay careful attention to the specific subtasks when assessing whether cooperative activity truly classifies as teamwork. For a second example, consider the following: Jung et al. (1997) describe two robots cleaning a floor. One robot can sense and sweep fine particles into piles; the second robot can only sense the piles (not the fine particles) but is equipped with a vacuum cleaner. At first sight, one might consider that they are a cooperative team: One sweeps, one sucks, and because of the robots’ individual limitations, there is a necessary division of labor. However, they are not necessarily a team. Potentially, the sweeper could


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sweep the whole floor, leave the room and never return; later, the vacuumer would arrive to complete its subtask. Here the subtasks would be sequential and, overall, it would be a partitioned task. Consider instead a situation in which the room was very windy or involved some other disturbance that quickly dispersed the piles. If the piles had to be vacuumed very soon after being swept (see Balch, 2002) then this might classify as a team, the two robots having to work more closely together. Here, the basic subtasks in the two situations are unchanged, but the constraints (that the piles must be vacuumed quickly after being made) can switch the task type from partitioned to team. 2. The boundary between groupwork and teamwork In our example of cooperative hunting in humpback whales (Section III.B), one whale blew a bubble net while the others herded the prey and thus there is an unmistakable division of labor. However, situations are not always so clear. What are we to make of the following: ‘‘Wu¨rsig (1983) has described how dusky dolphins herd anchovies in the open ocean, diving and swimming at them from below and from the sides while vocalizing loudly. This results in a tight ball of anchovies; and the dolphins take turns swimming into the aggregation and seizing fish while others continue the herding from outside the ball’’ (Griffin, 1992, p. 61). Are the dolphins a group, each individual acting similarly and merely taking prey when it gets the chance, or would one consider this some form of division of labor? We suggest that they are not a team—removal of one individual will likely not have a great impact on the group behavior and success until, however, the density is so low that the fish may escape—but this is definitely a borderline case. Here is another borderline example. A set of autonomous robots must map the floorplan of a building. Each robot does a random walk through the building, and at regular intervals scans 360 to spot other robots; if it has a direct sightline to another robot, then that means that there must be open floor without any intervening walls, columns, or other features between the two (Dellaert et al., 2002). Over (very extensive) time, the set of recorded sightlines converges on the true floor plan—this procedure is termed diffusion mapping. One could argue that this is a group task because the algorithm relies on having multiple individuals and each individual’s task is identical: ‘‘to wander the building and sight other individuals.’’ Alternatively, one could reason that there are two separate subtasks, a case of ‘‘see and be seen,’’ and although ‘‘be seen’’ is a passive subtask, nevertheless it is a crucial, different subtask and the robots are a team. We take the latter stance, although again, it is not entirely clear. Interestingly, the robot’s sensors and

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range finders are not entirely accurate and any errors in an individual’s series of sightings are additive. As such, the set of sightings—the map—may ‘‘drift’’ over time. Therefore, Dellaert et al. (2002) include several static individuals that do not move and who act as reference points used to correct for any drift. With these individuals, there is no ambiguity; it is a team. B. Experimental Tests for Teamwork How then does one test for teamwork? We start with a lesson learned from an earlier section. Detection of superefficiency (although an a priori seemingly reasonable test) is not sufficient. We have mentioned teams as being ‘‘more than the sum of the parts’’ (Sections II.D and IV.A; also Table III). However, as mentioned in our robot section, a set of trashcollecting robots that actively avoids other robots will tend to disperse itself across the environment better than a set of non-interacting, randomly roaming robots and so may work especially effectively. Indeed, they may be superefficient (Balch and Arkin, 1994; Balch et al., 1995). Hence, somewhat surprisingly, we must consider that groups are potentially superefficient as well. Let us recapitulate Anderson and Franks’ (2001) team task definition: a task that necessarily requires multiple individuals to perform different subtasks concurrently. The ideal test, therefore, would be to conduct a series of experiments to show that members of the supposed team are performing different subtasks concurrently (i.e., that different individuals must do different things at the same time) and that this is essential for the task to be completed successfully. The first obvious and necessary step is careful observation of the potential team and individual activity. First, this will help identify possible subtasks and their interdependencies. Second, and more importantly, although observation can never positively prove the existence of teamwork, through the logic of falsifiability (Popper, 1959) it may conclusively disprove teamwork. For instance, one may observe that two concurrent subtasks are not always performed at the same time. Next, through careful experimentation, individuals would be removed (or somehow impaired), one at a time, from a large series of replicate putative teams. This is most easily achieved in robotics—the off switch— and is reported in the literature (e.g., Parker, 1999). Such individuals should exemplify all of the possible subtasks, and each type of putative team member should be removed from a suitably large series of replicated teams. The supposed subtasks individual team members are performing should be identified before they are removed. Ideally, quantitative and qualitative predictions should be made about how the missing individuals


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and their associated deleted subtasks will lead to the failure of the collective task. We should stress that removal of an individual and subsequent failure of the task is not sufficient per se to demonstrate teamwork. For example, imagine a box that requires the combined strength of at least 1.5 robots to move it. Two identical robots are moving the box with ease, but removal of one of them reduces the remaining effort sufficiently that the task fails, despite the fact that the two robots are a group. Ideally, the removed individual should be replaced or substituted by other individuals. This should enable all the necessary subtasks to be performed and should restore full team performance. In short, this method would involve the classical experimental techniques of vivisection and restoration. Thankfully, as we are dissecting the society and not individuals, it is easy, comprehensive, and painless (cf. sociotomy experiments [Lenoir, 1979a,b; Lachaud and Fresneau, 1987] or Wilson’s pseudomutant technique [1980a,b]). Such experiments are likely to be most difficult with vertebrates, as individuals might become alarmed by the removal of their workmate or may recognize that a particular individual is missing. Certain experiments to demonstrate teamwork have been conducted on army ants (Franks, 1986, 1987; Franks et al., 2001) and in some of these cases the team task was so strongly associated with particular prey items that a second team with properties similar to the initial one could be shown to form around the replaced items. Most intriguingly, we suspect that it may be possible in the near future to replace team members in certain animal societies with machines such as robots or even rather simple mechanical devices that can substitute for certain subtask performances. For instance, initial tests have begun on sugar cube-sized Alice robots with which ants directly interact (G. Theraulaz, personal communication; illustrated in Caprari et al., 2000 Fig. 4; Caprari et al., 2002). Less sophisticated is the possibility of adding tiny wheels to certain army ant prey items to substitute the back runner in their ‘‘penny farthing teams.’’ Such manipulations should help to clearly establish the form of the subtasks and hence the divisions of labor that may occur in animal teams. When such experiments are not possible, the putatively distinct subtasks of different team members should be quantified and classical bottom-up modeling (e.g., Camazine et al., 2001) should be performed to demonstrate that the successful performance of the collective task is the sum of the different performances and the interactions of the different members. Once again, this is most easily achieved in the field of robotics as most robotic experiments are first simulated before being tested with actual robots.

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In addition, especially in cases where full ablation, restoration, and experimental protocols cannot be achieved, it may be possible to get the putative team to operate in different controlled and treatment environments. For instance, one may be able to alter the relative ease, speed, or efficiency at which different subtasks can be performed, independent of the individuals tackling them (e.g., making a box more heavy in a robot ‘‘push-a-box’’ task). In this way, changes in team performance might be proved to result from the various subtask contributions of the different team members. C. Case Study As an example of the above testing procedures, we highlight Quinn et al.’s (2002) study of three homogeneous robots whose task was to remain within sensory range of each other and move a certain distance as a group/team in an obstacle-free environment. Each box-like robot is equipped with four infrared sensors and is initially placed in a random configuration within sensory range of each other. Thus, successful task completion consists of two sequential phases: reorienting into formation and then group translation. There was no particular required formation, simply one that worked—the study’s greater objective was to evolve a successful group level strategy using an evolutionary algorithm. The system was first evolved in silico and then implemented with real robots. Successful strategies evolved in which the robots moved together (Fig. 2), but were they acting as a team? They moved in a line, but had a leader/ follower scenario arisen as the authors had supposed? To demonstrate that each individual made some crucial but different contribution to the overall success, Quinn et al. (2002)—who had adopted Anderson and Franks’ (2001) team definition—removed individual robots and studied the effect upon the remaining two. Removal of the middle robot simply left the other two out of sensory range, while removal of the rear robot caused overall translation of the remaining pair to cease. They were not motionless, however, and entered a dynamically stable, cyclical pattern in which they oscillated (through rotation only) in anti-phase to one another. Replacement of the third robot soon restored group translation. Finally, removal of the front robot caused the middle robot to swivel around and soon thereafter enter the same cyclical pattern that resulted when the rear robot was removed. Quickly rotating the middle robot by 180 or moving the rear robot to the front caused the group to move in the opposite direction. This latter result thus demonstrates that roles are spatially determined and are not robot specific. Quinn et al. (2002) thus found that (1) the rear robot did not affect the


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Fig. 2. A three-member robot team travels in the direction of the arrow (courtesy Matt Quinn).

other two robots’ formation ability but was crucial for translation; (2) the middle robot moves forward in response to the rear robot’s presence, and hence the rear pair must persist for group translation; and (3) the front robot is crucial as well. They conclude that ‘‘these robots are working as [a] team, concurrently performing separate but complementary roles which, in combination, result in coordinated formation movement,’’ an analysis with which we agree.

VIII. Misconceptions About Teamwork In this section, drawing on the ideas and examples presented above, we will expose a number of misconceptions about teamwork. When dealing with such diverse teams and diverse social systems as we do in this chapter, it is inevitable that certain issues are particularly relevant in some systems but less so in others. Hence, the following clarification operates on a fundamental, almost philosophical, level. Our aim is to show that certain claims and ideas about teams, resulting from the perspective of one field (e.g., robotics) do not appear to be true when considering teams from another field (e.g., social insects). That is, they are not fundamentally true

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of teams in general; thus, essentially, the following is an attempt to spell out some of the more important, generic features of teams. Misconception #1: Groupwork is synonymous with teamwork. The most common misconception appears to be the assumption that concurrent activity among multiple individuals must be teamwork (e.g., Balch, 1997, called his trash collecting robots a team). This is not necessarily so. As we emphasize above, and as Katzenback and Smith (1993) stress in their much-cited book on management teams, it could just be groupwork—that is, necessarily involving concurrent activity, but not necessarily requiring division of labor (Section II.A). Indeed, it may simply be an example of series-parallel activity (Oster and Wilson, 1978), that is, individuals independently engaged in individual tasks, but just happening to be working simultaneously. Only when both concurrent activity of multiple individuals and a division of labor is required to complete a task successfully (for a certain set of specified individuals, see below), does activity class as teamwork. Misconception #2: Teamwork requires interindividual differences. Teamwork does not fundamentally require interindividual differences (e.g., contra Ho¨lldobler and Wilson, 1990). Our earlier example of the parcel-tying helper (Section II.A) was designed to illustrate this point; even your clone could have aided you. Despite the fact that teamwork involves a necessary division of labor, this does not imply that team members must be fundamentally different or specialized for their subtasks. However, selection pressures (natural or otherwise) in all the very diverse systems in which teamwork is employed may well favor interindividual differences and constancy in tackling those subtasks for which the individuals are particularly well-suited (Section II.A). Misconception #3: Teamwork requires individual recognition. Teamwork does not fundamentally require individual recognition (cf. Katzenbach and Smith, 1993). Again, our parcel-tying example illustrates this point (Section II.A). You do not need to know who this helper is, or ever interact with them again, for you to work together as a team. However, and this is an important distinction, in certain situations in which interindividual differences are crucial, to successfully in complete tasks you may need to recognize the skills in those potential team members (e.g., as members of a certain class of individuals but not necessarily as individuals). For instance, a group of Pheidole minors may have pinned down an intruder and need to recruit a major to decapitate the victim. If recruitment is an active process (rather than a major, by chance, encountering the immobilization activity), then the ants must recruit a major because only a major can complete the task. This then would require distinguishing between majors, who could complete the task, and minors, who could not.


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Misconception #4: Some tasks are inherently team tasks. As it stands, the assertion ‘‘Some tasks are inherently team tasks’’ is false (cf. Parker and Touzet, 2000). The type of task is only defined within the skills and constraints of the individuals tackling it, in addition to any external constraints (e.g., that the task must be completed within ten minutes; Balch, 2002). A tough task for some types of individuals, requiring cooperation and assistance, may be a trivial task to other, more highly skilled individuals (Balch, 2002). This is exemplified in the case of the large Camponotus brutus ants who could milk Caternautellia rugosa nymphs alone, whereas the smaller Myrmicaria opaciventris ants had to work cooperatively (Dejean et al., 2000; Section II.C). Therefore, what is needed to correct the above misconceived statement is a qualification; for instance, ‘‘Given the skill set of the individuals, 1, 2,. . ., n, and the constraints 1, 2,. . ., n, task X is necessarily a team task.’’ A second reason why the earlier assertion is wrong, at least from a philosophical rather than a practical standpoint, is that a task may be viewed as being of a different type when viewed from a different hierarchical level. This is best explained through an example. Consider an adult human unscrewing a jar of peanut butter. Our focal level is the whole organism level, the human. This jar-unscrewing task would usually be an individual task; he or she can open the jar without requiring help from other individuals. (This would not necessarily be true, for example, for weaker, young children though—another illustration of the point made in the previous paragraph.) However, shifting our focus down to the level of the hands, this is a team task, one hand holding the jar (subtask 1) while the other screws off the lid (subtask 2). This concept is not as abstract as it first sounds because it may be useful and important to view a group or team as a functional unit, a black box in the grander organizational scheme of the social entity. For instance, the head of a large company may wish or indeed need to view his or her organization solely from the perspective of interacting teams. From their perspective, to view it at a lower level may mean that they do not see ‘‘the wood for the trees.’’ To a personnel manager, however, perhaps only the individual level will suffice. In short, tasks may involve two sorts of hierarchy; first, that of the hierarchy of subtasks (e.g., a team within a team and so on), and second, that of different focal hierarchical levels. Only when the latter is changed, may the overall type change. Misconception #5: Efficient teamwork requires direct communication. As teamwork involves crucial concurrent action, activity must be coordinated appropriately and effectively. This implies that teamwork requires some form of information exchange among members. However, intermember communication need not be direct. There are at least two

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other alternatives for the mediation of communication—through the work in progress and through the environment. Certainly in social insects, and perhaps also in human and robotic teams, effective coordination and communication—through signals and cues (sensu Lloyd, 1983)—can be channeled through the work itself. This is known as stigmergy (Holland and Melhuish, 1999; Camazine et al., 2001). Consider the example earlier of Eciton and Dorylus ants forming teams to transport prey (Section II.D). To transport the prey at the standard retrieval speed, it seems that a close match is needed between the weight of the prey item and the combined weight (and therefore strengths) of the ants themselves. New individuals attempting to join a team can probably sense their contribution to the team by the change in speed of the prey item when they start to help. Likewise, individuals already transporting the item can likely sense the contribution of the new ant through the same mechanism. Thus, the speed of the prey item acts as a cue to the new individual as to whether its efforts are useful to the team (Franks, 1986). Roboticists cite a number of similar examples of ‘‘cooperation without communication,’’ such as coordinated box pushing (Brown and Jennings, 1995; Cao et al., 1997; Dudek et al., 2002). Consider a mountain rescue team whose members work concurrently to search for and then rescue some lost climber. The team may first break up into pairs, each of which searches a different section of the mountain. If for some reason direct communication (e.g., radio contact) is not possible among the pairs, they could still coordinate their activity through some signals left in the environment. For instance, to let others know that the search had been called off or to signal that a certain area had been checked, they could leave a colored flag or a pile of rocks in a conspicuous location. Provided that everyone knew the specific meaning of such signals, indirect communication could be effective among the team members. Misconception #6: Teams require a leader. Teams do not necessarily require a leader, contradicting the majority of the management literature. Many teams have leaders, or at least key individuals who play a crucial coordinating role, but many teams, including all of our social insect examples, do not. There are various reasons why a team may not have a leader. Indirect communication, as described above, may be sufficient or even preferable to coordinate activity, rather than a dedicated, specialist individual who leads the other team members. For instance, if the size of the team is large or the subtasks complex, it may be very difficult for a leader to collect and process the information about the team’s activities and then send out directives for the next step. Therefore, self-organized and hence leaderless teams (as considered in C. Anderson and E.


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McMillan, 2003) may be more effective. In addition, no member of a team may have the cognitive abilities, experience, or other skills required to lead. Either way, it is clear that leaderless teams do exist. As in the many definitions of teams within this article, however, the key issue of teams is not leadership but appropriate and effective coordination of the team members’ contributions, whether it occurs through leadership or not. Misconception #7: Team members need to know the state and goals of other members. One does not necessarily need to know the state or goal of other team members (contra Hexmoor and Beavers, 2001; see also Stone and Veloso, 2002, p. 44). As mentioned above (Misconception #5), the behavior, and additionally, the state, of an individual may be mediated through the task. For instance, in Brown and Jennings’ (1995) pusher/ steerer system, the state of the steerer (its wheel orientation) is effectively channeled through the box to the pusher. Hexmoor and Beavers (2001) also claim that, ‘‘agents with nontrivial ability and objectives who are not aware of other agents sharing their objectives cannot partner [for teamwork].’’ Nontrivial is obviously subjective, but ants, as far as we know, are not aware of other ants’ goals and intentions (in short, we believe that they lack a ‘‘theory of mind,’’ Premack and Woodruff, 1978), but do work as teams.

IX. Conclusions In this chapter we have considered what it means to work as a team in several fields, namely robotics, management, and sociobiology. We have detailed many new examples of teams, especially in sociobiology, and also demonstrated a number of generic lessons (chiefly in Sections VII and VIII). Through our various illustrative examples and the remarkably similar definitions across fields, we have elucidated some fundamental issues and concepts of teamwork. These are principally captured in our generally applicable definition of a team task: a task that necessarily requires multiple individuals to perform different subtasks simultaneously. As stated earlier, our approach focuses on the structure of tasks (Ratnieks and Anderson, 1999; Anderson et al., 2001; Anderson and Franks, 2002). As such, the question of why individuals may work as teams, especially the matter of common goals, is not relevant to our perspective, but nevertheless is an important issue of teamwork. Teams form to tackle a particular task; the team only exists as long as the goal exists (Plovnick et al., 1975; Stacey, 1996; Hexmoor and Beavers, 2001; Section V). However, more research is needed concerning the heuristics and algorithms by which teams form, operate, and disassemble.

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The proximate mechanisms can be very simple. For instance, for an Eciton worker deciding whether it should join a team, its rule may be ‘‘join so long as you increase the retrieval speed, but do not exceed the standard retrieval speed’’ (cf. Franks, 1986, and Franks et al., 2001; Anderson and McMillan, 2003). In this manner, individuals can easily self-select themselves for team membership without overseers and leaders, and without the need for predetermined roles (contra Belbin, 1981, 1983; Anderson and McMillan, 2003). In all fields, the degree of heterogeneity and the specialization of team members is an important facet of teamwork research. Significantly, how teams are assessed, rewarded, and selected can be crucial. If such selection operates at the individual level, then this tends to promote homogeneity, whereas heterogeneity is promoted if it operates at the team level (e.g., Balch, 1997, and Quinn et al., 2002, in robotics). Obviously, in most cases it is the new, team-level functionality absent at the individual level, that is desired and is why teams are principally used. This is most often voiced in the management literature with the following acronym: TEAM ¼ Together Everyone Achieves More. Constraints, both these placed upon the task and the individuals tackling it, play a crucial role in work organization. As stated earlier, no task is inherently a team task (Section VIII) unless it is qualified by the skills and limitations of a set of focal individuals. Even then, it is perfectly possible that the same set of individuals may tackle the task as individuals on some occasions and as a team on others (Anderson and Franks, 2001; Section VII.A). Teamwork not only allows a task to be completed successfully when a set of individuals working alone are doomed to fail (especially if the team is superefficient), but also may simply allow the task to be completed more quickly, effectively, or efficiently. Cao et al. (1997) cite the need for ‘‘robust definitions and metrics for various forms of cooperation’’ as a major challenge for the future of cooperative mobile robotics. Anderson et al. (2001) have begun progress on this by developing a new metric for quantifying the structural complexity of a task on an interval scale. Once the structure of the task has been found, as in the left-hand column of Table II, one point is assigned to each ‘‘individual’’ subtask, two points to each ‘‘group,’’ and three to each ‘‘partitioned’’ or ‘‘team’’ subtask; these are simply summed to give an overall complexity score for the task that can used to rank different tasks or teams (see Anderson et al., 2001 for more details). We suggest that our metric could easily be used in robotics, and although such a structuralist perspective is unusual in management, it could potentially be used here too (P. Saul, personal communication).


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We have attempted to unite seemingly disparate fields. We believe that this has been successful both within and across each field. Direct benefits arise because both similarities and differences are illuminating. We believe that we have been able to expose generic principles within human management, robotics, and especially animal behavior by focusing on the work itself rather than the workers. This approach focuses attention on the tactics and mechanisms of social interaction and later on the strategic benefits. Thus, both levels of explanation—the how and the why—come under scrutiny and are mutually benefitial.

X. Summary We have considered what it means to work as a team in several fields: robotics, management, and sociobiology. We have demonstrated that a single, generic definition of teamwork—a task that necessarily requires multiple individuals to perform different subtasks simultaneously—applies in vastly different social systems; in other words, we suggest that teamwork is a fundamental aspect of cooperative activity in highly social systems. We have detailed many new examples of teams, especially in non-human animals, and also demonstrated a number of generic lessons about teams, especially in our sections in which we draw attention to a number of misconceptions about teamwork (Section VIII) and in which we specify how one objectively and rigorously tests for teamwork and distinguishes it from related phenomena such as groupwork (Section VII). Acknowledgments We thank Tucker Balch, Peter Godwin, Stephen Harris, Peter Neumann, Scott Powell, Matt Quinn, Tim Roper, Peter Saul, Peter Slater, and an anonymous referee for their help and suggestions during the preparation of this manuscript. We also thank Alain Dejean, Turid Ho¨lldobler-Forsyth, and Matt Quinn for permission to publish the drawings and photographs that appear in our figures.

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The ‘‘Mute’’ Sex Revisited: Vocal Production and Perception Learning in Female Songbirds Katharina Riebel behavioural biology institute of biology leiden university leiden, the netherlands

I. Introduction In almost all songbird species studied males sing, but differences in female song range from species where females have never been observed to sing to those where females sing as much as males. In male songbirds, song functions both as a territorial signal and a mate-attracting signal (Catchpole and Slater, 1995), and thus song is under sexual selection through male-male competition and female choice (Andersson, 1994). In the majority of species studied, males have been described as the vocally displaying, females the choosing sex. All the true songbirds (oscines), which comprise about half of the extant bird species, acquire at least part of their song by imitation (Catchpole and Slater, 1995). They are, by far, the best studied taxon among those documented to be vocal learners (Janik and Slater, 1997). However, a closer inspection of the literature shows that it has almost exclusively addressed the subject of vocal learning in male oscines. For example, the absence of the subject of female vocal learning is striking in all the most recent comprehensive reviews on bird song (Kroodsma and Miller 1982; 1996; Catchpole and Slater, 1995). While it is undisputed that many species show clear sex differences in song usage, vocal learning in female songbirds has been so little studied that a sex difference in vocal learning is less certain. Much of bird song research effort has been biased towards temperate zone species where female song is supposed to be rare compared to the tropics (Kroodsma et al., 1996) or to Australia (Robinson, 1949). However, this view has also changed recently. Female song in temperate zones might be rare in terms of absolute time spent singing, but in almost all of the more intensively 49 Copyright 2003, Elsevier Inc. All rights reserved. 0065-3454/03 $35.00

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studied species, females are reported to sing at least occasionally (reviews and references, e.g., Nice, 1943; Ringleben, 1982; Ritchison, 1983a; Langmore, 1998). Recent observational and experimental studies have revised the notion that ‘‘mute’’ females occasionally produce functionless song when in hormonal disbalance, and a number of hypotheses have been brought forward regarding the possible function of female song (reviews in Ritchison, 1983a; Langmore, 1998). This recent interest in female song has also revealed that its acquisition is poorly understood. For almost all species where both sexes sing it is unclear whether and how females learn their songs and whether they learn the same way as males do. A thorough understanding of the behavioral sex differences is paramount to studying the covarying neurophysiology and anatomy, but it is also necessary to understand the intricate interplay in gene-culture coevolutionary processes. With a culturally transmitted mating signal, the question arises of the extent to which cultural transmission in the actively advertising sex is paralleled in the choosing one. Song is an important factor in female choice, with different song attributes varying in their relative importance across species (Andersson, 1994; Catchpole and Slater, 1995; Searcy and Yasukawa, 1996). Given that songs are culturally transmitted, perception of oscine vocalizations, like their production, should show some developmental plasticity. Learning processes on the receiver’s side might be essential to the dynamics of a communication system relying on culturally transmitted signals. Evidence is accumulating that female preferences for specific variants of conspecific acoustic signals are indeed greatly influenced by learning. The fact that song is often sexually dimorphic offers the unique opportunity to disentangle production from perception learning and to identify specialized adaptations of the brain. This is of great interest from a neuroethological point of view, especially to those focusing on mechanisms of learning and memory (Nottebohm et al., 1990; MacDougall-Shackleton and Ball, 1999; Bolhuis and Eda-Fujiwara, 2003). However, there has also been a recent surge of interest into perception learning from those with a more functionally and evolutionary orientated approach to behavior. While learning processes have now been acknowledged to contribute to variation between males, several authors have recently stressed that imprinting-like processes could play a far more important role in forming female preference than previously assumed (Owens et al., 1999; ten Cate and Vos, 1999). Developmental influences on female preferences are little understood, but have been identified as important sources for within-population variation in female preference (Jennions and Petrie, 1997). Therefore, an important first step is to map the distribution and extent of its occurrence.

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It seems timely to review what is currently known on how learning processes influence female songbird perception, as well as the extent to which females learn their song and calls. This may provide a starting point for a more informed discussion on how earlier consideration of sex differences in vocal learning might have been at least partly confounded with sex differences in vocal performance. In addition, I hope to provide enough evidence for auditory perception learning in female songbirds to stimulate more research into receiver learning, as mating decisions exert selection pressures that are likely to have played an important role both in origin and maintenance of vocal learning.

II. Vocal Perception Learning in Female Songbirds Song is often addressed toward potential mates (Kroodsma and Byers, 1991). There is now ample evidence that male song influences female choices (reviewed in Searcy and Yasukawa, 1996) and there is a lot to choose among. In many species, males have repertoires and so sing more than one variant of the species-specific song. In repertoire species, although birds may share song types, no two individual vocal repertoires may be the same. Males will also differ in how much they sing and the way they sing (e.g., at a fast or slow song rate). Across a great number of species the categories of variation identified so far as most relevant for females are versatility, performance aspects such as song rate, and the population of origin (Searcy and Yasukawa, 1996; Searcy and Nowicki, 2000). As a consequence of cultural transmission in male song in oscine species, song tends to be highly variant across individuals, but also between different geographic locations (e.g., Marler and Tamura, 1964; Mundinger, 1982; Slater et al., 1984). Female preferences for local song variants could result in prezygotic mating barriers, which has spawned a great research interest into testing female song preferences (reviewed in Baker and Cunningham, 1985; Searcy and Yasukawa, 1996). However, with the first evidence that female song preferences might be at least partly learned (Miller, 1979b; Clayton, 1988), it became apparent that the extent of song preference learning and its timing (e.g., pre- or post-dispersal) have to be understood, because this will have a strong influence on whether learning could reinforce or break down separation between populations. However, learning to prefer (or avoid) songs of the local population are not the only way learning could influence female preference. It will become apparent later that learning also influences preferences for specific song variants within, rather than between populations and that it is shaping perception beyond the preferences for specific song types. The following sections

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will describe some of these studies in more detail. A summary is given in Table I. A. Recognition In the study of perception, the two terms ‘‘preference’’ and ‘‘recognition’’ are often used interchangeably, even though they do not mean the same thing. In the context of mating signals, for example, the process of recognition would result in the identification of a potential mate, while preference refers to a choice between several such potential mates (for discussion see Ryan and Rand, 1993). However, further confusion is rising because recognition is also used in the context of learning to recognize a specific vocalization (e.g., in the context of social recognition learning or a mate’s or neighbor’s song, Wiley et al., 1991; Lind et al., 1996; Lampe and Slagsvold, 1998; O’Loghlen and Beecher, 1999) or simply in the context of an operant discrimination task (e.g., Cynx and Nottebohm, 1992). This section will refer to learning processes that influence what is classified or recognized to belong to the species or population specific vocalizations (‘‘recognition’’ sensu Ryan and Rand, 1993). It is well documented that unlearned sensory biases predispose male songbirds to learn speciesspecific song (Thorpe, 1958; Marler, 1970) or even specific geographic variants of it (Nelson, 2000). This might be why recognition learning has received relatively less attention than preference learning in the context of song perception, as similar unlearned biases for the species song seem to exist in female songbirds. Isolation-reared female zebra finches (Taeniopygia guttata) preferred zebra finch over heterospecific songs when given the choice in an operant task (Braaten and Reynolds, 1999). Nestling white-crowned sparrows (Zonotrichia leucophrys) reacted more to speciesspecific song than to any other test sound (Whaling et al., 1997). Likewise, females of a number of different species reared without song exposure have been found to react with more copulation solicitation displays to conspecific than heterospecific song (e.g., King and West, 1983b; Nagle and Kreutzer, 1997b). At first this might suggest that learning does not play a role in species recognition in female songbirds. However, this conclusion is premature. In Darwin’s finches (Geospiza spp.), song is culturally transmitted along paternal lines. In some species, both sexes hybridize frequently and female hybrids mated assortatively according to paternal song, either by mating with other hybrids or by backcrossing to the species represented by the paternal song (Grant and Grant, 1997a; 1997b). Another recent example in a female brood parasite suggests that perceptual learning might even lead to a combined mate and host recognition. In an aviary study with brood-parasitic indigobirds (Vidua chalybeata), using a traditional and a new experimental

TABLE I Influence of Early Exposure on Female Song Preferences Species

Common name

Test

Parus major

Great tit

Mate choice

Emberiza calandra

Corn bunting

Mate choice

Melospiza georgiana

Swamp sparrow

CSDþe

Zonotrichia leucophrys Z. l. nutalli

White-crowned sparrow Nutall’s w.-c. s.

CSDþe

53

Mate choice Z. l. oriantha

Z. l. oriantha, gambelii

Montane w.-c. s.

CSDþe Mate choice

Montane w.-c. s.

CSDþe

Montane w.-c. s.

Mate choice

Gambel’s w.-c. s.

Various

Preference

Effect

Source

Mates’ songs similar to fathers’ songs Chance matching between mates’ and fathers’ songs Songs with natal syntax preferred independent of early tutoring

þ

McGregor and Krebs, 1982 McGregor et al., 1988

Natal dialect tutor (< day 50) vs. alien (tutoring > day 50)b Tutor (only natal!) dialect vs. aliena Females’ songs (T-implants) like their mates’ songs Tutor (only natal!) dialect vs. aliena Females’ songs (T-implants) unlike their mates’ songs 2nd year song preference for natal dialect weakened in females exposed to alien dialect during 1st breeding season Not assortative to father’s song, pref. change across years Females from mixed dialect area – no clear relationship between T-induced own song, mate’s song and CSD’s

þ?

Casey and Baker, 1992

þ? þ

Baker, 1983 Tomback and Baker, 1984

þ?

Baker et al., 1981, 1982 Baptista and Morton, 1982

Balaban, 1988

MacDougall-Shackleton et al., 2001

Chilton et al., 1990 Chilton and Lein, 1996

(continued)

TABLE I (continued) Species

Common name

Moluthrus a. ater

Brown-headed cowbird

Test CSD CSD CSD Mate choice

Moluthrus a. artemisiae

Serinus canaria

54

Canary, domestic stock

CSD CSD

Fringilla coelebs Geospiza spec.

Chaffinch Darwin’s finches

Operant Mate choice Mate choice Mate choice

G. fortis Cardinalis cardinalis Taeniopygia guttata T.g. guttata þ castanotis

Northern cardinal Zebra finch

CSD Phonotaxis Phonotaxis CSDþe

Preference Male ‘‘tutor’’ M. a. obscurus vs. M. a. a. unfamiliar song Own dialect preferred over dialect heard after 60d Housing with different subspecies males changed preference Juveniles housed with M.a. ater preferred them as mates and passed this on to new generation naı¨ve M.a.artemisae Tutor over unfamiliar songs, domestic over wild en vice versa Domestic, but not wild song tutored, preferred domestic Tape tutor songs vs. unfamiliar Hybrids pair according to paternal species’ song Not mating assortatively to father’s song 2nd year females mate slightly disassortatively to father’s song Tutor songs vs. unfamiliar Father vs. unfamiliar Father vs. unfamiliar Foster subspecies song vs. own

Effect

Source West and King, 1980 King and West, 1983b

þ

King et al., 1986

þ

Freeberg, 1996, 1998

þ

Nagle and Kreutzer, 1997a,b

þ

Depraz et al., 2000

þ

Riebel and Slater, 1998 Grant and Grant, 1997a,b Millington and Price, 1985

þ

Grant and Grant, 1996

þ þ þ

Yamaguchi, 1999 Miller, 1979b Clayton, 1988 Clayton, 1990

Phonotaxis

T. guttata

Operant

55

Vidua chalybeata

Zebra Finch

Operant Operant

Z. f., wild stock Indigobird

Operant Mate choice

Preference for supernormal songs absent in isolates Tutored but not untutored showed repeatable preferences Preference for father’s song Unfamiliar brothers tutored by father Non-related tutor from day 35–90 Assortative mating according to females’ host species

þ

Neubauer, 1999

þ

Riebel, 2000

þ

Riebel et al., 2002 Riebel and Smallegange, 2003 Riebel et al., in prep. Payne et al., 2000

þ þ

CSD: Copulation solicitation displays during song playback (CSD e: with estradiol implants). a Only local dialect as tutorsong, females caught 7–10 days after fledging, begin and end of tutoring period not given, control with unfamiliar song as tutor missing. b This could also be seen as an unlearned bias: evidence for learning unclear as fledglings (10–50d) exposed to home dialect first, followed later (50–90d) by alien song. þ effect on preference, no effect observed.

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KATHARINA RIEBEL

host species, females preferred males raised by and singing like their respective host species, as well as laying their eggs in the new host species’ nest (Payne et al., 2000). A number of examples in the following sections will also illustrate that learning processes resulting from early song exposure might change perception of within and between population song variation, which in some cases suggests not only an effect on female preference but also on recognition.

B. Song Preferences 1. Geographic Song Variation When looking for learned female preferences for local over alien song variants, studies have to control for the pre-existing biases mentioned above. Ideally, several groups of females of similar genetic background should experience different songs when young. As adults they should be tested with both their native and their tutored dialects, and test songs should be different from the tutor songs to avoid testing a preference for familiar over unfamiliar songs (Section II.B.2). In a study using these criteria, Balaban (1988) tutored hand-reared fledglings from two populations of swamp sparrows (Melospiza georgiana) with different syllable syntax. Tape-tutored males learned to sing either syntax from a tape tutor, whereas females showed more copulation solicitation displays (CSDs) to songs with syntax of their natal population irrespective of their tape tutoring experience. This study thus identified a pre-existing bias that, at least with the chosen tutoring regime, showed no developmental plasticity. However, the intricate interplay between unlearned sensory biases and acquired preferences is often difficult to disentangle in a single experiment. Female cowbirds (Molothrus a. ater) reared in acoustic isolation reacted as adults with more copulation solicitation displays to male song of their own subspecies than to that of an alien one (King and West, 1983b). This was at first interpreted as evidence for a closed developmental program, but great plasticity in female song preference and the male song learning process was discovered subsequently. First, male song acquisition is greatly influenced by females behaviorally reinforcing the performance and retention of particular elements (King and West, 1983a; Smith et al., 2000). Second, females’ preferences and males’ song learning of a particular subspecies’ song did not depend on genetic background, but instead on upbringing. They could be ‘‘encultured’’ depending on whether they were raised by males and females of the same or a different subspecies, or even by second generation crossculturally raised individuals (Freeberg, 1996, 1998). Although the latter studies concentrated on


57

females’ mate choice rather than song preferences only, previous studies had shown that female cowbird song preferences and mate choices corresponded (West et al., 1981) and that males’ songs in this study had differed, like female mate choice, according to cultural, not genetic, background (Freeberg et al., 2001), making this some very compelling, albeit indirect, evidence for learned song preferences. In most populations of the white-crowned sparrow, males sing only one song type that is shared between all individuals in a particular location. Where there is a clear boundary that delineates two populations, each with a particular song type, the term ‘‘dialect’’ is perhaps most often and unambiguously used. However, different authors have used different definitions of this term (reviewed in Mundinger, 1982; Baker and Cunningham, 1985; Catchpole and Slater, 1995). In a number of studies on white-crowned sparrows, their own population dialects elicited more copulation solicitation displays from females than alien dialects and this has been suggested as being because females experienced this song when young (Baker et al., 1981, 1982; Baker, 1983; Casey and Baker, 1992). Unfortunately, all these studies had exclusively tutored with either the females’ own dialect (Baker et al., 1981; 1982) or an unfamiliar dialect after early first tutoring from their own dialect (Casey and Baker, 1992). None of these studies had an additional group receive the alien dialect as tutor song throughout, making this evidence unfortunately less clinching than it could have been, especially given that there is an own subspecies bias in this species for male song learning (Nelson, 2000). Unequivocal evidence for a learned preference for own subspecies song comes from zebra finches of the two subspecies from mainland Australia and the Lesser Sunda Islands, Taeniopygia g. guttata and T. g. castanotis. These populations differ in several macrostructural aspects of their songs. After crossfostering, and thus experiencing either their own or the other subspecies’’ song (Clayton, 1990), adult females gave more CSDs towards songs of whichever subspecies had fostered them. The crossfostering controlled for unlearned predispositions of their own population song and, by using unfamiliar songs rather than the tutor songs in the tests, it is clear that females must have reacted to the structural differences between songs, rather than to their familiarity (for preferences of familiar over unfamiliar songs, see II.B.2). Early exposure had clearly overridden any genetic predisposition at the subspecies level. Similarly, domestic strains of female canaries (Serinus canaria) prefer their own strain’s song to wild canary song and both normally reared and isolation reared females rarely reacted with copulation solicitation displays to wild canary song unless they had been tape-tutored with it when young (Nagle and Kreutzer, 1997a,b). However, in this study the songs with which females were tested had also

58

KATHARINA RIEBEL

been used in tutoring, which makes it possible that they reacted to a particular song because it was familiar (Section II.B.2) rather than generalizing its features to all other wild canary songs. 2. Within-Population Variation in Song The first experimental evidence that females’ perception of different song variants within the population can be influenced by social learning came from an experiment with female zebra finches. In a phonotaxis test with two loudspeakers playing back the father’s song and an unfamiliar song, females preferentially approached the loudspeaker playing back their father’s song (Miller, 1979b). Subsequent studies have placed song preference learning in this species beyond doubt: female zebra finches have now been shown to prefer the song they heard when young rather than unfamiliar songs, be it the father’s or foster father’s song (Miller, 1979b; Clayton, 1988; Riebel et al., 2002), the song of another live tutor (Clayton, 1988), or a song they heard from tape only (Riebel, 2000). They also prefer the song of a second tutor heard much later in life, without loosing the initially learned preference for the father’s or foster father’s song (Clayton, 1988). Likewise, females mated randomly to males in an experimental study preferentially approached their mate’s song rather than another male’s from a neighboring cage (Miller, 1979a). In an extensive experimental study with domesticated canaries, Nagle and Kreutzer (1997a,b) compared song preferences in different groups of adult females after they were raised with different song exposures. When tested with their respective tutor songs (domestic and wild canary, pine siskin (Carduelis spinus) songs) plus additional unfamiliar exemplars of each category, the canary and heterospecific tutored and the isolates preferred canary song. The wild song-tutored females were the only ones to prefer the wild-type tutor song over all other songs. One tutor group that had heard three different songs (one pine siskin, one domestic, and one wild canary song each) preferred both the familiar and unfamiliar domestic as well as the familiar (but not the unfamiliar) wild canary song. This experiment demonstrated a learned preference for specific song variants from a population or strain, but also that such sensory biases can be altered by learning and that several familiar songs can be preferred over unfamiliar ones. As with the zebra finch, additional songs could also become attractive later in life (here after tape-tutored and isolates had been paired and bred successfully in an aviary) without overwriting the preference for the original tutor songs (Nagle and Kreutzer, 1997a). In contrast, female chaffinches (Fringilla coelebs) did not prefer songs they had heard from a tape tutor to unfamiliar songs in an operant task


59

(Riebel and Slater, 1998). Tape-tutored female cardinals (Cardinalis cardinalis), although they had learned to produce the songs they heard from a tape tutor, did not show more CSDs for tutor versus unfamiliar songs (Yamaguchi, 1999). Although they did not provide evidence for learned preferences, neither of these studies showed conclusive evidence against either. First, an absence of preference does not demonstrate an absence of discrimination or memorization. Second, in both studies additional factors could have confounded the outcome. In the study with cardinals, only two unfamiliar song types were tested, whereas females had been exposed to 40 plus different tutor songs. In both studies, there was only one experimental treatment and no reciprocal group receiving the test songs of the first as tutor songs. Neither was there a comparison with untutored females, which might have shown different choices. Both species are repertoire species in which, despite there being song sharing within locations, song is not population specific. The tutored females might have learned to prefer general features shared by tutor and test songs of which relatively few different ones were used (only two unfamiliar song types for the cardinals, three for the chaffinches). 3. Father’s Song and Mate Choice A more indirect approach to testing learned song preferences is to record a father’s song in the field and to compare it to the songs of males chosen by his daughters in the subsequent spring. This approach assumes that a female’s father’s song is memorized to form a ‘‘preference’’ template. The prediction following from this is that females should mate assortatively with regard to song similarity between potential mates and their fathers. In a mixed-dialect population of white-crowned sparrows, Chilton et al. (1990) discovered no influence of the father’s song on female choice and also found the same females chose males singing different dialects in different years. Other comparisons between fathers and mates songs provided different results. In great tits (Parus major), females were found to be paired to males sharing more song types with their fathers than expected by chance (McGregor and Krebs, 1982). Assortative mating in relation to dialect was not found in female corn buntings (Emberiza calandra) (McGregor et al., 1988) or Darwin’s finches [Geospiza fortis (Millington and Price, 1985)]. However, in the latter, a more recent study provided evidence that second-year females avoided pairing with males singing songs like their fathers (Grant and Grant, 1996). On the within population level, learning thus led them to avoid rather than to prefer the father’s song. However, on a between-species level, recognition and preference of species-specific features seem to be learned from the father’s song. Hybrids (Geospiza spp.) mated assortatively with regard to paternal song, either by

60

KATHARINA RIEBEL

mating with other hybrids or by preferring to backcross to the species represented by the paternal song (Grant and Grant, 1997a,b). The patchy evidence from the field so far stresses that future studies need to identify from whom and when females learn which songs to prefer outside a laboratory context. However, laboratory studies might help identify when females learn (e.g., Riebel, 2003) or how exposure to several songs or tutors influences their preferences (Clayton, 1988; Nagle and Kreutzer, 1997a). Important in this context is to know whether females learn exclusively pre- or post-dispersal, or at both stages, and whether preference learning is purely dependent on timing and frequency of exposure or linked to social interactions. Some of the field studies might have provided non-conclusive evidence because they only considered the father’s song as a possible source for the acquisition of a preference template. While those studies showing positive (or negative) assortative mating with regard to song provide evidence for a learned preference, negative evidence cannot be interpreted as an absence of preference learning. Even where females choose apparently at random with regard to their father’s song, they still might have learned song preferences. If females learn from individuals other than their father, singing at their natal site or post-dispersal, studies that test for, and fail to find, assortative mating with regard to the father’s song cannot be interpreted as an absence of preference learning in general. It is also possible that females learn general population typical features but not necessarily to prefer specific songs within this range, but as a consequence of the learned preference will discriminate against songs outside this range, as has been demonstrated for example for population specific song features in the zebra finch (Clayton, 1990). C. Perceptual Fine Tuning Several very recent studies suggest that we might have focused too much on testing whether exposure to a particular song leads to a preference for it and thereby have overlooked other developmental consequences of early perceptual learning. Several examples suggest that early exposure to song is important for perceptual fine tuning. Isolation-reared zebra finches performed less well in operant auditory discrimination tasks (Sturdy et al., 2001). Adult female zebra finches tested several times with the same songs over several months showed repeatable song preferences in an operant task if they had had early exposure to a (taped) song, but not if they had been reared without exposure to male song (Riebel, 2000). In a study where both normally raised and acoustically isolated female zebra finches were tested for a preference for supernormal song length, the aviary or bird-room raised showed a preference for supernormal song length,


61

but not the females reared without exposure to songs. These females chose between playbacks of normal-length song and the supernormal songs at random (Neubauer, 1999). A possible interpretation of these results is that female zebra finches might have to learn about ‘‘average song length’’ to perceive unusually long songs as more attractive. Similarly, clear differences in song perception have been reported between female canaries reared without exposure to male song and aviary-reared females. Interestingly, in the canaries, early exposure to male song seemed to narrow or shift preferences for certain characteristics towards the experienced range. Isolation but not aviary-raised female canaries showed stronger preferences for a supernormal song (fast trill with fast frequency modulation over a wide frequency range). While the females that experienced song also generally preferred faster trills, they did not prefer the supernormal over the normal (Dra˘ga˘noiu et al., 2002). The authors interpret their results as indicating directional selection; a different way to read the results is that early learning might channel females’ perception towards the population range. The evidence is patchy as yet, but the extent to which learning helps to fine-tune a female’s perception and whether it leads towards narrowing or broadening of her adult preferences is surely a line of investigation worth pursuing in the future. D. Interaction Between Song Production and Perception? The question of whether there is an interaction between production and perception learning has received considerable attention as well as empirical support from studies in both humans and songbirds (Liberman et al., 1967; Nottebohm et al., 1990). Unclear here is whether production learning influences perception, or perception learning influences production, or the two are one and the same. A number of studies have addressed these questions in male songbirds by looking at the interaction between own song and perception, but they have rarely addressed whether it was a male’s own song or its similarity with the original tutor song heard early in life that was channeling perception. Little is known about possible interactions between song production and perception in singing female songbirds. A number of studies in the white-crowned sparrow (Baptista and Morton, 1982; Tomback and Baker, 1984) addressed the question of whether females actually chose their males according to dialect by comparing females’ own song to their respective mates’ songs, but have not found unequivocal results. Females mated assortatively in relation to song in one (Tomback and Baker, 1984) but not the other location (Baptista and Morton, 1982), as was also observed in a mixed dialect population where males and females sang one of two different types of

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KATHARINA RIEBEL

song (Chilton et al., 1990; Chilton and Lein, 1996). In the mixed dialect population, early exposure to several songs could have led to preference for all of them (see examples in Section II.B.2; e.g., Nagle and Kreutzer, 1997b). While this provides a possible explanation for the results in the mixed dialect area, it does not for the contradicting results from the two studies in pure dialect areas. However, it is currently unclear when and how females acquire their preferences in the wild. Females might not learn their songs from their fathers (Baptista and Morton, 1988) and might learn both pre- and post-dispersal, for example, as fledglings as well as during their first breeding season (e.g., MacDougall-Shackleton et al., 2001). It is also currently unclear whether the songs that females sing can be used to predict their preferences. If production and perception learning are indeed two different processes, a lack of consistent preferences for mates singing a female’s own song is not surprising. Some laboratory studies suggest that the two learning processes are not the same. Preference strength for the natal dialect was weaker in females that experienced exposure to non-natal dialect song in their first breeding season, but all females induced to sing with testosterone sang only natal dialect elements (MacDougall-Shackleton et al., 2001). Tape-tutored female cardinals displayed as frequently to songs they had learned to produce as to those they had also heard during tape tutoring but had not learned to sing (Yamaguchi, 1999). Female starlings (Sturnus vulgaris) showed more orientation movements towards those of their own songs that were also shared with a social mate (Hausberger et al., 1997). This assay does not necessarily demonstrate a preference, but the results demonstrate that songs falling into the category ‘‘own songs’’ can still be perceived differently. The strongest evidence for a dissociation of production and preference learning comes from zebra finches. Females do not produce song, but both males and females with the same auditory experiences as fledglings prefer songs to which they have been exposed at that stage equally strongly. Clayton (1988) found no sex differences when measuring the duration of approach towards a speaker playing back the father’s or another social tutor’s song. Riebel et al. (2002), when quantifying preference strength across siblings with an operant task, found male and female siblings to press keys triggering playbacks of the familiar father’s song over unfamiliar songs with equal frequency. Clearly, these questions need addressing in future studies. The study of female song preference learning provides the unique opportunity to compare perceptual learning in non-singing females with their male counterparts. As stressed by Ratcliffe and Otter (1996) in a recent review, our knowledge on possible sex differences in song perception is rather thin,


63

as studies testing males and females with the same test songs and in the same context are few and far between. I would add to this another caveat: No conclusions regarding a potential sex difference should be drawn where a subject’s ontogeny and the quality of song input during development are unknown.

III. Vocal Production Learning in Female Songbirds Bird vocalizations are traditionally divided into calls and songs. The categorization is based both on physical characteristics of the signal (calls are shorter and less complex than songs) and also on its function (see later). This distinction has sometimes caused confusion, but has still proven useful in describing vocal repertoires (for discussion see Catchpole and Slater, 1995). Generally, calls are described to be used by both sexes for communication all year round, whereas songs are more complex vocalizations used predominantly in the reproductive context. Songs have rightly been described as ‘‘acoustic peacocks’ tails’’ (Catchpole, 2000), and in most species, they are not only an acoustic ornament but also an acoustic armament. Important functions of song are resource defense, and competition over and attraction of mates, which are all typical ‘‘male functions’’ (Andersson, 1994). This might be one of the reasons why song has long been considered a mere epiphenomenon in females (Nice, 1943; Catchpole and Slater, 1995), and why song learning has rarely been studied systematically and experimentally in female songbirds. However, female song is now seen as an adaptive trait even in those species where it is only facultative (e.g., Ritchison 1983a; Langmore 1998, 2002). Given the omnipresence of vocal learning in oscine birds (Catchpole and Slater, 1995), it seems likely that in those oscine species where females have been reported to sing, females, like males, will have learned at least some aspects of their songs. However, this could be a premature conclusion, as there are undeniable sex differences both in the usage of song as well as in its form (e.g., male and female specific song in some of the duetting species). Thus, there might also be substantial sex differences in vocal learning abilities. I shall use the criteria outlined by Janik and Slater (1997; 2000) when reviewing those studies providing evidence for female song or call learning. I shall thereby leave out many studies where female song has been documented, but where unfortunately not enough information on either development or song sharing within the population is available to imply learning at this stage.

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A. Song Learning 1. Indirect Evidence From Male and Female Song Sharing In a number of species where females are observed to sing in the wild regularly, they have been found to share some of males’ learned song types (Table II). Starling repertoires, for example, are highly individual-specific. A field observation of a polygynous trio where the two females and the male shared almost all their whistle types with each other (including imitations of a number of heterospecific calls) makes compelling evidence for vocal learning (Hausberger and Black, 1991). Females of two subspecies of the white-crowned sparrow are regularly observed to sing in the wild. A detailed parametric analysis of the acoustic characteristics of female songs in Nutall’s white-crowned sparrows (Zonotrichia leucophrys nutalli) showed these to be of the local dialect and to match male song in the majority of the measured parameters. In montane white-crowned sparrows (Z. l. oriantha) this was even more the case, and the authors state that they could not distinguish females from males in the field (Baptista et al., 1993). Similar indirect evidence, although not always based on such detailed analysis, has been obtained for a number of other species from various families as listed in Table II. The literature survey also identified many more species with singing females. However, because there was not enough information on individual differences or song sharing to deduce learning, they are not listed in Table II (reviews and references in, e.g., Nice, 1943; Ringleben, 1982; Ritchison, 1983a; Langmore, 1998). 2. Impoverished Songs in Females Raised Without Song Models Ontogeny of female song has been studied little. As with studies of male song, experimentally manipulating the amount and kind of exposure during development and comparing the song of adults from different exposure regimes can provide unequivocal evidence of female song learning. Depriving young birds of exposure to adult conspecific vocalizations is a safe test for the importance of acoustic stimulation in the development of vocalizations, albeit not necessarily an indication for a crucial role of social learning processes (Janik and Slater, 1997, 2000). All studies in which adult songs of females deprived of exposure to adult conspecific song were analyzed, report impoverished song lacking either some of the fine detail, complex notes, or location-specific markers, for example, in cardinals (Lemon and Scott, 1966; Dittus and Lemon, 1969; Yamaguchi, 2001) or in white-crowned sparrows (Cunningham and Baker, 1983; Petrinovich, 1985; Baptista and Petrinovich, 1986; Petrinovich, 1988). While this is highly suggestive of learning, the lack of auditory stimulation

65


TABLE II Indirect or Observational Evidence for Female Song Learning (Females’ Ontogeny Unknown) Species

Common name

Red-shouldered Agelaius assimilis blackbird (formerly Cuban race (formerly: Cuban of A. phoeniceus) red-winged blackbird) Icterus galbula Northern oriole Dendroica petechia Yellow warbler Symplectes bicolor Forest weaver Ploceus bicolor sclateri Forest weaver Corvus corax Common raven Copsychus malabaricus Shama Erithacus rubecula European robin Prunella collaris Alpine accentor Cardinalis cardinalis Cardinal Pheucticus Black-headed grosbeak melanocephalus Troglodytes aedon House wren Uraeginthus bengalus Red-cheeked cordon-bleu Gymnorhina tibicen Australian magpie Zonotrichia leucophrys

White-crowned sparrow

Z. l. nutalli

Nutall’s w.-c. sparrow

Zonotrichia leucophrys Fringilla coelebs Emberiza citrinella Anthus campestris Carpodacus mexicanus Malurus splendens Torreornis inexpectata Psophodes olivaceus

White-crowned sparrow Chaffinch Yellowhammer Tawny pipit House finch Splendid fairy wren Zapata sparrow Eastern whipbird

Evidence

Source

A

Whittingham et al., 1992

A A, A A, B, C A, C C A E A A

Beletsky, 1982 Hobson and Sealy, 1990 Wickler and Seibt, 1980 Seibt et al., 2002 Gwinner and Kneutgen, 1963

A A

Hoelzel, 1986 Langmore et al., 1996 Halkin, 1997 Ritchison, 1983a,b 1985 Johnson and Kermott, 1990 Gahr and Gu¨ttinger, 1986

A, C, D

Brown et al., 1988a; Farabaugh et al., 1988 T (A, B) Konishi, 1965; Baker et al., 1982; Cunningham and Baker, 1983; Tomback and Baker, 1984; Chilton et al., 1990; Chilton and Lein, 1996 A Petrinovich and Baptista, 1984 B Baptista et al., 1993 T T (B) A* A A, (D?) A? B

Kling and Stevenson, 1977 Baker et al., 1987 Neuschulz, 1986 Mundinger, 1975 Payne et al., 1988 Morton and Gonzalez, 1982 Watson, 1969

A Female songs match male song or syllable types or A* individual song types matched between pairs. B Female songs of the local dialect. C Heterospecific mimicry. D Group living species: within-group sharing higher than between group sharing. E First year females have simpler songs than older females. T Song induced with testosterone implants.

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could also have delayed maturation processes or reduced the amount of motor practice (Nelson, 1997, 1998; Janik and Slater, 2000). However, the majority of these isolation experiments were conducted in combination with tutoring experiments where those females exposed to song copied the song types to which they were exposed when young (Table III and Section II.A.3). 3. Tutoring Experiments Raising young birds that originate from the same population, but varying the kind of acoustic exposure they receive during development, ideally by cross-fostering them, provides perhaps the most powerful and most unambiguous test for vocal learning. Above-average matching of song types between tutor and student leaves learning from the tutor the most parsimonious explanation, especially where unrelated live or tape tutors are used in a controlled environment. Aviary-raised female bullfinches (Pyrrhula pyrrhula) imitated aspects of their father’s song (Nicolai, 1959). Females also learned song motifs of their first mates, most dramatically illustrated by a female that started to sing canary song when she paired with a male singing canary song he had copied from his canary foster parents. In marsh tits (Parus palustris), females sing, although more rarely, as well as males and with a peak just after the young fledge. Both sexes of aviary-fledged young learned from both their parents as comparisons between their repertoires and transmission of elements unique to one parent showed (Rost, 1987). In an earlier tape tutoring experiment on the same species, hardly any of the elements played back had been copied (Becker, 1978). However, in the tape-tutored and isolation groups, group mates ended up sharing elements even though they originated from different nests. In contrast to Rost (1987), Becker (1978) describes the songs of the females as less complex and less stereotyped than those of their male siblings. Interestingly, this could be interpreted that female song might depend even more on learning as the songs of their male siblings (although they also had failed to imitate the songs from tape) were described not to differ too much from normal wild song. Studies on the white-crowned sparrow also illustrate how difficult it is at this stage to make comparisons about possible sex differences in song and song learning (see discussion in Section V). Female song recorded in the field corresponds to male song (Baptista et al., 1993). Hand-raised females sing song as impoverished as that of males when not exposed to conspecific song (Baptista and Petrinovich, 1986; Petrinovich and Baptista, 1987). However, in those studies where females and males were tutored from tape, males learned from tape tutors but females did not (e.g., Cunningham and Baker, 1983; Baptista and Petrinovich, 1986). Female canaries sing

TABLE III Female Song Learning – Developmental and Experimental Evidence Species

Common Name

Pyrrhula pyrrhula

Bullfinch

Zonotrichia leucophrys nutalli


Zonotrichia leucophrys

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Z. l. nutalli


Z. l. nutalli


Z. l. oriantha

Montane w.-c. s.

Parus palustris

Marsh tit

Gracula religiosa

Indian hill mynah

Evidence Some of father’s as well as (first) mate’s song copied Hand-reared tape-tutored females did not learn song types from first (before 50 days) or second (after 50d) tape tutor, occasional element copied, songs unlike wild caught adult females Tape and live tutoring after 50 days only, some learning from live tutor, one from heterospecific A. amandava T-induced song of lab-raised isolates highly impoverished, tape tutored with song of better quality but few specific elements copied Isolates impoverished song, one female copied tape tutor heard before day 50, 2 fledglings that of natal area, no learning after 50 days Female progeny of 3 fathers sang local dialect even if not father’s song Male and female chicks learn from each other (in related and unrelated fledgling groups) but not from tape tutor Females’ song as complex as males’, high song sharing between mates, equally extensive learning from both mother and father in both sexes Sharing of elements between females, aviary kept females copied from aviary companions

Source Nicolai, 1959 Cunningham and Baker, 1983

Baptista and Petrinovich, 1986

Petrinovich, 1985

Petrinovich, 1988

Baptista and Morton, 1988 Becker, 1978

Rost, 1987

Bertram, 1970

(continued)

TABLE III (continued) Species Sturnus vulgaris

Common Name Starling

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Laniarius funebris

Slate-colored boubou

Tiaris canora Gymnorhina tibicen Richmondena cardinalis

Cuban grassquit Australian magpie Cardinal

Corvus corax corax

Common raven

Corvus brachyrhynchos

Common crow

Ploceus bicolor sclateri

Forest weaver

Turdus merula

Blackbird

Evidence Heterospecific imitations English words and whistled songs by human caretaker Rearing regime (hand reared, parents, foster parents) influences adult song, element repertoire and sequencing Father, daughter, and son shared song motif Hand-reared female imitated human whistles Acoustic isolates with impoverished songs Non-local syllables copied from tape tutor Adult songs match tape tutor Hand-raised birds were observed to copy rare call from each other as well as to show heterospecific mimicry Group specific calls: individual repertoires change in new social group (i) captivity-bred birds only sang like their parents if housed with them, (ii) adult song was modified up until 24 months depending on cage mates, (iii) acoustic isolate copied whistled tune from her keeper Handreared female (after T-implants 1st summer), still learned new motifs during subsequent autumn after breeding successfully

Source Hausberger and Black, 1991; Hausberger et al., 1995b West et al., 1983 Wickler and Seibt, 1988; Wickler and Sonnenschein, 1989 Baptista, 1978 Brown et al., 1988a Lemon and Scott, 1966 Dittus and Lemon, 1969 Yamaguchi, 1999, 2001 Gwinner, 1964

Brown, 1985 Seibt et al., 2002

Thielcke and Thielcke, 1960


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post molt as much as males, and, while song output during the rest of the season is low in paired females, unpaired females can sing as much as and indistinguishably from males (Gu¨ttinger et al., 1988). While female song is less stereotyped on average, syllable repertoire size is equal and some females will sing songs as stereotyped and complex as males, others will after having received testosterone implants but without additional song exposure (Pesch and Gu¨ttinger, 1985; Gu¨ttinger et al., 1988). Interestingly, these implants do not seem to lead to masculinization in general, as these implanted females bred successfully immediately after termination of the treatment (e.g., in both canaries and blackbirds, see Thielcke and Thielcke, 1960; Gu¨ttinger and Weichel, 1989). Unequivocal evidence for vocal learning is provided where birds mimic heterospecific sounds in their individual repertoires. A hand-reared female starling imitated English words as well as parts of melodies whistled by her caregivers, which she integrated into her songs (West et al., 1983). Similarly, a female Australian magpie (Gymnorhina tibicen) imitated whistles from her human caregivers (Brown et al., 1988b). And there are a number of other mimicking species (see Table II) in which both males and females have been reported to copy heterospecific sounds, for example, ravens and shamas (Gwinner and Kneutgen, 1963; Gwinner, 1964), or starlings (Hausberger and Black, 1991). 4. Duetting Species Females of duetting species provide the earliest acknowledged examples of female song equaling male song both in form and function (reviewed in Thorpe, 1972; Kunkel, 1974; Farabaugh, 1982; Hall, in press). However, studies on song learning in duetting species are scarce. Many of them sing antiphonally, that is, specific non-overlapping song parts alternate between partners, and where this is the case sex roles seem to be consistent throughout the population (Thorpe, 1972). Where males and females consistently sing differently, they might acquire their songs in different ways. A laboratory study of slate-colored boubous (Laniarius funebris) showed that rearing conditions clearly influenced adult repertoires (Wickler and Seibt, 1988; Wickler and Sonnenschein, 1989). Four handreared birds housed without conspecific tutors, and with only heterospecifics in earshot, had some poorer versions of some of the elements observed in the wild, but also had learned from each other and had developed matching element repertoires. In a group reared by adult conspecifics, both males and females learned elements from each other or the adults they were housed with. Two females learned exclusively from other females, while the males mostly learned from males. This led the

TABLE IV Evidence for Female Call Learning Species

Common Name

Carduelis spinus

European siskin

Carduelis flavirostris Loxia curvirostra

Twite Red crossbill

Parus atricapillus

Black-capped chickadee

Parus montanus

Willow tit

Euphonia laniirostris Campylorhynchus nuchalis

Thick-billed euphonia Stripe-backed wren

Evidence i) mates share flight calls, ii) experimental pairing: either partner could learn mate’s flight call or both converged on new intermediate call Each pair shares own distinctive flight call i) pairs match flight calls, ii) flight call learning from foster parents Call convergence in adult flocks Impoverished calls in acoustic isolates Microgeographic dialects, absent in calls of acoustic isolates Unique call of one pair copied by most of their offspring and one adult female socialising with them Heterospecific alarm calls Sex-specific calls for maternal and paternal lines

Source Mundinger, 1970

Marler and Mundinger, 1975 Groth, 1993a,b Nowicki, 1989 Hughes et al., 1998 Ficken et al., 1985 Haftorn, 1993

Morton, 1976 Price, 1998


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authors to suggest that there might be gender dialects in this species. In another duetting species (the bay wren Thryothorus nigricapillus), in which males and females also sing sex-specific songs, tape and live tutoring clearly led to imitation of model songs by males and females (Levin et al., 1996). Baptista (1978) reports that female Cuban grassquits (Tiaris canona) share some of their song types with males and gives spectrograms of song types of laboratory-hatched individuals where a father, son, and daughter share some of their songs. 5. Adult Learning There are several reports of female starlings singing, a species in which male repertoire changes occur between years (for review see Eens, 1997). In a captive study, wild-caught adult males and females from different locations were placed in a communal aviary (Hausberger et al., 1995a; 1995b). Females showed repertoire changes between the different recording dates, which were timed to cover the changes in social environment. Within a year, most females had added some song types but had also dropped others from their repertoire. Some of the new song types were shared between socially associated females, and, with one exception, no sharing between the sexes was observed. However, as the extent of song exposure during the first year was not known for any of the subjects, and all reported copying was between same population females, it remains unclear whether these songs were newly acquired or whether the females had not sung them during earlier recording sessions but had started using them again as a consequence of the social interactions (Nelson, 1997). While this needs to be addressed in future studies, the observations so far have demonstrated adult flexibility in usage learning (sensu Janik and Slater, 2000) and are suggestive of adult production learning as has been observed in males of this species (Eens, 1997). Other examples include bullfinches, where females learn from their first mate (Nicolai, 1959), or alpine accentors (Prunella collaris), where all first year females were observed to have smaller repertoires than older females, indirectly suggesting that vocal learning continues after the first breeding season (Langmore et al., 1996). Future studies will have to show whether females fall into the same categories of closed and open ended learners as males do (Nottebohm, 1993). B. Call Learning In contrast to song, the call repertoire in many species develops in acoustically isolated birds (for a recent review, see Marler and Hope, in press). However, call dialects have been reported and call learning seems to occur in a number of songbird species. In most songbird species, male

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and female call repertoires overlap partially (or totally) and their learning abilities may do so too, as the examples from a variety of oscine taxa given in Table III suggest. A study on call learning in finches of the genus Carduelis, among them female pine siskins (C. pinus), showed that flight calls are changed by adults to match those of their mates either because one imitates the other or because both home in on an intermediate call (Mundinger, 1970). Similarly, pairs of crossbills (Loxia curvirostra) have pair-specific flight calls. Their great variation within a population, and the observation that cross-fostered chicks have flight calls resembling those of their foster parents, strongly suggest that these are learned (Groth, 1993a; 1993b). In black-capped chickadees (Parus atricapillus), the development of the full adult structure of the ‘‘chickadee’’ and ‘‘gargle’’ calls depends on learning. Some of the notes in these two calls are absent in birds raised without being able to hear conspecific vocalizations, and the calls of nonrelated fledglings come to resemble each other if they are housed together (Ficken et al., 1985; Hughes et al., 1998). At least for the ‘‘chickadee’’ call, plasticity persists into adulthood. The ‘‘chickadee’’ calls of both male and female wild-caught adults housed in aviaries converged in the course of a week to a group specific call (Nowicki, 1989). Another example is that both male and female thick-billed euphonias (Euphonia laniirostris) mimic a variety of heterospecific alarm calls, always of species nesting nearby (Morton, 1976). An intriguing example also comes from the ‘‘WAU’’ calls of stripe-backed wrens (Campylorhynchos nuchalis). In a color-ringed population, male and female relatives shared similar calls. Call sharing must be a consequence of learning, as siblings matched their same sex parents’ calls but not each other if they were of the opposite sex. Since intermediates were not observed, genetic inheritance can be excluded (Price, 1998).

IV. Female Vocal Learning in Non-Oscine Birds Oscine songbirds are not the only bird taxon for which vocal learning has been reported (Catchpole and Slater, 1995), but they are the best studied. In comparison, literature on the subject available in other taxa is rather scarce, but there are at least two orders for which vocal learning has been established (i.e., parrots [Psittaciformes] and hummingbirds [Apodiformes]), and this might also involve females where they vocalize. Male and female budgerigars (Melopsittacus undulatus) modify their calls when joining new groups, (Farabaugh et al., 1994), male and female grey parrots, (Psittacus erithacus) can mimic human speech (Pepperberg, 1994), and for at least one hummingbird species, complex female song has been reported (Ficken et al., 2000). However, examples are few and far between but,


73

given how little we know about female song learning in the well studied oscines, this is more likely to reflect a research bias. This is likely to be a fruitful future research area, especially in the light of the potential for comparative studies on different morphological adaptations of the brain across the different taxa (Gahr, 2000; Jarvis et al., 2000).

V. Sex Differences in Learning? The previous sections have provided ample evidence for female vocal learning. Sex differences in the amount of singing are well documented in many species, but does a sex difference in song output equal sex differences in vocal learning? To compare male and female learning abilities, the two sexes need to be raised and tested under the same conditions and with identical song exposure, as even small differences in the circumstances under which song learning takes place can change its outcome (Nelson, 1997, 1998). Even where such studies demonstrate that females and males do learn differently when raised and tutored in the same way, sex differences in vocal learning abilities are but one reason why the sexes could sing different songs as adults. With our current knowledge, a whole suite of potential mechanisms can be suggested to possibly cause sex differences in songbirds’ vocalizations: Differences between male and female song could come about because (1) female songbirds do not learn their vocalizations or they learn less well than males, or (2) female songbirds learn differently even when exposed to the same songs, or (3) females learn at different times from males and are thereby likely to pick up different vocalizations than their male siblings, or (4) females learn as well as males, but sex differences in the anatomy of the vocal tract results in a different output, or (5) males and females learn the same songs, but females’ songs are different because lower testosterone levels lead to songs being more like the uncrystallized song of young males, or (6) there are sex-specific lineages: While both sexes can learn and vocalize equally well, each sex has specific vocalizations and these are passed on between same sex birds only. As the subsequent paragraphs will indicate, for most of these possible hypothesized causes for sex differences, there is as yet little evidence to either support or reject them. A. Neuroendocrinological Sex Differences and Song Learning The avian song system has provided examples for the most extreme sex differences in functional brain anatomy in vertebrates documented so far. The large differences between closely related species provide excellent

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opportunities for comparative studies in neuroethology (for reviews see Brenowitz 1997; MacDougall-Shackleton and Ball, 1999; Ball and MacDougall-Shackleton, 2001). On a between-species level, sex differences in the song system were found to be correlated with sex differences in song output and repertoire size for the about 20 species compared to date (MacDougall-Shackleton and Ball, 1999). However, it should be emphasized that comparisons so far have mostly been based on sex differences in quantity and quality of adult song output, not song acquisition (in the sense of memorization either to sing or to recognize) and that distributions of repertoire size often overlap between the two sexes (e.g., Gahr et al., 1998). Some of the observed sex differences in brain anatomy might actually be related to the striking behavioral dimorphism of adult song output, but not its acquisition (Bolhuis and Macphail, 2001). Data on female brain anatomy often stem from individuals with unknown ontogeny, while the data on average repertoire size for correlational studies often stem from the literature. However, where song is a facultative trait in females, repertoire sizes might easily be underestimated. Female canaries, for example, are reported by some authors to have a substantially smaller repertoire size than males (e.g., Nottebohm, 1980) and by others to have one similar to that of males (Gu¨ttinger et al., 1988). Starlings provide another example (cf. Hausberger et al., 1995a; MacDougall-Shackleton and Ball, 1999). If we add to this how little we know about how, when, and how much of their vocalizations females learn (see Section III), it seems premature to discuss how sex differences in neuro-anatomy, neuro-endocrinology, and quantity of vocal output relate to sex differences in vocal learning. Increasing our knowledge of song acquisition processes in females and integrating it into these comparative studies should prove extremely interesting and rewarding in the future. B. Sex Differences in Learning Abilities and Sensitive Phases? Next to differences in learning abilities, about which we know very little, males and females could develop different song repertoires because they learn at different times. Again, little is known about sensitive phases for song acquisition in females (both on the production and perception level, Riebel, 2003). Nelson et al. (1997) found that fledgling male and female white-crowned sparrows showed, up to a certain age, higher call rates to sequentially introduced songs that had already become familiar than to novel unfamiliar ones. Although the peak of calling activity (probably equal to the sensitive phase as males later sung these songs) was the same in the two sexes, females stopped showing a differential response to different songs at an earlier age than males. Similarly, tape tutoring in


75

cardinals suggests a shorter time for song acquisition in females than in males. Although adult females’ repertoires on average consisted of as many different song types as those of males, females had preferentially learned songs played back earlier during an extended song tutoring period (Yamaguchi, 2001). In another tape tutoring study in the white-crowned sparrow, tutoring after 50 days posthatching was successful in males but not females (Petrinovich and Baptista, 1987); then again, females learn badly in the laboratory anyway even if tutored earlier (Cunningham and Baker, 1983; Petrinovich, 1985), despite singing full song in the wild (Baptista et al., 1993). In northern cardinals, differences in male and female song can be demonstrated by spectrographic analysis (Yamaguchi, 1998b), and these differences are perceived by both males and females during playback experiments (Yamaguchi, 1998; but see Ritchison, 1986). However, in a tape tutoring experiment, both sexes learned indiscriminately from male and female model songs (Yamaguchi, 2001). The main differences in male and female songs were actually in spectral composition with females’ songs having less energy concentrated in the fundamental frequency (Yamaguchi, 1998). This is also one of the major sex differences in nonlearned vocalizations of a non-oscine bird, the collared dove (Streptopelia decaocto). In this species, sex differences in sound production correlated highly with age, that is, increasing with differences in the anatomy of the syrinx and other parts of the vocal tract (Ballintijn and ten Cate, 1997a). Interestingly, the decrease of harmonic overtones in males occurred gradually during development, well after voice breaking, which made the authors suggest that this could be a consequence of increased motor practice in more vocally active males (Ballintijn and ten Cate, 1997b). In an unsuccessful tape tutoring experiment, marsh tits learned little from tapes, but male songs were more species-specific than female songs (Becker, 1978). However, when tutored by their parents, males and females copied equal numbers of syllables and learning took place from both fathers and mothers (Rost, 1987). Studies specifically comparing male and female repertoires within a population are relatively rare. Males and females in the wild sing the same regional dialect in white-crowned sparrows (Baptista et al., 1993). However, laboratory tutoring showed that there must be sex differences in the timing or circumstances for learning because females failed to learn song under a number of circumstances in which males did learn (e.g., Cunningham and Baker, 1983; Petrinovich, 1985; Petrinovich and Baptista, 1987). Female song is often relatively rare in terms of the absolute time spent singing. Consequently, many field studies have small sample sizes both with respect to the total number of individuals and total number of songs

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recorded. The latter could of course easily lead to lower repertoire estimates for females. This can be illustrated by a random example. Female European robins (Erithacus rubecula) were described by Hoelzel (1986) as having smaller repertoire size, slightly shorter songs, and more repetitions than males in the same population. However, only two females were recorded and, when comparing the figures and cumulative plots for repertoire size, the two females’ songs fell within the range of male song in most parameters. Another caveat concerns recording context. Singing activity might peak at different times of the year for males and females and other differences in recording contexts for males and females could also bias repertoire estimates. Where there is considerable overlap in male and female repertoires, but where song has been recorded in different contexts, some of the conclusions regarding differences in male and female repertoire size might have been drawn without sufficient data to support them statistically. C. Sex-Specific Lineages? A number of authors have suggested that there might be sex-specific lineages for song learning in species where both sexes sing but consistent differences in male and female repertoires are found (Bertram, 1970; Hausberger et al., 1995b; Hausberger, 1997), which might result in gender dialects (Wickler and Seibt, 1988). This is a hypothesis worth testing where males and females are observed to sing regularly but with only partly or even nonoverlapping repertoires, as has been reported particularly from a number of duetting species (for review see Hall, in press). Australian magpies live either in territory-defending groups or nonterritory-owning flocks. All group members of both sexes will sing together and countersing with neighbors. Syllable sharing is high within groups, but also between neighboring groups (Farabaugh et al., 1988; Brown and Farabaugh, 1991) in which same sex birds share more syllables than opposite sex birds. At the same time, each individual has a high percentage of unique syllables. However, for one bird where the parents’ repertoire was known there was high sharing between it and its parents (unfortunately the percentages for sharing with each parent are not given). While sex specific syllables are one possible interpretation the authors give for their observations, pairwise comparisons among all birds across all groups in the sample showed no more sharing between same than opposite sex birds. Sex-specific dispersal patterns could be an alternative explanation. In a population of stripe-backed wrens male, but not female, calls within a group showed high similarity. Dispersal patterns in the studied population were known and males remained in the natal group while females


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dispersed (Price, 1998). What at first glimpse could be interpreted as males learning a group specific call where females fail to do so seems in this species a consequence of sex specific dispersal. These questions should ideally be addressed by combining learning experiments in the laboratory with field studies. However, only for two species in which sex-specific lineages have been suggested is detailed analysis of song ontogeny available. In the slate-colored boubou, handreared birds housed without conspecific tutors sang poorer versions of some of the elements observed in the wild, but had also learned from each other and developed matching element repertoires (Wickler and Sonnenschein, 1989). In a group reared by adult conspecifics, both males and females learned their elements from each other or from the adults with whom they were housed (Wickler and Sonnenschein, 1989). Similarly, duetting bay wrens have sex-specific repertoires, but they can learn both male and female elements when tape tutored (Levin et al., 1996). This suggests that the differences between male and female repertoires are not due to different abilities in learning or in producing songs, but that other factors during development guide which songs are learned. If such mechanisms exist in the wild, sex-specific lineages in these two species remain a possibility, but no other data are available as yet from song learning or tutor choice experiments in these or other species.

VI. Summary Songbirds are known for their vocal versatility and the great developmental plasticity that permits or even makes it normal that adult signals are shaped by social learning processes. Song functions as an important mate attraction signal. Hence, it is often sexually dimorphic, with males typically the vocally displaying and advertising sex. Female song seems rare in comparison, and these behavioral dimorphisms also seem to map onto neuroanatomical differences in the specialized brain nuclei involved in singing. Consequently, there has been an emphasis on studying song acquisition in male songbirds. However, with female song described in a growing number of species, a new interest in the form and function of female song has surged. Likewise, theory has spawned interest in causes of variation on the receiver’s side but also increasingly in the extent and function of female ornaments. With a culturally transmitted mating signal, learned preferences arise as an additional dimension next to genetically inherited and condition-dependent variation in female preferences and signaling.

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Surveying the current literature shows that the occurrence of vocal learning in female songbirds is supported by many different lines of evidence. Learning processes, in particular during development, contribute to shaping adult vocalizations in those species where females are known to sing, but also seem to contribute to variation in calls in a number of species. While plenty of evidence for vocal learning could be found, this review has also revealed how little we know about the circumstances under which females learn and when and from whom they learn their songs. Furthermore, learning how to sing or to call is but one way learning processes seem to affect vocal communication in songbirds. Perhaps even more importantly, for both species with singing and non-singing females, early acoustic experiences seem to have far-reaching consequences on adult song perception. Despite pre-existing biases, there seems to be a developmental window during which acoustic experience will fine-tune these perceptual filters towards particular song variants or characteristics but which also seems to allow widening of the range of meaningful signals. Perception in isolation-reared females is reminiscent of the impoverished vocalizations of male songbirds reared in acoustic isolation. A picture emerges that shows that learning in the vocal domain is even more prevalent in songbirds than previously thought, as perception learning seems as widespread as production learning. Cultural transmission is taking place, both in the advertising and in the choosing sex. Learned preferences could alter selection for particular song variants on the sender’s side, but where males and females are exposed to the same tutors, they might also lead to drastic changes in mate recognition from just one generation to the next. The notion of sex differences in vocal learning, where both production and perception are concerned, clearly needs closer study. There is no doubt that there are sex differences in the amount and context of singing. However, inferring from this that there are sex differences in vocal learning abilities could well have been premature, and for a number of species future studies may reveal that sex differences are either absent or differences are in learning content, not abilities. It remains undisputed that females in some species do not sing; in these the challenge for the future is to discover how and when the observed perceptual learning is taking place, and when memorizing of songs leads to permanent or temporary changes in perception. Reviewing the empirical evidence has stressed the multiple consequences of early learning on female song preferences, suggesting an important role for receiver learning on sexual selection-driven signal evolution. This aspect is still poorly understood in the evolution of vocal learning but is perhaps the key to understanding its origin and maintenance.


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Acknowledgments I would like to thank Vincent Janik, Carel ten Cate, and Peter Slater for many fruitful discussions on the subject of vocal learning. Carel ten Cate, Hans Slabbekoorn, Johan Bolhuis, Peter Slater, Tim Roper, and Naomi Langmore provided constructive and much appreciated comments on earlier versions of this manuscript.

References Andersson, M. (1994). ‘‘Sexual Selection.’’ Princeton University Press, Princeton. Baker, M. C. (1983). The behavioral response of female Nuttall’s white-crowned sparrows to male song of natal and alien dialects. Behav. Ecol. Sociobiol. 12, 309–316. Baker, M. C., Bjerke, T. K., Lampe, H. U., and Espmark, Y. O. (1987). Sexual response of female yellowhammers to differences in regional song dialects and repertoire sizes. Anim. Behav. 35, 395–401. Baker, M. C., and Cunningham, M. A. (1985). The biology of bird-song dialects. Behav. Brain Sci. 8, 85–133. Baker, M. C., Spitler-Nabors, K. J., and Bradley, D. C. (1981). Early experience determines song dialect responsiveness of female sparrows. Science 214, 819–821. Baker, M. C., Spitler-Nabors, K. J., and Bradley, D. C. (1982). The response of female mountain white-crowned sparrows to songs from their natal dialect and an alien dialect. Behav. Ecol. Sociobiol. 10, 175–179. Balaban, E. (1988). Cultural and genetic variation in swamp sparrows (Melospiza georgiana) II. Behavioural salience of geographic song variants. Behaviour 105, 292–322. Ball, G. F., and MacDougall-Shackleton, S. A. (2001). Sex differences in songbirds 25 years later: What have we learned and where do we go? Microsc. Res. Tech. 54, 327–334. Ballintijn, M. R., and ten Cate, C. (1997a). Sex differences in the vocalizations and syrinx of the collared dove (Streptopelia decaocto). Auk 114, 445–479. Ballintijn, M. R., and ten Cate, C. (1997b). Vocal development and its differentiation in a nonsongbird: The collared dove (Streptopelia decaocto). Behaviour 134, 595–621. Baptista, L. F. (1978). Territorial, courtship and duet songs of the Cuban grassquit (Tiaris canora). J. Orn. 119, 91–101. Baptista, L. F., and Morton, M. L. (1982). Song dialects and mate selection in montane whitecrowned sparrows. Auk 99, 537–547. Baptista, L. F., and Morton, M. L. (1988). Song learning in montane white-crowned sparrows: From whom and when? Anim. Behav. 36, 1753–1764. Baptista, L. F., and Petrinovich, L. (1986). Song development in the white-crowned sparrow: Social factors and sex differences. Anim. Behav. 34, 1359–1371. Baptista, L. F., Trail, P. W., DeWolfe, B. B., and Morton, M. L. (1993). Singing and its functions in female white-crowned sparrows. Anim. Behav. 46, 511–524. Becker, P. H. (1978). Der Einflub des Lernens auf einfache und komplexe Gesangsstrophen der Sumpfmeise (Parus palustris). J. Orn. 119, 388–411. Beletsky, L. D. (1982). Vocalizations of female northern orioles. Condor 84, 445–447. Bertram, B. (1970). The vocal behaviour of the Indian hill mynah. Anim. Behav. Monogr. 3, 81–192. Bolhuis, J. J., and Eda-Fujiwara, H. (2003). Bird brains and songs: Neural mechanisms of birdsong perception and memory. Anim. Biol. 53, 129–145. Bolhuis, J. J., and Macphail, E. M. (2001). A critique of the neuroecology of learning and memory. Trends in Cognitive Sciences 4, 426–433.

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Selection in Relation to Sex in Primates Joanna M. Setchell1 and Peter M. Kappeler2 1

2

centre international de recherches medicales bp 769 franceville, gabon

abteilung verhaltensforschung und o¨kologie deutsches primatenzentrum ¨ ttingen, germany 37077 go

I. Introduction Essentially neglected for 100 years after the publication of ‘‘The Descent of Man and Selection in Relation to Sex’’ (Darwin, 1871), sexual selection is now one of the most active fields in evolutionary biology, with a vast literature devoted to empirical and theoretical research (Andersson, 1994). However, although Darwin addressed the question of sexual dimorphism, secondary sexual characteristics, and weapons in primates, and later published a paper entitled ‘‘Sexual Selection in Relation to Monkeys’’ (Darwin, 1871, 1876), studies of non-human primates continue to be underrepresented in this field. This is especially true for investigations of the diversity of sexually selected behavioral strategies and tactics. Whereas primatologists have described and analyzed anatomical differences between the sexes in great detail (see Dixson, 1998a for a recent review), other targets of sexual selection remain relatively poorly studied, especially in comparison with other taxa (e.g., insects, birds, amphibia, and fish; Johnstone, 1995, 2000; Andersson and Iwasa, 1996; Ryan, 1998; Paul, 2002). Moreover, although several reviews have covered aspects of sexual selection in primates (Hrdy and Whitten, 1987; Smuts, 1987; Small, 1989; Keddy-Hector, 1992; Smuts and Smuts, 1993; van Schaik et al., 1999; van Schaik, 2000a; Paul, 2002), the existing body of relevant primate data has largely remained un-synthesized in recent years. Some behavioral aspects of sexual selection are perhaps better studied in human primates (Thornhill and Gangestad, 1996; Buss, 1994, 1999), but evolutionary 87 Copyright 2003 Elsevier Inc. All rights reserved. 0065-3454/03 $35.00

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psychology, the discipline mostly concerned with evolutionary studies of human sexual behavior, is largely isolated from mainstream primatology. We aim to begin filling these gaps by reviewing research on the causes and consequences of reproductive competition, mate selection, and intersexual conflict in primates and teasing apart specific adaptations and tactics from the perspective of both sexes. We begin our review with a brief summary of the main concepts of sexual selection theory. We then examine the relevance of sexual selection to primates and the relevance of primate studies to studies of sexual selection. Next, by using a comparative and theory-oriented approach to examine the reproductive strategies of male and female primates, we hope to draw some general conclusions about sexual selection in primates and to stimulate future research on all aspects of sexual selection in primates.

II. Causes, Mechanisms, and Consequences of Sexual Selection Sexual selection arises from ‘‘the advantages that certain individuals have over others of the same sex and species, in exclusive relation to reproduction’’ (Darwin, 1871). Darwin developed the theory of sexual selection to explain the evolution of conspicuous male traits such as bright colors, long tails, and antlers. Such traits pose a risk to a male’s survival; however, Darwin suggested that this cost was outweighed by an advantage in fighting other males or attracting females, and a higher chance of mating with females. In practice, however, it is not always easy to demonstrate that a trait is sexually selected because several criteria, such as discrimination of traits by rivals or mates and their reproductive consequences, need to be fulfilled (Snowdon, 2003). Darwin reviewed an amazing diversity of sex differences in invertebrates, birds, mammals, and humans, noting that sexual selection usually involved males competing over females (intra-sexual selection), leading to the evolution of aggressiveness, larger body size, and weaponry; and females choosing males (inter-sexual selection), leading to the evolution of extravagant male ornaments (1871). These patterns have since been theoretically explained by differential parental investment (Trivers, 1972) and differential potential rates of reproduction in the two sexes (CluttonBrock and Vincent, 1991). Individuals have finite resources, time, and energy for reproduction. Males can normally increase the number of offspring they produce by mating with more than one female, whereas females are limited by the resources required to nurture offspring and generally cannot increase the number of offspring produced by mating with more males (Bateman, 1948; Trivers, 1972). This basic strategic

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difference between the sexes means that in polygynous species, where some males mate with many females and other males with none, success in competition with rival males is crucial to male fitness; sexual selection, however, can also work in monogamous species, if mates differ in quality (Darwin, 1871; Kirkpatrick et al., 1990). Thus, males generally apportion reproductive effort to competition in order to fertilize as many females as possible and show greater variance in reproductive success than females. Females, by contrast, are typically more discriminatory in mating choices. They choose mates that provide benefits, either directly, in terms of resources, protection, or parental care, or indirectly, via good genes to produce offspring of the highest possible quality, and show less variance in reproductive success than males. Traditionally, sexual selection theory has concentrated on competition between males for access to mates and female choice for male traits (Bradbury and Davies, 1987). However, sex role reversal can occur where the general rule of high female investment is reversed, males are the main investors in offspring, and females compete for males (reviewed by Petrie, 1983; Andersson, 1994). If the costs of reproduction are high, then males should compete selectively to maximize benefits and distribute their copulations to ensure fertilization, while females compete among themselves for mating opportunities, exhibiting physical adornments or displays that enhance their attractiveness to mates (e.g., Berglund and Rosenqvist, 2001). Furthermore, there is mounting theoretical and empirical evidence for the occurrence of mate choice by males and competition among females in species without sex-role reversal under various circumstances (Engqvist and Sauer, 2001; Koeninger and Altmann, 2001; Gowaty, 2003) and for the importance of random factors in generating variance in reproductive success (Hubbell and Johnson, 1987). Males and females in many taxa can therefore be expected to be both choosy and to engage in mate competition simultaneously (Johnstone et al., 1996; Cunningham and Birkhead, 1998; Kraak and Bakker, 1998). The mechanisms and consequences of competition with same-sex conspecifics for access to mates have traditionally received less attention than studies of mate choice, but some important insights have emerged. First, it has been important to realize that intra-sexual selection not only occurs before copulation, but also afterwards (Parker, 1970; Eberhard, 1996). Specifically, pre-copulatory competition occurs in the contexts of mate searching and monopolization, whereas post-copulatory competition includes mate guarding, sperm competition, induced abortions, and infanticide. Second, the relative importance of the main mechanisms of competition is largely determined by the distribution of mates in space and time (Emlen and Oring, 1977). Where mates are dispersed, scramble

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competition operates, where individuals attempt to locate a mate before rivals do so. This selects for well-developed sensory organs and mobility. Moreover, when mates cannot be effectively monopolized, for example, because their fertile periods are highly synchronized, scramble competition is also expected among sperm of two or more males that are able to mate with females under these circumstances. Over evolutionary time, the resulting sperm competition will favor the production and ejaculation of larger numbers of sperm (Birkhead and Hunter, 1990; Birkhead, 1996). In addition, sperm competition may operate at the level of fertilization efficiency for individual sperm, which might differ in quality, including motility and length (see Tregenza, 2000), resistance to products of the female reproductive tract (Stockley, 1997), interference with foreign sperm or their deposition (Parker, 1984; Birkhead and Møller, 1998), or cooperation and altruism between sperm from the same male (Moore et al., 2002). Contest competition, in contrast, is expected whenever groups of mates are clumped in space or when their fertile periods are not synchronized (Emlen and Oring, 1977). Under these conditions, individual males should try to exclude rivals from mates or at least prevent co-resident rivals from mating. Such contests include displays and often escalate into physical fights, so that traits that confer an advantage in these interactions (such as size, strength, weaponry, endurance, and well-developed substrates of various signals used in displays) are positively selected (Harvey and Bradbury, 1991; Zuk, 1991). Reduction of gonadal and function in the presence of rivals by socioendocrinological mechanisms represents an additional, indirect form of contest competition (e.g., von Holst, 1998). Third, individuals of the same species may vary in the use of a particular competitive strategy or tactic. For example, some males compete for matings, while others sneak. Polymorphisms occasionally have a genetic basis (i.e., strategies) but are usually condition or status-dependent (i.e., tactics) (Gross, 1996). A much greater amount of both theoretical and empirical work has concentrated on inter-sexual selection, particularly the benefits of mate choice to females and the evolution of extravagant male displays (reviewed by Andersson, 1994). Three main models of mate choice can be distinguished, depending on what the choosy sex obtains. First, particular mates may be chosen because they provide the greatest or most valuable direct benefits to females. These direct benefits can be material in nature, such as food or other resources (e.g., Engqvist and Sauer, 2001), or accrue in the form of parental care. Second, females obtain only indirect benefits in the form of particularly good genes for their offspring. These genetic benefits may affect offspring attractiveness (Fisher, 1958; Lande, 1981; Kirkpatrick, 1982), other heritable qualities and developmental stability


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(Zahavi, 1975; Møller and Swaddle, 1997) or immunocompetence and parasite resistance (Hamilton and Zuk, 1982; Folstad and Karter, 1992; von Schantz et al., 1996; Grob et al., 1998). Third, the choosy sex may obtain no benefits at all. Instead, mate choice is based on traits that are favored because they exploit pre-existing sensory biases (Ryan and Keddy-Hector, 1992) or because they are so exaggerated that they help to overcome female resistance (‘‘chase away selection,’’ Holland and Rice, 1998). Finally, it is important to realize that inter-sexual selection can also operate after insemination. Whenever a female receives sperm from two or more males, cryptic female choice (Eberhard, 1985, 1996) can influence the fate of spermatozoa within her reproductive tract, favoring one male’s sperm over another and leading to selective fertilization, implantation, and/or abortion (Birkhead, 2000). For example, if female feral fowl are sexually coerced by subordinate males, they differentially eject the sperm from subdominant males (Pizzari and Birkhead, 2000). It has been suggested, for example, that post-copulatory mechanisms of female choice may be more successful at detecting genetic compatibility than pre-copulatory mechanisms because males cannot disguise their identity as easily (Zeh and Zeh, 1997). In addition to competition between animals of the same sex, both before and after insemination, inter-sexual conflict is beginning to be recognized as an important factor in determining patterns of mating behavior and mating systems (Davies, 1992; Andersson, 1994; Clutton-Brock and Parker, 1995; Chapman et al., 2003). Indeed, it has been suggested that sexual coercion should be regarded as a third important selective force influencing the evolution of male and female reproductive strategies, on par with inter- and intra-sexual selection (Smuts and Smuts, 1993). Defined as ‘‘the use of force or the threat of force to increase the probability that a member of the opposite sex will engage in fertile matings at some cost to the recipient’’ (Smuts and Smuts, 1993), coercion includes physical aggression against females, forced copulation, harassment and intimidation, induced abortion and reinsemination by a second male (‘‘Bruce effect’’: Schwagmeyer, 1979; Huck, 1984), and sexually-selected male infanticide (Clutton-Brock and Parker, 1995; van Schaik, 2000a). Females are by no means the passive victims of male aggressive strategies, however. Female counter-strategies to sexual coercion include the avoidance of males, female-female coalitions, and mating preferences (Smuts and Smuts, 1993; Clutton-Brock and Parker, 1995; van Schaik, 2000b; Moore et al., 2001).* Female strategies may also persist *

Here and throughout this contribution, we use the terms ‘‘strategy’’ and ‘‘tactic’’ loosely, as they are used interchangeably in the primate literature, and the genetic basis of reproductive strategies in primates is generally as yet unknown.

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post-fertilization in terms of biased investment in offspring according to the female’s own condition, the sex of the infant and/or the identity of the sire (Qvarnstrom and Price, 2001), or sex ratio manipulation (Dhondt and Hochachka, 2001). Mating and reproductive outcomes are therefore the product of the conflicting strategies of males and females. Males attempt to inseminate as many females as possible, although the benefits of doing so are tempered by the costs involved (e.g., disease risks, conflicts with other males, less time for mate guarding of the ‘‘best’’ available female), while females attempt to avoid the costs of male strategies and to control fertilization of their ova (Johnstone and Keller, 2000). The higher the potential variance in male reproductive success, the more important sexual selection becomes in males and the greater is the likelihood of the evolution of male traits that are incidentally harmful to females. Females therefore evolve resistance to male competitive adaptation (Brooks and Jennions, 1999; Johnstone and Keller, 2000). That this is costly to both sexes has been elegantly demonstrated by studies of sex-antagonistic genes (alleles that are simultaneously beneficial to the fitness of one sex and costly to the fitness of the other sex) in Drosophila melanogaster (Holland and Rice, 1999). In summary, although sexual selection is often regarded as being distinct from natural selection, it should in fact be regarded as natural selection acting differently on the two sexes (i.e., ‘‘selection in relation to sex’’) (Darwin, 1871; Clutton-Brock, 2003). Modern sexual selection theory encompasses the conflicting interests of males and females and the evolutionary consequences of all aspects of competition for mates. The mechanisms and consequences of the differing reproductive interests of the two sexes are summarized in Table I.

III. Relevance of Primates to Sexual Selection Given the extensive data available concerning sexual selection in other taxa, why do we need a review like this chapter or entire books (Kappeler and van Schaik, 2003; Jones, 2003) on sexual selection in primates? Primates are not obvious candidates for the experimental approach required to test sexual selection hypotheses. Ethical issues and their slow life-history limit the possibilities for study (Janson, 2000; Stearns, et al., 2003). Long-term studies are essential, and small sample sizes make it difficult to obtain conclusive results. However, there are several reasons why primates are of interest to students of sexual selection. First, in contrast to the extensively studied taxa, primates tend to live in close social

TABLE I Mechanisms and Conseuencies of Sexual Selection in Primates (see also Andersson, 1994). Consequences

Mechanism Scramble

Rapid location of mate crucial to fitness

Sex differences in dispersal and roaming

Endurance rivalry

Persistence in mating arena affects mating success Rivals display to one another or fight for access to mates (or resources that attract mates)

Investment in maintenance, and body condition compromised for mating opportunities Evolution of traits that improve or advertise fighting ability (large size, weaponry, displays)

Contest

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Behavioral and/or physiological suppression of reproduction in subordinate individuals

Evolution of alternative strategies in competitively inferior individuals Mate choice

Mate influences mating success

Evolution of behavioral and morphological traits that attract the opposite sex

Evolution of sexual coercion

Primate examples Males of non-gregarious nocturnal species range more widely during the mating season (Kappeler, 1997b), and males visit and inspect females in rapid succession (Fietz, 1999; Eberle and Kappeler, 2002) Mate-guarding constrains foraging behavior in baboons (Bercovitch, 1983; Alberts et al., 1996) Sexual dimorphism in body size and weaponry (Plavcan, 1999). Greater mating and reproductive success for dominant males Physiological suppression of reproduction in subordinate female callitrichids (Abbott et al., 1990) and male sifakas (Kraus et al., 1999). Suppression of secondary sexual traits in subordinate male mandrills and orang-utans (Setchell, 2003) Subordinate male baboons form coalitions (Noe¨ and Sluijter, 1990); subordinate male mandrills mate sneakily (Setchell, 1999) Mate choice for direct or indirect benefits (Paul, 2002), e.g. female choice for fully developed ‘‘flanged’’ male orang-utans (van Hooff, 2003); male choice for females with larger sexual swellings (Domb and Pagel, 2001) Male aggression towards females (Smuts and Smuts, 1993) including infanticide (Hrdy, 1979; van Schaik and Janson, 2000) (continued)

TABLE I (continued) Mechanism

Sperm competition

Consequences Evolution of mate-guarding, complex genital morphology, ejaculate characteristics, etc.

Competition between spermatozoa of more than one male within female reproductive tract

Evolution of mate-guarding to prevent rivals from mating Production of large amounts of sperm

Males physically aggress females Induced abortion or killing of infant sired by a rival male

Evolution of ejaculate characteristics that promote fertilization Evolution of female strategies to resist coercion Evolution of infanticide avoidance strategies in females to bias and confuse paternity

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Cryptic female choice influences reproductive success post-insemination

Sexual coercion

Primate examples Males mate guard females in an attempt to prevent other males from mating (Dixson, 1998a). Species with polyandrous females tend to have a longer and morphologically more complex penis (Dixson, 1987b) Males defend access to receptive females (Dixson, 1998a) Evolution of larger testes in species where females commonly mate with a number of partners during a single receptive period (Short, 1979; Harcourt et al., 1981; Kappeler, 1997a) Copulatory plugs in genera where females commonly mate with multiple partners (Dixson and Anderson, 2002) Females mate with dominant male for effective protection (Smuts and Smuts, 1993) Lengthened follicular phase, sexual advertisement and unpredictable ovulation in catarrhines (Nunn, 1999a; van Schaik et al., 2000) Pseudo-estrus in species in which infants sired by a previous male are vulnerable to infanticide after group takeover by a new male (Hrdy, 1979; Hrdy and Whitten, 1987; van Schaik et al., 1999)


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groups in which several generations are present. Under such conditions, obvious signals of competitive or genetic fitness may be less important as cues to mating. Mate assessment can be a cumulative process over months and years, whereas in seasonally-pairing birds or in the brief sexual encounters of insects, reproductive choices must be made quickly on the basis of relatively little information. In most primate species, prior knowledge of potential mates means that choices are less likely to be based on arbitrary ornaments than on other assessments. The comparatively advanced social intelligence of many primates may also interact with their complex sociality in influencing reproductive decisions. Thus, long-term co-residence in social groups may provide a very different set of cues than is needed by species where mating is for short periods or even ephemeral. Studies of sexual selection are currently dominated by work on birds, fish, and invertebrates. The hypotheses addressed and theoretical models constructed for these taxa may not be directly relevant to primate research (Kappeler and van Schaik, 2002). Thus, primate studies challenge students of sexual selection to develop and test new theories and explanations for observed phenomena. Second, primates exhibit a variety of social organizations, social structures, and mating systems that are rivalled by few other mammalian orders (Kappeler and van Schaik, 2002). The 300 or so primate species cover several orders of magnitude in body size and represent an associated diversity in life histories (Kappeler and Pereira, 2003). They also stand for the major social systems, including solitary, pair-living, and group-living species; male, female, or bisexual dispersal; as well as all major mammalian mating systems and different types of parental care. Furthermore, perhaps due to an anthropocentric bias, a great deal of detailed information is available concerning primate behavior and ecology in comparison to other mammals, making non-human primates a rich source of comparative data (Smuts et al., 1987; Lee, 1999; Kappeler, 2000). A few primate species are exceptionally well studied (e.g., chimpanzees and Old World monkeys living in relatively accessible habitats), and some of the great long-term studies of vertebrate populations concern primates. Such information, concerning a broad array of species with divergent social systems and ecology, allows primatologists to examine the effects of sexual selection from a comparative perspective and investigate the influence of ecological and social constraints on reproductive strategies. In an attempt to counteract the general lack of contact between the fields of primate and non-primate socioecology (Hauser, 1993; Harcourt, 1998; Snowdon, 2003), our goal in this review is to examine theoretical predictions and synthesize empirical data concerning male and female

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reproductive strategies, to reach some general conclusions, and to encourage studies of all aspects of sexual selection in primates.

IV. Relevance of Sexual Selection to Primates What evidence do we have for the operation of sexual selection in primates? As in other mammals, the costs of internal fertilization, gestation, and lactation are especially high for female primates (Altmann, 1980; Oftedal, 1984; Gittleman and Oftedal, 1987; Clutton-Brock et al., 1989; Lee et al., 1991; Lee, 1996). As a result, some form of polygyny is expected in most species (Clutton-Brock, 1989; Dunbar, 1995). The great variety of mating systems that exist in primates has been reviewed elsewhere (Eisenberg et al., 1972; Harvey and Harcourt, 1984; Smuts, 1987; Dunbar, 1988; Dixson, 1997) and is summarized briefly in Table II. Within species, the level of competition for mates, the within-sex variance in reproductive success, and therefore the potential for sexual selection, depend on the potential rates of reproduction for each sex, as well as the distribution, quality, and reproductive strategies of mates and sexual rivals (Clutton-Brock and Parker, 1992). Predicted variance in reproductive success for males and females and the types of sexual selection mechanisms therefore vary among mating systems. This summary indicates that the potential for sexual selection is very great in some mating systems. However, traditional classifications of mating systems suffer from the problem of not considering reproductive strategies of both males and females equally; traditional categories are biased by a strong male perspective (Crook and Gartlan, 1966; Crook, 1972). We therefore prefer to proceed by discussing male and female perspectives separately. Further, it is important to note that sexual strategies operate at the level of the individual and that variation may occur between the individuals in a single species. Facultative responses to variations in the social, ecological, or physical environment lead to flexible condition and situation-dependent strategies (Brockmann, 2001).

V. The Male Perspective: The ‘‘Copulatory Imperative’’ The reproductive success of a male primate is limited by the number of females he can fertilize, selecting for a ‘‘copulatory imperative’’ (Ghiselin, 1974). The primary type and intensity of competition between males is determined by the monopolizability of females, which in turn is determined by their spatial distribution, the absolute number of females

TABLE II Primate Mating Systems, with Variance in Reproductive Success and the Potential for Sexual Selection (See Text for References)

Mating system

Description

Examples

Variance in reproductive success

Monogamy

Males and females typically mate with only one member of the opposite sex

Indri, Callicebus Aotus, Hylobates

Roughly equal

Polyandry

One female mates with several males and each of those males mates only with that particular female Males defend mating access to several females

Saguinus fuscicollis, Callithrix humeralifer

Female > male

Galagoides demidoff, Perodicticus potto, Lepilemur leucopus, Tarsius syrichta and Pongo pygmaeus Mirza coquereli, Microcebus murinus

Male > female

Spatial polygyny

Scramble polygyny

Female defense polygyny Harem polygyny Polygynandry

Females are dispersed, and not defensible, males roam widely in search of mating opportunities with receptive females, both sexes typically mate with several partners Coalitions of males defend a territory containing several females with which most males mate A single male defends exclusive mating access to a group of females Several males defend groups of females, both males and females mate with multiple partners

Potential for sexual selection Low, although mate choice and competition for mates may play a role if mates differ in quality Sperm competition where extra-pair copulations occur Female-female competition Sperm competition and cryptic female choice Male contest competition

Male > female

Scramble competition between males Sperm competition

Brachyteles, Pan

Male > female

Male contest competition Sperm competition

Theropithecus, Papio hamadryas Macaca, most Papio spp.

Male > female

Male contest competition

Male > female

Male contest competition Sperm competition Female choice

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in group-living species, and the degree of synchrony of their receptive periods (Mitani et al., 1996a, b; Nunn, 1999b; Kappeler, 2000a). In the following section we review male reproductive strategies and tactics and the corresponding mechanisms of reproductive competition under these various boundary conditions. A. Basic Considerations and Ground Rules It is important to recognize that different types of social organization are both determinants and outcomes of sexual strategies (Kappeler and van Schaik, 2002). The number of members of the same and opposite sex that live together has important consequences for male reproductive and competitive strategies in particular (see also Davies, 1991). We therefore begin by outlining the main scenarios from the males’ perspective to deduce syndromes of behavioral, morphological, and physiological competitive mechanisms characterizing particular situations. We consider the spatial distribution of females as the primary determinant of male sexual strategies. From the males’ perspective, the most basic question is whether females are dispersed in space or not. In about one third of all primate species, reproductively active females are not associated with each other (van Schaik and Kappeler, 2003). From the males perspective they are dispersed in space and require a strategic decision about dispersal and ranging behavior (Dunbar, 2000). Depending on the males’ decision, two fundamentally different types of social organizations can be distinguished (Kappeler and van Schaik, 2002). First, males range independently, often trying to encompass ranges of several females within their home range. Such a social system is found in orangutans (Pongo pygmaeus) and many nocturnal prosimians (Kappeler, 1999a). Second, males associate permanently with a single female, resulting in the formation of either pairs or small groups containing one female and several males. Pairs have evolved independently in all major primate lineages, whereas so-called polyandrous groups are the modal grouping pattern only in some New World callitrichids (Kappeler, 1999a; van Schaik and Kappeler, 2003). In the majority of primates, however, two or more females are permanently associated or form subunits of variable size and composition with a set of other females. In these species, males are permanently associated with these spatially-clumped females. Notably in some colobines and guenons, most males are excluded from the female group and live in all-male bands for most of the year or until they can successfully take over a group of females (Borries, 2000; Cords, 2000). Given a particular spatial distribution of females and the males’ decision to associate with them or not, three hierarchical levels of inter-male


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competition for fertilizations can be distinguished (see also Kappeler, 1999a). First and foremost, males ought to be concerned with gaining access to as many receptive females as possible, while at the same time preventing rivals from doing so. Complete monopolization of several females should always be the most successful male reproductive strategy and thus, the top male priority. If complete monopolization is not possible, a male should try to maximize his number of copulations while keeping the number of copulations by rivals at a minimum. Finally, if males cannot skew the number of copulations in their favor, they may rely on various mechanisms of post-copulatory selection to maximize their chances of fertilization with just one or a few copulations. At each level of competition, mechanisms of both scramble and contest competition can be employed and combined. Before focusing on male sexual strategies, we briefly outline different competitive scenarios in which a male primate may find himself. B. Competitive Scenarios Where female primates are dispersed, several different competitive scenarios are possible from the male perspective. First, individual powerful males are able to defend home ranges that encompass ranges of several females to the exclusion of rival males. Inter-sexual selection is intense, and contest mechanisms involving physical superiority and displays predominate. Males excluded from direct access to females may either range at the periphery of a population nucleus or pursue alternative reproductive tactics while floating through the population. This category, which is often considered to represent the typical pattern for solitary mammals (Mu¨ller and Thalmann, 2000), includes species from independent higher taxa, such as Demidoff’s galago (Galagoides demidoff), pottos (Perodicticus potto), white-footed sportive lemurs (Lepilemur leucopus), Philippine tarsiers (Tarsius syrichta), and orangutans (Charles-Dominique and Hladik, 1971; Charles-Dominique, 1977; Niemitz, 1984; Delgado and van Schaik, 2000). Second, in some species with dispersed females, males cannot monopolize access to females. Here male ranges are larger than those of females, and overlap with the ranges of several females and rival males. It is theoretically expected, but as yet unconfirmed (see Eberle and Kappeler, 2002) that close synchronization of female receptive periods breaks male monopolization potential in these species. In this situation, sexual selection favors males that travel further, are better at detecting receptive females, and are more successful in sperm competition than their rivals. Examples include gray mouse lemurs (Microcebus murinus, Fietz, 1999a; Radespiel et al., 2001) and Coquerel’s dwarf lemur (Mirza coquereli, Kappeler, 1997a).

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Third, when females are dispersed, males may also associate permanently with one of them. There are several potential, non-mutually exclusive explanations as to why these pair-living males apparently ignore the copulatory imperative (Fuentes, 1999; van Schaik and Kappeler, 2003). Because variance in male and female reproductive success is theoretically most even in this situation, the intensity of intra-sexual selection in these supposedly monogamous species has been assumed to be most relaxed and to involve little more than mate defense displays (Rutberg, 1983; Leighton, 1987). However, recent studies have revealed that pair-partners are sometimes only loosely associated (Schu¨lke and Kappeler, 2003) and that extra-pair copulations (EPCs) and extra-pair paternity are not uncommon in some species, so that at least sperm competition may be part of their competitive regime. For example, five EPCs were observed during a 2.5 year study of a siamang group (Hylobates syndactylus, Palombit, 1994); EPCs were observed on about 9% of days when gibbons (Hylobates lar) were observed (Reichard, 1995); 7 of 16 (44%) social fathers were not the genetically determined sire in pair-living fat-tailed dwarf lemurs (Cheirogaleus medius, Fietz et al., 2000); and 4 out of 7 genotyped offspring in fork-marked lemurs (Phaner furcifer) were not sired by the social father (Schu¨lke et al., unpublished data). Pairs are unusually common among lemurs, where they are found in several genera (Indri, Avahi, Lepilemur, Eulemur, Hapalemur, Varecia, Phaner and Cheirogaleus), but are also found in all other major clades (e.g., in Galagoides, Tarsius, Callimico, Aotus, Callicebus, Pithecia, Presbytis, Simias, and Hylobates) (Fuentes, 1999; Kappeler and van Schaik, 2002; van Schaik and Kappeler, 2003). Fourth, several males may permanently associate with a single reproductive female, a type of social organization found only among New World callitrichids with any frequency (Goldizen, 1987). From the males’ perspective, this requires most unusual conditions to evolve as the best option to maximize the number of offspring that survive and reproduce offspring (not necessarily achieved by maximizing the number of fertilizations or females mated) (Dunbar, 1995; Heymann, 2000). In the callitrichid taxa with such a social organization, all males copulate with the female with little mutual interference except temporary aggressive mate guarding, so that sperm competition appears to be the main mechanism of intra-sexual competition (Heymann, 2000). Where female primates are clumped in groups and males can potentially defend a group of females, contest competition generally exists between males, and variance in male reproductive success is potentially high. The number of males that associate with a group of females is the most variable determinant of the mechanisms and intensity of intra-sexual selection (reviewed in Kappeler, 2000a). Qualitatively, the distinction between


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one-male and multi-male groups is of greatest importance from a male perspective, but in reality, variation along this axis is rarely a speciestypical trait. Only very few species of Old World monkeys (e.g. hamadryas baboons (Papio hamadryas) and geladas (Theropithecus)) appear to live invariably in one-male, multi-female groups (Cords, 2000). Others, such as gorillas (Gorilla gorilla), Hanuman langurs (Semnopithecus entellus), and various Presbytis and Alouatta species, are characterized by variation between one- and multi-male, multi-female groups among groups or populations, or within groups over time (Crockett and Eisenberg, 1987; Robbins, 1995; Sterck, 1999; Watts, 2000). Both groups of species are characterized by high levels of variance in male reproductive success, and thus by contest competition. Males fight for access to receptive females with a risk of serious injury or death (Drews, 1996). This high risk, high benefit strategy with higher injury and mortality risks in males than in females is ultimately responsible for the female-biased sex ratios in these species (Clutton-Brock et al., 1977; Clutton-Brock, 1991; Kappeler, 1999b). In the remaining primate species, more than two members of both sexes are permanently associated. From a male’s perspective, these are groups in which single males fail to monopolize access to several females. The absolute number of females, in combination with their reproductive synchrony, is responsible for the lack of an absolute monopolization potential; however, these two variables exhibit much inter-specific variation. In cercopithecines, for example, multi-male groups arise whenever female group size exceeds anywhere between 5 and 20 females, whereas virtually all lemur groups contain fewer than 5 females but nevertheless also contain several males (Andelman, 1986; Kappeler, 2000b). Whenever several males co-reside in a group, a mixture of different contest and scramble competition mechanisms for fertilizations is found between group males. These mechanisms include dominance, mate guarding, physiological suppression, aspects of copulatory behavior, and sperm competition. In the next section, we summarize these and other mechanisms of intra-sexual selection.

C. Mechanisms of Intra-Sexual Selection 1. Mate Detection In species in which females are dispersed and males are not permanently associated with them, males need to find receptive females. Whenever males defend ranges of several females, they may meet and/or interact at sufficiently regular intervals so that periods of receptivity are predictable for males. Because most species in this category are nocturnal prosimians, olfactory signals may be of particular importance in this respect. Whenever

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males defend no exclusive ranges, they can increase their chances of detecting and encountering potential mates by ranging over greater areas and for longer parts of their activity period. This situation should favor small size because of the associated reduced costs of locomotion, endurance, and improved abilities to detect female acoustic and olfactory signals from long range in males. Preliminary observations confirm that male ranges in some solitary species increase several-fold during the mating season (Kappeler, 1997b) and that females and their sleeping sites are visited and inspected in rapid succession (Fietz, 1999a; Eberle and Kappeler, 2002). Physiological studies of individual variation in perceptive abilities among males, as well as detailed studies of individual male ranging behavior during the mating season (see e.g., Fig. 1 in Kappeler, 2000b) are required to further illuminate the importance and detailed mechanism of detecting potential mates. 2. Signals and Displays Fighting and other forms of contest competition between two males may benefit a third male if both contestants are wounded or exhausted. This drives selection for displays or signals that reduce the risk of escalated combat. Body size and canine length may be used in male-male assessment, and male primates also show a wide variety of other exaggerated traits and signals. Striking visual traits of male primates with a potential function in intrasexual selection include brightly colored sexual skin surrounding the perineum and genitalia, manes and capes of hair, and various facial adornments including cheek flanges (summarized in Dixson, 1998a). Visual status signals will be of particular advantage in populations where frequent agonistic interactions occur with unfamiliar individuals, as they preclude costly battles (Rohwer and Ewald, 1981). It is interesting, therefore, that ornaments frequently occur in primate species with very large group sizes (e.g., mandrills (Mandrillus sphinx), red uakaris (Cacajao calvus), hamadryas baboons) or where adult males are widely dispersed (e.g., orangutans). As suggested by their concentration in taxa with polygynous mating systems, these sexually dimorphic traits are thought to function in intra-sexual selection (female choice, see Section VI.D). However, in stark contrast to studies of birds, fish, and invertebrates, where experimental studies abound (Hauser, 1996), most evidence supporting this hypothesis is limited to descriptions of status-dependent modification of some of these traits (Dixson, 1998a). In some primate species, ornament expression varies both between and within individuals as a function of condition or status (red uakaris: Ayres, 1996; vervets (Cercopithecus aethiops): Isbell, 1995; hamadryas baboons:


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Kummer, 1968; mandrills: Setchell and Dixson, 2001a), and experimental evidence has shown that male vervets attend to differences in the coloration of rivals (Gerald, 2001). However, very little is known about the proximate mechanisms underlying variability in trait expression or the costs of production and maintenance of signals. No studies have systematically investigated female preference for male ornaments in non-human primates, which is a potential additional function of these visual signals. For the moment, we can therefore only hypothesize that ornaments may indicate male status and quality, and therefore competitive ability to other males and to females, perhaps demonstrating the ability to overcome a handicap (Zahavi, 1975), parasite resistance (Hamilton and Zuk, 1982), and/or the ability to cope with possible immunosuppressive effects of testosterone (Folstad and Karter, 1992; Verhulst et al., 1999; but see Hews and Moore, 1997; Owens and Wilson, 1999; Siva-Jothy, 1995). Much innovative experimental work will be required by primatologists to approach these questions. Many male primates produce acoustic signals in the form of spectacular long or loud calls (Wich and Nunn, 2002). Because disproportionatelymany forest-living polygynous species exhibit these calls, as well as sexually dimorphic laryngeal anatomies (Dixson, 1998a), it has been speculated that loud calls function in male-male competition, most likely in repelling and deterring non-resident rivals (Mitani, 1985; Crockett and Eisenberg, 1987; van Schaik et al., 1992). Moreover, Cowlishaw (1996) showed that song in male, but not female, gibbons may also be sexually selected as a signal of resource-holding potential in pair-living species. Particular male calls may also function in inter-sexual selection by aiding species recognition and influencing female mating decisions. A particularly important function of vocal signals in male-male competition is expected in the sexually-dimorphic vocal behavior of solitary species (Zimmermann and Lerch, 1993; Bearder et al., 1995; Zimmermann, 1996) where males encounter each other more rarely than co-resident males in group-living species. However, in his careful review that used stringent but crucial criteria, Snowdon (2003) found little general support so far for an intersexually-selected function of primate vocalizations, although intra-sexual selection may play a more important role. Sexual dimorphism in primate vocal signals must therefore be more fully documented and subjected to playback experiments to assess their potential function in attracting mates, deterring rivals, or in species recognition (Bearder et al., 1995). Finally, olfactory signals in urine or from specialized scent glands may serve several important functions in male-male competition, especially in prosimians and New World primates, which have more elaborate signaling and receptor systems for olfactory information than Old World monkeys

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and apes (Dixson, 1998a). In many primates, particular glands are limited to males or bigger in males, males mark more often and they also investigate scents more frequently than females (Epple, 1986; Heymann, 1998), suggesting that these differences can be attributed to sexual selection. The effects of olfactory signals on physiology and behavior may be several-fold and act in both directions. First, the frequency with which individual males scent-mark may provide a signal in itself because it can be positively correlated with dominance status (Kappeler, 1990a; Feistner, 1991). In group-living species, this signal may have an important visual component as well (Mertl, 1976). Second, the composition or quality of male signals may vary as a function of status or condition (Epple, 1978; Fuchs et al., 1991). Third, the frequency with which foreign scents are approached, investigated and sometimes over-marked may also be statusdependent (Heymann, 1998; Kappeler, 1998; Lazaro-Perea et al., 1999). Finally, olfactory signals may be honest signals of a male’s physiological status (Perret, 1992; Kappeler, 1998). A direct function of olfactory signals in intra-sexual selection has so far only been demonstrated unequivocally in gray mouse lemurs, where urinary pheromones of dominant males induce a suite of behavioral, physiological, and morphological responses that reduce the reproductive capacity of naive subordinates (Schilling et al., 1984; Perret and Schilling, 1987a). Much more experimental and fieldwork is required to illuminate this particular function of primate olfactory signals in more detail. 3. Physical Superiority Where males fight for access to receptive females, sexual selection theory predicts that any characteristics, such as large body size and/or weaponry, which give an advantage in competition, will be favored. As a result, most polygynous primates are sexually dimorphic in body size and weaponry. For example, male cercopithecoids are often twice the mass of females (Plavcan and van Schaik, 1997) and possess impressive canines. At the extreme, male mandrills are 3.4 times the mass and 1.3 times the body length of females (Setchell et al., 2001), with a canine crown height of 44 mm (Setchell and Dixson, 2001b). The relationships between mating system, intra-sexual competition, and the evolution of sexual dimorphism in body size and weaponry in primates have been more intensively studied and reviewed than any other topic in primate sexual selection studies (see also Plavcan, 2003). As noted by several authors, tests of the sexual selection hypothesis for the evolution of body size and canine dimorphism are hampered by the use of behavioral indices to estimate the selective pressure of male contest competition and reproductive skew. Instead, various comparative studies have used mating


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system classification (e.g., Clutton-Brock et al., 1977; Harvey et al., 1978; Gaulin and Sailer, 1984; Cheverud et al., 1985; Kappeler, 1990b), behavioral classifications of intra-sexual competition levels (Kay et al., 1988; Plavcan and van Schaik, 1992; Plavcan et al., 1995), or the operational sex ratio (Mitani et al., 1996b) as estimates of the intensity of male competition for mates. Unfortunately, insufficient data are currently available on the individual physical condition of males to relate this to intra-specific variation in actual mating or reproductive success. The inter-specific studies have demonstrated that, as predicted, the extent of dimorphism in body mass and canine teeth is positively related to the level of competition between males. Species in which contest competition is more important are more dimorphic in body mass and canine size than monogamous or polyandrous species, although dietary and energetic constraints, predation pressure, selection on female size, locomotor substrate, allometric effects, and phylogeny have also played a part in the evolution of dimorphism (Coelho, 1974; Leutenegger and Cheverud, 1982; Ely and Kurland, 1989; Clutton-Brock, 1991; Godfrey et al., 1993; Ford, 1994; Martin et al., 1994; Kappeler, 1996; Lindenfors and Tullberg, 1998; Plavcan, 2001, 2003). Finally, it is worth emphasizing in this context that, starting from typically not-very-pronounced neonatal sexual dimorphism (Smith and Leigh, 1998), different developmental trajectories can produce similar manifestations of adult dimorphism in species with similar competitive regimes (Leigh, 1992a, b, 1995; Leigh and Terranova, 1998; Pereira and Leigh, 2003), further demonstrating the far-reaching effects of intra-sexual selection on male life histories. 4. Dominance and Egalitarianism Dominance, the ability to elicit submissive behavior from conspecifics, is typically closely connected to physical superiority. Dominance is frequently used by male primates to obtain and defend access to receptive females (Packer, 1979; Samuels et al., 1984; Shively and Smith, 1985; Bercovitch, 1988). At the behavioral level, this mechanism of reproductive competition is often manifested as mate guarding or consortships. Such temporary associations between a male and a female within a larger group during the female’s period of receptivity have been described in detail for about 20 species of New and Old World monkeys (Dixson, 1998a). However, mate guarding also occurs among many prosimians even though most of them are receptive for only a few hours (Sauther, 1991; Brockman et al., 1998). In species where consortships occur, most copulations take place during this time, thus increasing the consorting male’s probability of mating, in addition to providing an opportunity for preventing rivals from doing so. High-ranking males are more often able to form successful

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consortships (Bercovitch, 1991; Cowlishaw and Dunbar, 1991), but some females form consortships with several different males in succession (Hrdy and Whitten, 1987; Dixson, 1998a; Hrdy, 2000a), indicating that top or high dominance rank does not invariably guarantee priority of access to a given receptive female. Consequently, there has been much debate over the relationships among dominance, mating, and reproductive success in male primates. Much of the available primate literature on this topic uses male copulation success to estimate male reproductive success; however, it is important to emphasize that mating success does not necessarily equal fertilization success. Nor does short-term fertilization success (e.g., across one or a few mating seasons) necessarily equate to male lifetime reproductive success. Several reviews agree that high dominance rank is positively associated with male mating success, but there are populations in which rank and mating success are uncorrelated or even negatively correlated (Fedigan, 1983; Cowlishaw and Dunbar, 1991; de Ruiter and van Hooff, 1993). This variation still needs to be fully reconciled with the priority of access model, the theoretical framework that explicitly describes the relation between rank and mating success, postulating that the dominance hierarchy functions as a queue and that the number of simultaneously fertile females determines male access (Altmann, 1962). A comparative study of variation among species and within groups of the Amboseli population of yellow baboons (Papio cynocephalus) has indicated that group size, and thus the number of competing males, has an important influence on the effectiveness of the queue system (Alberts et al., 2001). In addition, the stability of the dominance hierarchy, in particular that of the top position, has important consequences for priority of access. Moreover, the prevalence of male coalitions, which is dependent on the age distribution and number of high-ranking males, explains an important part of the variation between studies (Noe¨ and Sluijter, 1990; Alberts et al., 2001). Seasonality of reproduction is another explanatory variable because male monopolization potential decreases with increased temporal clumping of receptive females (Paul, 1997; Section VI.A). Finally, it is important to note that rank is a relational variable that changes over an individual’s lifetime, so that variation in lifetime reproductive success as a function of rank may not be as important as indicated by short-term crosssectional studies (Altmann et al., 1986). As a last point, it should be kept in mind that virtually all existing studies of this relationship come from a few Old World monkeys and that the conclusions may change when more platyrrhines and strepsirrhines with different social systems are included. Less is known about the relationship between mating success and reproductive success. Genetic measures of reproductive skew among males


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belonging to the same reproductive unit can help determine this relationship (Johnstone et al., 1999), but they have only been initiated in recent years. In most species examined so far, rank and/or mating success is indeed highly correlated with reproductive success (de Ruiter et al., 1992; Altmann et al., 1997; Borries et al., 1999; Nievergelt et al., 2000; Andre`s et al., 2001). Reduced reproductive skew among males may be due to the success of alternative mating tactics, sperm competition, and/or female sexual strategies, including cryptic female choice (see Section VI.E). Unlike food, fertilizations cannot be shared. Thus, relationships between males tend to be more competitive (van Hooff and van Schaik, 1994) and less affiliative than female relationships (van Schaik and Aureli, 2000). However, males of some species (e.g., spider monkeys (Brachyteles), chimpanzees and bonobos (Pan) ) show more egalitarian relationships where mate guarding is rare or absent and most females mate with most males at least once (Tutin, 1979; de Waal, 1987; Strier, 1996; MatsumotoOda, 1999). Males in these ‘‘male-bonded’’ species are philopatric. There appears to be very little male-male competition and a high level of embracing, grooming, and other affiliative behavior occurs among males, which are often closely related to one another (Goodall, 1986; Kano, 1992; White, 1992; Strier, 1996). At first sight, evidence of intra-sexual selection appears to be minimal in such species. However, male chimpanzees show hierarchical dominance relationships, interfere with copulation attempts by other males, and form coalitions to defend access to estrous females when the number of females is large (Watts, 1998). Male bonobos also show dominance hierarchies although they do not form male-male coalitions, relying on maternal support to attain high rank. High-ranking males appear to attain higher mating success as an indirect consequence of their more central position in their groups rather than as a result of direct contest over access to estrous females (Furuichi and Ihobe, 1994; Kano, 1996; Furuichi, 1997). In contrast to chimpanzees, male northern muriquis (Brachyteles arachnoides hypoxanthus), show no evidence of agonistically-mediated dominance hierarchies, nor of male contest competition for access to mates (Strier, 1990; 1992). However, this is not to say that intra-sexual selection does not act on male muriquis and that competition does not occur between males for fertilizations. Indeed, male muriquis, as well as male chimpanzees and bonobos, have relatively large testes for their body size, reflecting scramble competition for fertilizations between males via sperm competition (van Hooff & van Schaik, 1994; van Hooff, 2000; Section V.C.8). It seems that, in male muriquis, male kin tolerate one another’s sexual activity in exchange for cooperation in competition with neighboring male kin-groups

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over access to females but that male-male competition still occurs, albeit at a post-copulatory level. 5. Physiological Suppression Behavioral inhibition of reproduction in subordinate males in the presence of dominant males may extend to physiological suppression of sexual function in subordinates, although sexual function is unlikely to be completely suppressed in such males. Physiological suppression is characterized by reduced body mass and condition, reduced size of the testes, smaller, less active scent glands, a lack of or reduced development of secondary sexual traits, decreased levels of circulating testosterone, growth hormone and luteinizing hormone, lower frequencies of sexual and olfactory behaviors or any combination thereof (Perret, 1992; Kraus et al., 1999; Maggioncalda et al., 1999, 2000; Setchell and Dixson, 2001b). This form of physiological suppression has so far been documented among lemurs (Microcebus, Propithecus), Old World monkeys (Mandrillus) and apes (Pongo), but it may be even more widespread. In lemurs, there is strong experimental evidence that physiological suppression is mediated by olfactory cues from dominants (Schilling et al., 1984; Perret and Schilling, 1987a, b; Schilling and Perret, 1987; see also Kappeler, 1998), but visual and auditory signals may be more important in other species. Physiological suppression may contribute to the dominants’ reproductive success in several ways. First, subordinate males may suffer a disadvantage in sperm competition in those species where they get to copulate at all. Second, suppression may also result in the suppressed males being less attractive to females (e.g., orangutans: Schu¨rmann, 1982; Utami, 2000; mandrills: Setchell, 1999). However, arresting development of secondary sexual characteristics may represent an adaptive alternative tactic whereby competitively inferior males avoid aggression and the costs of high levels of testosterone for a period (Setchell, 2003). The finding that unflanged male orangutans succeed in siring offspring suggests that arrested development may truly represent an alternative reproductive tactic in this species (Utami et al., 2002). Further data are required to evaluate these possibilities and to explain why and how some males forego reproductive opportunities. 6. Alternative Tactics Males with a disadvantage in a particular competitive arena sometimes have the option to pursue other ways of gaining access to receptive females. Such alternative tactics are mainly behavioral or morphological and may be abandoned or modified with changes in physical or social condition. In highly sexually-dimorphic species, for example, where


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physical superiority and dominance determine access to females, juvenile males may prolong growth and delay maturation to achieve larger size and competitive ability upon entering the mating arena (Alberts and Altmann, 1995a). This delay, which involves greater expenditure, may reduce the risk of damaging aggression from superior rivals. The testes are typically already spermatogenic in maturing males, and as they may obtain a few low-risk sneaky copulations (e.g., rhesus macaques (Macaca mulatta): Berard et al., 1994; mandrills: Setchell, 1999), they may sire offspring during this phase. Several other alternative mating tactics have been reported. First, males in poor physical condition or social position may form coalitions among themselves to force a superior male to relinquish a receptive female. Such coalition partners, which have been well-studied in yellow baboons, for example (Noe¨ and Sluijter, 1990), may take turns in leading the dominant away and copulating with the female (Packer, 1977; Bercovitch, 1988). Under certain conditions, even dominant males may abandon the usual priority of access rule and form coalitions that mate-guard mutualistically (Watts, 1998). Second, in several Old World monkeys (e.g., Cercopithecus spp., Semnopithecus), adult males live more or less peacefully in all-male bands throughout most of the year and raid groups consisting of multiple females and a single resident male during the brief mating season, thereby presumably avoiding the costs of dominance for most of the year (Cords, 1987, 1988, 2000; Borries, 2000). Third, in other species such as certain howler monkeys and gorillas, younger, less powerful males associate with a fully developed male and the group of females associated with him, thereby obtaining occasional mating opportunities with reduced costs of female defense (Eisenberg et al., 1972; Pope, 1990, 1998; Robbins, 1995; Watts, 2000). Fourth, transferring to groups with more favorable reproductive prospects may also be considered as a form of alternative mating tactic (Alberts and Altmann, 1995b; van Noordwijk and van Schaik, 2001, 2003). Finally, by forming friendships with particular females, some males obtain access to at least one female at little risk of aggression from dominant males (Smuts, 1985; Palombit et al., 1997; Pereira and McGlynn, 1997). This list is possibly not exhaustive and it is likely that not all alternative mating tactics of male primates have been discovered yet. In addition, we clearly need more detailed information from long-term studies on their stability and genetic payoffs. 7. Copulatory Behavior Once a male has successfully gained access to a receptive female, several variable aspects of the copulatory act itself may influence its reproductive success. These aspects concern frequency and pattern, and appear to vary

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primarily among species, although intra-specific variation has not yet been studied, to our knowledge. Copulation frequency is highly variable among different primate species. Detailed documentation of mating behavior in wild populations is rare, and most quantitative data focus on the number of ejaculations a male can achieve and not on the number of copulations individual females receive (see Dixson, 1998a). Several studies have pointed out, however, that females may copulate (repeatedly) with 90 to 100% of all resident males on any given day (e.g., Taub, 1980; de Ruiter et al., 1992), and it has been reported, for example, that chimpanzee females can mate up to 4 times with 13 or more males within an hour, adding up to an estimated 6000 or more copulations in a lifetime (Wrangham, 1993)—only to produce an average of 4 or so offspring. Despite the limitations of these data, much of the variation in copulation frequency among species can be explained by the mating system (Dixson, 1995a). In promiscuous species such as ringtailed lemurs (Lemur catta), muriquis (Brachyteles archnoides), stumptail macaques (Macaca arctoides), and bonobos (Pan paniscus), individual males can ejaculate up to 30 times a day, which is in contrast to monogamous and polygynous species with much lower frequencies (1 to 3 ejaculations per day, summarized in Dixson, 1998a). This difference correlates well with that in the intensity of sperm competition, so that frequent copulations may contribute to the reproductive success of individual males, even though the probability of a given ejaculation resulting in a conception is very low. Ejaculations are thus frequent in promiscuously breeding species. However, their sexual behavior is typically concentrated over a relatively short receptive period after which females are pregnant and lactating (Dixson, 1998). As an interesting comparison, callitrichids mate throughout the ovulatory cycle and during pregnancy (Kleiman and Mack, 1977; Kendrick and Dixson, 1983; Stribley et al., 1987), meaning that the annual copulatory activity of socially monogamous species might be well in excess of those promiscuous species who concentrate their sexual activity to a few days each year. Primates also show diverse copulatory patterns, including variation in intromission and ejaculatory patterns; number of thrusts before ejaculation; length of intromission; duration of copulation; and the need for single or multiple intromissions before ejaculation (Dixson, 1998a). Again, the more complex patterns characterized by multiple or prolonged intromissions are primarily, but not exclusively, found in species where females mate with multiple males (Dixson, 1995b, 1997; but see Dewsbury and Pierce, 1989). Some prolonged intromissions, lasting for an hour or even more, may functionally approach mate guarding. Multiple intromissions, in association with pelvic thrusting, may serve to remove sperm plugs


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deposited by previous males or to facilitate sperm transport within the female tract, but there is no evidence yet to test these speculative ideas (see Gomendio et al., 1998). Both of these copulatory patterns may therefore also enhance a male’s success in sperm competition, but the classification and functional interpretation of different patterns remains both poorly documented and controversial (Shively et al., 1982; Dewsbury and Pierce, 1989; Gomendio et al., 1998), providing an important area for future systematic comparisons. 8. Sperm Competition Sperm competition occurs whenever ejaculations from two or more males compete to fertilize the same eggs (Parker, 1970; Birkhead and Hunter, 1990). Compared to other taxa, primates are notoriously promiscuous (Birkhead and Kappeler, 2003). Males may engage in matings with an already-mated female because the costs are sufficiently low and because they will result in paternity probabilities greater than zero. Proceptive and receptive females in many primate species actively seek multiple matings (Hrdy and Whitten, 1987; Hrdy, 2000a), presumably because they can effectively reduce their unusually high risk of infanticide by confusing paternity this way (van Schaik, 2000a; see Section VI.D). Other female benefits include increased mate choice and the opportunity to bias paternity, as well as a reduction of sexual harassment (Drukker et al., 1991; van Schaik et al., 1999; Hrdy, 2000a). Thus, the apparent ubiquity of primate promiscuity may reflect an adaptation to female reproductive interests, as female polyandry is not in the male’s interest. Factors determining success in sperm competition are still poorly known because the mechanisms of sperm competition in primates remain virtually unstudied when compared to birds or insects (Birkhead and Møller, 1998; Birkhead and Kappeler, 2003). However, because of basic similarities in sperm longevity and egg life span with other mammals (Gomendio et al., 1998), it is safe to assume that the timing of an ejaculation relative to ovulation is of greatest importance for its fertilization success (see Huck et al., 1985, 1989). Whether factors other than sperm quantity determine the success of ejaculations of different males deposited during this critical time window in primates remains unknown. The situation in most primates is complicated by the fact that litter size is one and that most males ejaculate repeatedly, so that sequence or timing effects of particular ejaculations are impossible to determine and to distinguish from a raffle (Parker, 1990). Only experimentally controlled matings will provide insights into mechanisms of sperm competition, but the required experimental control is difficult to achieve with most primates.

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Some primates produce a copulatory plug or coagulation of semen in the female’s vagina (e.g., many prosimians, Kappeler, 1997a; mandrill, J. M. Setchell, personal observation; chimpanzee, Dixson and Mundy, 1994). These plugs harden shortly after ejaculation and completely block the female vaginal tract. Dixson and Anderson (2002) have examined the distribution of copulatory plugs across primates, demonstrating that comparative ratings of seminal coagulation are highest in genera where females mate polyandrously and lowest in those where females are unlikely to mate with more than one male per receptive period. These results suggest that seminal coagulation may function as a physical barrier to subsequent matings, and/or that they hamper sperm loss by the female, in which case they may qualify as mechanisms of sperm competition that contribute to the reproductive success of males who deposit a plug. However, observations of plug ejection by female ringtailed lemurs during the approach of another mate (P. M. Kappeler, unpublished observation), plug removal by male and female muriquis to allow further matings (Strier, 1999), plug removal by female mandrills (J. M. Setchell, unpublished observation), and the removal of several plugs with the help of penile spines by male gray mouse lemurs (M. Eberle, unpublished observation) indicate that copulatory plugs may not be very effective barriers. Primates exhibit an array of adaptations to sperm competition that are thought to improve their odds in this competitive arena, primarily by increasing the number and competitiveness of their sperm. First, sexual selection has favored the evolution of larger testes in species where females commonly mate with a number of partners during a single receptive period and the potential for sperm competition is high, whereas testes are smaller relative to body mass in species where females have less opportunity to mate with multiple males (polygynous and monogamous species) (Short, 1979; Harcourt et al., 1981; Kappeler, 1997a). Large testes can produce more and or larger ejaculates (Møller, 1988). Second, the seminal vesicles, which produce the bulk of the fluid proportion of the ejaculate, are larger in species in which females copulate with more than one male (Dixson, 1998b), but little is known about variation in the composition of primate seminal fluid (Dixson, 1998a), which can have marked effects on female reproductive physiology in other taxa (e.g., Johnstone and Keller, 2000). Third, because primates store their sperm in the epididymis, the size of this organ may be even more crucial in sperm competition than the size of the testes. In promiscuous rhesus macaques, epididymis size is indeed strongly correlated with testis size (Bercovitch and Rodriguez, 1993), but data from other taxa are not available for a comparative test of this prediction. Fourth, sperm size and shape varies tremendously among primates and other mammals (Gage, 1998). Sperm


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length, in particular, has been linked to the intensity of sperm competition because longer sperm may have faster swimming speeds and thus a competitive advantage (Gomendio and Roldan, 1991; Dixson, 1993). More recently, it has also been demonstrated that the volume of the midpiece of individual sperm, which is an indicator of mitochondrial loading and thus motility, is greater in primate species in which the females mate polyandrously (Anderson and Dixson, 2002). Whether the individual sperm within an ejaculation (which are on average 50% related) demonstrate cooperation and altruism to gain an advantage in sperm competition (as in the common wood mouse (Apodemus sylvaticus), Moore et al., 2002) is unknown, but a study by Moore et al. (1999) found no evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. The variation across species in size, shape, and spinosity of the primate penis suggests important additional functions apart from simple intromission and sperm deposition. Existing studies indicate that much of the existing inter-specific variation in penile morphology is functionally related to sperm competition. Primate males in species with polyandrous females tend to have a longer and morphologically more complex penis (Dixson, 1987a). There is also some indication that the degree of spinosity is positively associated with a promiscuous mating system (Dixson, 1987b; Verrell, 1992; Harcourt and Gardiner, 1994), although there is a great deal of variation among higher taxa (Harcourt, 1996). Mechanically-stimulating penises may have been favored by female choice because they may act as internal courtship devices (Eberhard, 1990). In addition, penile morphologies vary considerably among species and genera, suggesting a potential function in species recognition, as among sympatric bush babies (Galagidae), for example (Anderson, 2000). Finally, the penis bone or baculum, which is absent only in some New World primates, tarsiers, and humans, is also highly variable in size and shape among the other primates. Here, much of this inter-specific variation is explained by differences in copulatory pattern, with long-intromission species having relatively longer penis bones (Dixson, 1987b). The lack of a baculum in humans has also been explained by sperm competition (Hobday, 2000). To what extent individual variation in primate testes size is positively correlated with competitive potential (rank, body size) on the one hand, and mating and reproductive success on the other hand, independent of potentially confounding co-variables, remains poorly studied and unresolved. For example, in promiscuous savannah baboons, neither body size nor testis size were related to inter-individual differences in male reproductive activity, measured as ejaculatory rate during consort with a fertile female (Bercovitch, 1989). In rhesus macaques, in contrast, testes

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were significantly larger in sires than in non-sires (genetic paternity testing), but testes size was also positively associated with body size, rank, and body condition (Bercovitch and Nu¨rnberg, 1996). Again, additional studies from a wide range of primate taxa are needed to determine general inter-relations among these traits and the potential advantage of large testes size at an individual level. Thus, despite some unfounded skepticism (Brown et al., 1995), and controversial studies of sperm competition in humans (e.g., Baker and Bellis, 1995; Birkhead et al., 1997), virtually all aspects of primate genital anatomy and sperm morphology examined so far appear to be influenced by sperm competition in the predicted direction (Harcourt, 1996, 1997; Dixson, 1998a; Birkhead and Kappeler, 2003). However, many more studies of variation in these and other components of the male genital tract are needed to better understand exactly how they contribute to advantages in sperm competition. 9. Other Post-Copulatory Mechanisms Once sperm from two or more males have been deposited inside a female primate during the critical time window, competition among males is far from over. Sperm from different males compete with those of others (see above), but they may also interact differentially with the female reproductive tract or the eggs, so that some sperm are favored by cryptic female choice (Section VI.E). Even after fertilization has been achieved, male reproductive success can be jeopardized via two additional mechanisms. First, a change in the social environment, usually in the form of the appearance of new dominant males, may induce females to terminate investment in the developing fetus, resulting in implantation failure and pregnancy disruption. Such early infant loss is difficult to detect but has been described for several taxa (baboons: Pereira, 1983; Hanuman langurs: Lhota et al., 2001; humans: Forbes, 1997; rodents: summary in Mahady and Wolff, 2002). This Bruce effect is advantageous for the male inducing it because it will create a mating opportunity in the near future, so that it was originally considered as a product of male-male competition (Trivers, 1972). However, the female is clearly not a passive commodity in this process. Resorption or abortion is considered adaptive from her perspective whenever the risk of infanticide or the loss of paternal care following birth are high (Labov, 1981), so that the benefits from mating with the new male should outweigh any costs of terminating current reproductive investment (Schwagmeyer, 1979) and it may therefore ultimately represent more of a female reproductive strategy.


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Second, males may interfere with the reproductive success of rivals, while at the same time improving their own by committing sexuallyselected infanticide (infanticide by females is discussed below in Section VI.F). The evidence in support of this hypothesis has recently been summarized (van Schaik and Janson, 2000) and is overwhelming. Briefly, males in dozens of primate species have now been observed to kill unrelated dependent infants, leading to a faster resumption of the affected mother’s reproductive activity, thereby creating additional mating opportunities for the male (Hrdy, 1979; Hausfater and Hrdy, 1984; Hrdy et al., 1995; van Schaik, 2000a). Due to their particular life history characteristics, primates are especially vulnerable to infanticide (van Schaik and Kappeler, 1997), but the same principles have been demonstrated in other mammals (van Noordwijk and van Schaik, 2000; van Schaik, 2000c). This strong selective force on male and female reproductive success has shaped many other aspects of primate reproductive physiology and social behavior that have recently been summarized elsewhere (Crockett and Janson, 2000; Nunn and van Schaik, 2000; Palombit, 2000; Paul et al., 2000; Steenbeck, 2000; Sterck and Korstjens, 2000; van Schaik et al., 2000). D. Paternal Care Paternity does not necessarily translate into successful offspring, and a primate male’s role in reproduction does not necessarily end when he successfully fertilizes a female. For the male to realize his own reproductive success, the resulting offspring must survive to maturity and themselves reproduce. In species where ‘‘single mothering’’ is sufficient and males do not contribute to the survival of offspring once they are conceived, male-male competition is sufficient to describe male reproductive strategies. However, if a male is essential in some way either for infant survival or as a protector for offspring, the copulatory imperative is less strong and, where males can influence the survival and reproductive success of their offspring, male reproductive strategies include paternal investment in offspring. For example, callitrichid males show extensive infant care (Goldizen 1987, 1988; Rylands 1986; Heymann 1990a), female reproductive success (infant survival) correlates with the number of adult males present in a group (Garber et al., 1984; Koenig, 1995), and cooperation between males may be required for successful rearing (Heymann, 1998). A further example of the requirement for paternal care occurs in mountain gorillas. In this species, young males can only achieve reproductive control of a group of females if their fathers survive to their son’s maturity (Robbins, 1995). In terms of offspring protection, paternal investment is thus necessary right through to sexual maturity of

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the offspring. Males may also increase the survival of their offspring by protecting them from other infanticidal males (van Noordwijk and van Schaik, 1988; Palombit et al., 1997), or by warming them or protecting them from other dangers (e.g., Fietz, 1999b). In situations where paternal care is essential in the survival and eventual reproduction of offspring, relationship-building between males and females, and between males and offspring, is important for both sexes to gain maximum reproductive success. In this way, sexual selection has driven the evolution of nuturing positive relationships between male and female primates in which grooming and nonconceptive sexual behavior appear to function as social reward (Section VI.C), in contrast to the violence of sexually selected male infanticide and sexual coercion. E. Do Male Primates Show Mate Choice? Even though female primates invest substantially more in reproduction, copulation may still be costly for males. Males risk injury in contests (Drews, 1996) and expend time and energy searching for and guarding mates (e.g., Alberts et al., 1996). Moreover, sperm production is costly and sperm delivery is compromised by successive ejaculations (Dewsbury, 1972; Preston et al., 2001; Wedell et al., 2002). Where the costs of reproduction are high and females differ in quality, males should compete selectively to maximize the benefits of their mating efforts and allocate their copulations so as to maximize fertilization probabilities. In other words, males should choose to compete for receptive females that will accept their mating attempts and that are likely to conceive and produce surviving offspring. There is evidence that male primates do indeed distribute mating efforts according to the likely fertility of females. For example, dominant male rhesus macaques (Chapais, 1983), baboons (Smuts, 1985), chimpanzees (Tutin, 1979), and mandrills (Setchell, 1999) concentrate their mating attempts when a female is most likely to ovulate, and males may compete more intensely for access to such females under certain conditions (e.g., Domb and Pagel, 2001; Zinner et al., 2002). Males may also show less sexual interest in adolescent, nulliparous females, by comparison with females who have already produced at least one infant (e.g., baboons: Smuts, 1985; mandrills: Setchell, 1999). This is likely due to the fact that adolescent females are typically less fertile and less adequate mothers than older, experienced females (Altmann, 1980). Males may also prefer to mate with high-ranking females (reviewed by Berenstain and Wade, 1983), which may be more fertile and able to invest more in resulting offspring (e.g., van Noordwijk and van Schaik, 1999; Setchell et al., 2002). Male primates both in the wild and in captivity also show strong mating


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preferences that are unrelated to female age, rank, or menstrual cycle stage, which may reflect long-term relationships (Takahata, 1982a, b; Chapais, 1983; Smuts, 1985, 1987; van Schaik and Aureli, 2000). Strategic mate choice by male primates has been directly demonstrated in a series of experiments with captive rhesus monkeys recently summarized by Wallen (2001). When kept as male-female pairs, some mating occurred on every day of the female’s cycle (Goy, 1979). However, when multiple females were kept with a single male, mating was limited to the fertile period of each female’s cycle (Wallen et al., 1984), demonstrating that male sexual capacity is limited and that such proximate limitations can contribute to mate selectivity. Callitrichids present a special case where reproduction is costly for males. In these species, males invest heavily in individual offspring (via paternal care: Sanchez et al., 1999; Achenbach and Snowdon, 2002), and choice of mate is therefore important for males. Heymann (1998) proposes that scent-marking in callitrichines represents a secondary sexual trait and that the degree of sex-bias in rates of scent-marking depends on the degree of female intrasexual competition. Female-biased rates of scent-marking are found in those callitrichine species where male investment in infant carrying exceeds female investment, and no sex bias is found when investment by males and females is equal. Males may choose females then on the basis of signal quality. A great deal of work has focused on mate choice and advertising in humans, showing that males prefer females with traits that signal reproductive potential and youth (Buss and Schmitt, 1993; Tesser and Martin, 1996). Thus men prefer signals of youth and physical attractiveness, such as ‘‘baby face’’ features (large eyes and a small nose, Cunningham et al., 1995). Men also seek an optimum waist-to-hip ratio in their partners, a trait associated with better health status and greater reproductive capacity (Singh, 1993). Interestingly, and in accordance with theories of parasite-mediated sexual selection, physical beauty is most important in cultures where parasitic infection is prevalent (Gangestad and Buss, 1993). Furthermore, secondary sexual features are hormonedependent, and individuals with signals that require high hormone levels are thus demonstrating the ability to withstand the compromising influence of steroid hormones on their immune system. The fact that these characteristics are attractive to the opposite sex is the only evidence available as yet for primates in support of the immunocompetence handicap hypothesis (Folstad and Karter, 1992). However, studies of human mate preference generally involve college students responding to questionnaires. Whether this self-reported mate preference is related to actual reproductive outcomes remains unknown (see Section VI.D.3).

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F. Summary of Sexual Strategies in Male Primates In summary, male primates compete for access to females and their gametes; however, they also show mate choice and parental care for infants where doing so improves their reproductive success. Male competitive strategies (contest or scramble) include a range of mechanisms before and/or after copulation that typically have an impact on rivals but can also affect mates. Male strategies are dependent on the defensibility of females, which is in turn dependent on female spatial distribution, synchrony of receptive cycles, and female behavior. Furthermore, females employ a range of behavioral and physiological strategies that act to manipulate males, altering the costs and benefits of various male reproductive strategies, which include timing of sexual activity, advertisement, and mate choice. In the following section, we take the female perspective and examine female reproductive strategies. The effects of these strategies may act in concert with, or oppose the effects of competition between males. Where female sexual strategies act against those of males, this brings the sexes into direct conflict over reproduction, as discussed in Section VII.

VI. The Female Perspective: Biasing and Confusing Paternity Because of their relatively slow life-histories, female primates invest heavily in a limited number of offspring. Consequently, to maximize their reproductive success, females are expected to benefit from conceiving with the best male, gaining good genes and (in some species) various male services. However, while females may want to bias paternity in favor of a particular male with a preferred phenotype or genotype, or both, there is an emerging consensus that female primates mate polyandrously to reduce the risk of infanticide for their offspring by confusing paternity (van Schaik, 2000a; van Schaik et al., 2000). Thus, female primates find themselves in a dilemma. Although confusing paternity is to the advantage of females in reducing the risk of sexually selected infanticide, sexual selection still drives females to concentrate matings on a preferred male when they are most likely to conceive. If other males can determine when ovulation occurs and determine their own probability of paternity, this will counter the females’ paternity confusion strategy. Thus, in species in which male infanticide poses a serious potential threat to infant survival, females are expected to adopt strategies that will both confuse and bias paternity (van Schaik, 2000a; van Schaik et al., 2000). Finally, much attention has focused on infanticide by males, but females may also kill


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other female’s infants and, in some species, female infanticide is more important than infant killing by males (Digby, 2000). Thus, females of some species must also employ strategies to reduce the risk of infanticide by competing females. In this section we review the sexual strategies employed by female primates and the potential for female choice under various conditions. A. Constraints on Female Choice Returning to our analysis of primate social organization, this time from the female perspective, we find that as with males, social organization both constrains and results from female reproductive strategies. As in males, the number of individuals of the same and opposite sex that live together has important consequences for female reproductive strategies. Primate species can be divided into those where females mate with only one male per cycle (monandry), and those where females mate with more than one male per receptive cycle (polyandry), producing very different scenarios for female choice. Where females are dispersed, they may only have the option of mating with the single dominant male that has an overlapping home-range, with no role for either pre- or post-copulatory female choice. However, in many cases, females can alter the pay-offs of male strategies by choosing to accept mating attempts from subordinate males employing alternative sneak strategies, with the potential for both paternity confusion and cryptic female choice. Females may also be able to prevent a single male from monopolizing mating opportunities by clumping their receptive periods in space and time (e.g., Eberle and Kappeler, 2002). Where a single dominant male is unable to monopolize a female’s home range, a receptive female may mate with many males that scramble for access to her, giving rise to opportunities for both pre-copulatory and, perhaps more importantly, cryptic female choice. Where females live as a pair with one male (social monogamy), the quality of that individual male, or of his territory, may be very important to the female’s reproductive success, selecting for competition between females for high quality mates. At first glance, there would seem little opportunity for mate choice once a female has paired with her mate. However, the increasing evidence for extra-pair copulations and paternity in such primate species suggest that both pre- and post-copulatory female choice may be more important here than previously thought (see also Birkhead and Kappeler, 2003). In the rare cases where a single female lives and mates with several males (polyandry), this promotes cryptic female choice between the sperm

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of multiple partners. Further, if the presence of a number of males has a positive influence on female reproductive success (by providing direct benefits such as care of offspring), then females are expected to compete for extra males. Moving on to group-living females, where a single male succeeds in sexually monopolizing a group of females (a harem), females mate monandrously. Similarly, within multi-male, multi-female social groups, mating opportunities may be monopolized to a greater or a lesser extent by a single dominant male. Here, and in any such situation of sequential polyandry, female choice is constrained by male tactics, in particular the risk of infanticide. Measuring the magnitude of infanticide risk in a primate population is problematic. Great variation occurs in rates of infant mortality due to infanticidal attack between species, study groups, and over time within the same study group (e.g., due to changes in male status) (van Schaik and Janson, 2000). Furthermore, the ‘‘risk’’ of infanticide is likely to be seriously underestimated by measures of directly observed cases in wild populations due to the confounding effects of female counterstrategies acting to lower infanticide risk. Janson and van Schaik (2000) provide realistic (not conservative) estimates of rates of infanticide per infant born in wild populations for 16 species of anthropoid primate. These estimates range from close to zero in some studies to 50% in others, and a recent critical evaluation of the sexually-selected infanticide hypothesis (see Section V.C.9) concludes that infanticide by males can be a major source of infant mortality in many primate species (van Schaik, 2000a). Hence, females are predicted to employ strategies to promote polyandrous mating in order to avoid the risk of infanticide by non-sires. For example, females can alter the timing of their sexual activity by synchronizing their receptive periods, advertising their receptive period to multiple males, concealing the exact timing of ovulation, and mating over a longer period than simply the peri-ovulatory phase (van Schaik et al., 1999). Further, females may exhibit choice for subordinate males pursuing alternative strategies. In both harem social systems and multi-male, multifemale groups, it is important to consider the presence of potential mates (and potential infanticidal males) beyond the limits of the group. For example, one-male, multi-female groups of both hamadryas baboons and proboscis monkeys (Nasalis larvatus) regularly come together in larger social groups (Stammbach, 1987; Yaeger, 1990), and multi-male influxes occur during the mating season in Hanuman langurs and some guenon species (Borries, 2000; Cords, 2000), leading to polyandrous mating by females. Finally, where multiple females live in groups with, and mate with, multiple males during a single fertile period, there are opportunities for both pre-copulatory and cryptic female choice.


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Females provide the bulk of parental care in the large majority of primate species. Thus, in theory, females might be expected to allocate their parental investment according to context, including the identity of the sire (Qvarnstrom and Price, 2001). For example, in cases where the risk of sexually selected infanticide is high and females are unable to reduce this risk by confusing paternity, then in the presence of a new male, it may benefit the female to terminate investment in a fetus that is likely to fall victim to infanticide. Indeed, takeovers have been observed to induce spontaneous abortions in pregnant females (Hanuman langurs: Agoramoorthy et al., 1988; captive hamadryas baboons: Colmenares and Gomendio, 1988; geladas: Mori and Dunbar, 1985). Further, where male strategies constrain female choice and females are obliged to reproduce with sub-optimal males, females might be predicted to compensate for this potential loss of fitness by varying parental care (Qvarnstrom and Price, 2001). In the following section, we examine the female strategies and mechanisms outlined above that allow female primates to influence which male eventually fertilizes their ova. We discuss the sort of evidence that will be required to demonstrate the consequences of such mechanisms, and the data that are currently available. We will show that a great deal less is known about female sexual strategies than about those of males, and that this is an area ripe for investigation. B. Timing of Sexual Activity Females can manipulate their spatial and temporal distribution, reproductive physiology, and mating behavior in order to promote mating with multiple males during a single cycle. This enhances opportunities for female choice and polyandrous mating (and therefore cryptic female choice), and also counters the threat of sexually selected infanticide by males by distributing paternity chances among the mates. However, these benefits of permanent associations with other males and females are checked by a concomitant increase in feeding competition within social units (Sterck et al., 1997). 1. Seasonality and Synchrony of Female Receptivity Where receptive females are clumped in space or time, a male that tries to monopolize one female will forfeit the opportunity to fertilize others. Seasonality and synchrony of receptivity thus reduce the ability of one male to monopolize all the females in an area (e.g., Zinner et al., 1994) and females have additional opportunities to mate polyandrously. Strict seasonality may itself serve to reduce the risk of infanticide if the death of an infant does not

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shorten a female’s inter-birth interval. However, a female that has lost the previous infant may still have more resources to invest in subsequent offspring, meaning that infanticide may still pay off for the male. 2. Lengthened Receptive Periods By comparison with most mammals, catarrhine ovarian cycles are characterized by long follicular phases and extended mating periods (Hrdy and Whitten, 1987; Martin, 1992). Indeed, the follicular phase in catarrhines is twice as long as in platyrrhines or prosimians (van Schaik et al., 2000). This phenomenon is costly, as mating activity decreases the time available for other activities and increases risks of harassment, predation, and disease transmission (Smuts and Smuts, 1993; Manson, 1994; Alberts et al., 1996; Soltis et al., 1997a,b; Nunn et al., 2000; Nunn and Altizer, 2003). Furthermore, an increased likelihood of fertilization of aged gametes leads to higher probabilities of pregnancy failure or embryonic abnormalities (German, 1968; Austin, 1970). van Schaik et al. (1999, 2000) have proposed that lengthy follicular phases represent a female strategy to reduce male monopolization and increase the number of males with a possibility of paternity, and thus reduce infanticide risk. Where males face a choice between synchronously receptive females, the optimal strategy for the dominant male is to mate-guard each female at her peak fertile period. The longer the duration of this period, the less likely is a male to successfully guard his mate and the more costly guarding becomes to the male. Thus, the longer the receptive period, the more likely it is that other males will also mate with the female while the dominant male is pursuing other females, thereby confusing paternity and lowering infanticide risk. This argument predicts that the receptive period will be longer in species in which there is high vulnerability to infanticide by males. However, precisely because females employ a counter-strategy to lessen the risk of infanticide, we cannot necessarily expect to find a relationship between the frequency of infanticide and the length of the receptive period. Instead, van Schaik et al. (1999, 2000) have used a measure of infanticide ‘‘risk’’ (rather than direct observations of actual occurrence of infanticide) to show that species in which males attempt to monopolize females by mateguarding and where the risk of sexual coercion is high, female receptive periods are markedly longer than in species where females are able to control mating interactions (van Schaik et al., 1999, 2000). 3. Unpredictable Ovulation In situations where females are unable to control mating, they may still be able to control the information available to males concerning paternity. Male mammals apparently cannot recognize their offspring (Elwood and


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Kennedy, 1994), even though odor-based individual recognition is rather sophisticated in some taxa (Hurst et al., 2001). A male’s assessment of his paternity chances are therefore presumably based on his mating history with the mother, and in particular, the proximity of mating to cues of ovulation in the female. By making the exact timing of ovulation unpredictable, females can therefore prevent males from accurately ascertaining their probability of paternity and protect their offspring from the risk of sexually selected infanticide (van Schaik et al., 2000). Investigations of whether males are able to detect ovulation require a combination of behavioral (distribution of matings) and genetic (paternity) data with female steroid profiles in order to determine the time of ovulation (e.g., Ziegler et al., 2000; Heistermann et al., 2002). Studies combining behavioral and hormonal data have shown that female sexual behavior and advertisement are not strictly related to ovulation (see below; Zinner et al., 2003), suggesting that a lengthened period of receptivity does indeed act to confuse paternity. If ovulation is truly concealed from males, and paternity confused, then this should result in at least some reproductive success for non-dominant males. These female strategies may go some way towards explaining the effect that paternity data do not always fit the priority of access model (Altmann, 1962; see above, Section V.C.4). However, such strategies are not apparent in all species and honest cues to ovulation have been shown to exist in callitrichids. Studies of cotton-top tamarins (Ziegler et al., 1993), pygmy marmosets (Converse et al., 1995), and common marmosets (Smith and Abbott, 1998) have shown that males are able to discriminate odors of ovulating females, although they still mate with their partners throughout the ovulatory and pregnancy cycle. In addition to confusing paternity by lengthening the period of sexual activity around ovulation, females of many primate species also manipulate male paternity assessment by mating post-conception, showing receptive periods when they are already pregnant and therefore unable to conceive (reviewed in van Schaik et al., 1999). In particular, in species in which infants sired by a previous male are vulnerable to infanticide after group take-over by a new male, females that are already pregnant undergo ‘‘pseudo-estrus’’ and solicit the new male for mating (Hrdy, 1979; Hrdy and Whitten, 1987; van Schaik et al., 1999). If males are unable to detect ovulation, this strategy may act to confuse paternity and avoid the risk of infanticide (reviewed by Smuts and Smuts, 1993), and is less costly to the female than terminating investment in a fetus that is likely to be the victim of infanticide post-parturition. Evidence as to whether this strategy works to avoid infanticide relies on observations of the fate of infants born following male take-over. Some studies have demonstrated

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that post-conception mating does appear to protect infants against infanticide, with the effect decreasing as pregnancy advances (Struhsaker and Leland, 1985; Sommer, 1994; Fairgrieve, 1995), although other studies have failed to show that post-conceptive mating effectively protects against infanticide (Borries et al., 1999). Finally, females may modify their reproductive timing in response to infanticide risk by resuming receptive cycles earlier after a male takeover than otherwise (Sigg et al., 1982; Mori and Dunbar, 1985; Colmenares and Gomendio, 1988; Winkler, 1988), although the evidence for this strategy is equivocal (Smuts and Smuts, 1993). C. Female Advertisement A female primate needs to mate only once with one male at the optimum stage of her reproductive cycle to conceive each infant. However, polyandrous mating is widespread among primates (Hrdy, 1981; van Noordwijk and van Schaik, 2000; Birkhead and Kappeler, 2003). Moreover, females of many species advertise impending ovulation with prominent behavioral (e.g., proceptive displays), visual (e.g., sexual swellings), acoustic (copulation calls), or olfactory signals (reviewed by Dixson, 1998a), which are broadcast to multiple males. Mating (and seeking to mate) with multiple males requires explanation, as it is costly to the female in terms of the investment of time and energy in sexual behavior, risks of harassment from other individuals or predation while mating, risk of disease transmission, and potentially negative effects of male seminal fluid (Smuts and Smuts, 1993; Manson, 1994; Soltis et al., 1997a,b; Johnstone and Keller, 2000; Nunn et al., 2000; Nunn and Altizer, 2003). We have seen that one potential benefit of mating with multiple males is paternity confusion, thereby lessening the risk of infanticide (Hrdy, 1979). Further suggested benefits of polyandrous mating in female primates include indirect mate choice via incitement of male-male competition (e.g., Clutton-Brock and Harvey, 1976; Hamilton and Arrowood, 1978; Hauser, 1990; Wiley and Poston, 1996) and increased offspring fitness by increasing the number of potential sires that compete and promoting sperm competition and cryptic female choice (Harvey and May, 1989). These hypotheses are not necessarily competing alternatives; for example, females may attract multiple males, distributing paternity chances among those that mate successfully, thereby promoting indirect pre-copulatory mate choice via male-male competition, sperm competition, and cryptic female choice between the ejaculates of successful males. However, mate choice hypotheses can only explain polyandrous mating during the fertile


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period, yet female primates also mate with multiple males outside the fertile period. These matings are costly but cannot be explained by either pre- or post-copulatory female choice (Soltis, 2002). Hypotheses proposed concerning the potential benefits of such non-procreative multiple matings include: ‘‘prostitution’’ for immediate resources (Symons, 1979); gaining parental investment from multiple males (e.g., Taub, 1980); fertilization insurance (Soltis, 2002); recruitment of males for group defense (Wrangham, 1980); avoidance of the costs of sexual coercion (i.e., females have no choice but to mate with any male that solicits mating: Smuts and Smuts, 1983); pure ‘‘fun’’ (Small, 1993); spite (depleting the sperm available for rival females: Small, 1988); and social reward, where sexual contact during non-conceptive periods is hypothesized to function in a similar manner to grooming and huddling, thus reinforcing male-female relationships in species for which such relationships are important (see Section V.D.). Soltis (2002) has reviewed these proposed explanations for polyandrous mating in primates, concluding that although gains in paternal investment may explain polyandrous mating in callitrichids (see Soltis and McElreath, 2001), paternity confusion (Hrdy, 1979), with the potential for cryptic female choice, appears to be the most likely explanation for pronounced polyandrous mating in large social groups of primates. If females advertise their receptivity in order to solve the ‘‘female’s dilemma’’ by attracting and mating with multiple males (confusing paternity), while at the same time biasing the chances of preferred males to sire the resulting offspring, then this predicts that ovulation should be related to advertisement, but with built-in unpredictability or ‘‘error’’ (Nunn, 1999a). This hypothesis, supporting evidence, and resulting predictions have been developed in detail by Nunn (1999a, see also Zinner et al., 2003) to explain the evolution of sexual swellings, but (as Nunn points out) it is equally applicable to olfactory and vocal signals. According to this ‘‘graded signal’’ hypothesis, the distribution of female advertisement should represent the probability of ovulation. Females thus manipulate male behavior by altering the costs and benefits of mateguarding, such that dominant males guard at the time when the female is most likely to ovulate, while other males mate at sub-optimal times when there is a smaller (but finite) chance of fertilizing the female. The female signal is thus ‘‘honest enough’’ to give the dominant male a reasonable degree of paternity certainty while leaving other males with a smaller (but greater than zero) probability of sirehood. This predicts that paternity will be concentrated on the dominant male, but that a percentage of offspring will be sired by other males in the group. ‘‘Bias and confuse’’ hypotheses for the evolution of female reproductive strategies also predict outcomes for individual females. For example, if females mate multiple times in

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order to confuse paternity, then the offspring of those females that mate with fewer males, and specifically those females that do not mate with males that subsequently become dominant, should be more vulnerable to infanticide than the offspring of females that mate with many males. 1. Proceptive Behavior Female primates actively solicit copulations from males around their likely conception date (Janson, 1984; Gangestad and Thornhill, 1998; Zehr et al., 2000), and show increased frequencies of particular behavior patterns during the peri-ovulatory phase (Carosi and Visalberghi, 2002). In an elegant study combining behavior, endocrinology, and genetic paternity determination, Heistermann et al. (2002) have examined relationships among mating behavior, timing of ovulation, and paternity outcome in Hanuman langurs, showing that females have variable and extended receptive periods (4–15 days), within which the timing of ovulation was extremely variable (from the first day to the last day of receptivity). Behavioral data suggested that ovulation was concealed from males in this species, and although dominant males monopolized females to a high degree, a substantial proportion of offspring were sired by other males. Thus, proceptive behavior in female Hanuman langurs conceals the exact timing of ovulation and is an effective strategy for paternity confusion. This study provides the first direct evidence in support of the hypothesis that extended receptive periods act to confuse paternity in catarrhine primates. 2. Visual Signals The evolution and adaptive significance of female sexual swellings has received a great deal of attention (reviewed by Nunn, 1999a; Stallmann and Froehlich, 2000; Snowdon, 2003; Zinner et al., 2003). These prominent and conspicuous swellings of the perineal skin occur in the females of many Old World primate species, reaching maximum size around the time of ovulation (Dixson, 1983). They are found mainly in species where females actually, or potentially, mate with more than one male during a receptive period (Clutton-Brock and Harvey, 1976; Dixson, 1983; Hrdy and Whitten, 1987; Nunn, 1999a), are hormone dependent (Dixson, 1983), attract males for mating independently of olfactory or behavioral cues (Bielert and Anderson, 1985), and are likely to be costly to the females (Nunn et al., 2001). A recent field study by Domb and Pagel (2001) found support for the ‘‘reliable indicator’’ hypothesis (Pagel, 1994), which proposes that sexual swellings can be regarded as costly handicaps that honestly signal female quality. Domb and Pagel (2001) suggested that sexual swellings in wild


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female baboons reliably advertise a female’s reproductive value over her lifetime, and that males use swelling size to determine their reproductive effort. However, only one of three measures of swelling ‘‘size’’ was significantly correlated with female reproductive history, and Zinner et al. (2002) have shown that this correlation is no longer significant if the data are re-analyzed, taking into account several flaws in the original analysis, including intra-individual variability in swelling characters, the co-variate body size, and variation in demography and food availability between the five baboon groups studied. Synchronously mating females were also excluded from the original analysis, although investigation of overlapping estrous cycles might be expected to show the strongest patterns of male mate choice for large swellings. Domb and Pagel (2002) have replied to these criticisms, but the findings remain controversial. Comparative tests also fail to support the ‘‘reliable indicator’’ hypothesis, as sexual swellings are not associated with increased female mating competition (Nunn et al., 2001; Zinner et al., 2003). The most likely proposed explanation for the evolution of exaggerated sexual swellings is that they present the probability of ovulation for an individual female along with a higher probability indicated by a larger swelling (the bias and confuse hypothesis mentioned above: Nunn, 1999a; Zinner et al., 2003). In support of this hypothesis, Nunn (1999a) shows that swellings gradually increase in size, and that ovulation is most likely at peak swelling, but that this association is not perfect. Males can therefore only judge the probability of ovulation occurring from swelling size rather than its exact timing. Dominant males mate-guard females at peak swelling, when they are most likely to ovulate, while subordinate males tend to mate outside the peak swelling when ovulation is less likely, but still possible. Tests of this hypothesis will require investigation of the endocrine correlates of swelling size to determine whether swellings are indeed a probabilistic signal of ovulation (e.g., Aujard et al., 1998; Reichert et al., 2002), as well as genetic investigations to test the prediction that paternity should be biased towards the dominant male, yet other males should have small pay-off in order to prevent the risk of infanticide. 3. Auditory Signals Auditory signals may ultimately also act to bias and confuse paternity by attracting males and signaling particular reproductive states. In support of this hypothesis, O’Connell and Cowlishaw (1994) have shown that copulation calls increase in length as females approach ovulation, and are longest at the most likely time of ovulation. Further, Semple (1998; Semple and McComb, 2000) has demonstrated that male Barbary macaques (Macaca sylvanus) can discriminate between female copulation

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calls given at different stages of the estrous cycle, responding more strongly to those given around the time when conception is most likely to occur. Calls also affect patterns of male reproductive behavior, not only by promoting pre-copulatory competition between males, but also by promoting sperm competition by reducing the interval between copulations. Finally, in some nocturnal prosimians, estrous females emit specific calls (Stanger, 1993, 1995) that presumably attract males from far afield and therefore have the potential to increase the probability of polyandrous matings. 4. Olfactory Signals Female primates scent-mark using cutaneous glands, urine, and genital secretions (Dixson, 1998a), and changes in these chemical signals can advertise reproductive status (Epple, 1986; Converse et al., 1995; Kappeler, 1998). For example, females of several lemur species mark more when they are receptive than at other times (Schilling, 1979; Kappeler, 1988; Buesching et al., 1998); and male common marmosets can discriminate between the odors of peri-ovulatory and anovulatory females (Smith and Abbott, 1998). Even in Old World monkeys, which lack a functional vomeronasal organ, males frequently smell the female’s perineum or touch her and sniff their finger (Dixson, 1998a). Thus, olfactory signals may act to attract multiple males to mate with the receptive female, promoting indirect mate choice (through male-male competition), direct mate choice, and post-copulatory mate choice if females mate with more than one male.

D. Female Choice Traditional sexual selection theory predicts that female primates should base their mating decisions on the quality of prospective males, choosing the sire of their offspring for direct benefits (resources, protection), or for indirect, genetic benefits (‘‘good genes’’ or attractive offspring). Previous reviews have demonstrated that female primates show mate choice, although they have reached differing conclusions as to its evolutionary importance (Hrdy, 1981; Cords, 1987; Smuts, 1987; Small, 1989; KeddyHector, 1992; reviewed in Paul, 2002). Much theoretical and empirical progress has been made since the majority of these reviews were published, and considerable evidence now exists that mate choice provides female primates with important direct and indirect benefits (Paul, 2002). However, Paul (2002) also points out that the functions and evolutionary consequences of mate choice are still to a large extent unclear.


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Unlike what was commonly assumed in the early days of primatology (e.g., Crook, 1972), female primates exhibit choice in both proceptive and receptive behaviors, as first forcefully pointed out by Hrdy (1981, 2000a). Proceptive choice occurs where females actively solicit copulations from some males, but not from others (e.g., orangutan females solicit more copulations from fully developed ‘‘flanged’’ adult males than from ‘‘unflanged’’ males: Utami and van Hooff, 2003). Receptive choice occurs where females reject the mating advances of certain males, yet mate with others (e.g., female chimpanzees accept mating invitations from some males but ignore others: Tutin and McGinnis, 1981; Goodall, 1986). These are choices related directly to mating partners but females may also exert mate choice by influencing male group membership (e.g., vervets: Raleigh and Macquire, 1990), choosing which group to join in species in which females disperse (e.g., Sterck, 1997) and engaging in extra-group copulations (e.g. callitrichids: Digby, 1999; Lazaro-Perea, 2001). Finally, female mate choice is not restricted to active discrimination between potential mates (Wiley and Poston, 1996). Strategies such as synchrony of receptive periods and sexual advertisement may also represent examples of ‘‘indirect female choice’’ where females incite male-male competition, with the result that only ‘‘winners’’ gain access to the receptive female (e.g., Clutton-Brock and Harvey, 1976; Hamilton and Arrowood, 1978; Hauser, 1990). Studies of mate choice in primates are hampered by the interaction of female choice with other male and female strategies. For example, we have seen that paternity confusion strategies may act to promote polyandrous mating with as many males as possible, and male strategies may limit female options to mating with only one male or no male at all, whatever the female’s preference criteria (Gowaty, 1997). Thus, when examining the criteria on which females base mate choice it is important to differentiate between female choice and female preference (Halliday, 1983; Soltis, 1999). Mate choice is constrained by the social environment and can be observed under natural conditions. On the other hand, underlying mate preference, free of other constraints, can only be studied experimentally (e.g., Keddy, 1986; Keddy-Hector, 1992; Moore et al., 2001). A further complication of mate choice studies lies in the choice of behavioral measures of female preference. To qualify as an indication of mate choice, a behavior must influence reproductive outcomes, such as the probability that the male and female will produce offspring (Fisher, 1958; Snowdon, 2003). However, disentangling the influence of male and female strategies on reproductive outcomes is challenging (e.g., Manson, 1995; Soltis et al., 1997a, b, 2001).

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1. Female Choice for Direct Benefits With the exception of humans (see below), there is little evidence that female primates choose mates for resources (unlike choice for nuptial gifts in insects or territories in birds). However, very little is known about partner selection in monogamous primates, and it is possible that females may choose a male for his ability to defend a territory (Smuts, 1987). Where direct paternal care occurs (e.g., in siamangs, owl monkeys, titi monkeys, and callitrichids), female choice of mates may be based on male ability to invest in offspring (Hrdy, 1981; Keddy-Hector, 1992), but again, little is known about mate choice in these species. In callitrichids, where female reproductive success is limited by parental care (Garber, 1997), females might be expected to show a preference for mating with males that demonstrate infant care. However, it remains unclear whether this is indeed the case (e.g., Price, 1990; 1992; van Schaik and Paul, 1996/1997; Tardiff and Bales, 1997). Males also appear to contribute to infant care in some multi-male, multifemale groups, by protecting or occasionally carrying infants. This can be seen as paternal investment, and therefore of direct benefit to the female, if males increase the survival of their own offspring by protecting them from infanticidal males (Palombit et al., 1997), or as a mating strategy if females choose to mate with males that have previously demonstrated infant care (Keddy-Hector, 1992; Smuts and Gubernick, 1992; van Schaik and Paul, 1996-1997). These two hypotheses are not mutually exclusive, but only the first requires that the male be related to the infant. Examples of male care in multi-male, multi-female groups include dominant, or previously dominant, male long-tail macaques and male ‘‘friends’’ in baboons. In both cases, the males concerned have a high probability of paternity (van Noordwijk and van Schaik, 1988; Palombit et al., 1997). In twinning callitrichids, however, all males invest heavily in infant care, although the only existing genetically-determined paternity study found that paternity was concentrated on the behaviorally-dominant resident male (Nievergelt et al., 2000). 2. Female Choice for Indirect Benefits Where males contribute little else but their genes to their offspring and females show choice, it may be for males that will pass on ‘‘good genes’’ to their offspring. Evidence for this is still slim in primates, and Bercovitch (1995) has suggested that the survival of individual offspring will be a more important influence on the reproductive success of female primates than mate quality, casting doubt on the evolutionary significance of mate choice for male genes. However, some evidence of female choice for dominant or


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ornamented males suggests that choice for ‘‘good genes’’ may be important in female primates. Furthermore, females may choose for genetic compatibility (e.g., Sauermann et al., 2001), rather than for particular ‘‘good genes’’ (Trivers, 1972; Brown, 1997; Zeh and Zeh, 1997; Penn and Potts, 1999), leading to individual variation in mate preferences between females. Females might be expected to prefer to mate with males of high status, as dominance may signal high genetic quality and the ability to accrue resources. In support of this, a number of studies show that females choose to mate with dominant males. For example, female brown capuchins (Cebus apella) solicit the dominant male exclusively during their fertile period and solicit other males only during less fertile periods (Janson, 1984; Welker et al., 1990). Female vervet monkeys also prefer dominant males to subordinate males (Keddy, 1986). Although dominance status changes over a male’s lifetime (Altmann et al., 1996), not all males will become dominant during their careers, meaning that a female is indeed choosing a superior male. However, female capuchins cease to choose a male when he loses dominant status (Janson, 1984), suggesting that there may be other reasons (in addition to genetic quality) for choosing the dominant male, including direct benefits such as protection from sexual coercion, harassment or infanticide (e.g., Pope, 1990; Pereira and Weiss, 1991). It seems likely that arbitrary phenotypic traits may be less important in primate female choice than in other taxa, as females generally know their potential mates from regular interactions as a result of long-term association (Kappeler and van Schaik, 2002). However, if the spectacular ornaments of some males do demonstrate ‘‘quality,’’ then it would pay females to attend to differences between males. Preliminary evidence that females of some primate species may choose for male adornments comes from squirrel monkeys (Saimiri oesterdii, Boinski, 1987) and mandrills (Setchell, 1999). Much more work is needed here, including experimental studies, but we can speculate that a positive interaction between the selective action of male-male competition and female choice on male display might go some way to explaining the most exaggerated ornaments in male primates (e.g., red color in male mandrills and flanged cheeks in male orangutans, Setchell, 2003). For example, a recent study combining experiments and long-term observation has demonstrated that male lions (Panthera leo) are intimidated by long, dark manes in other males, but that darker manes are also more attractive to females (West and Packer, 2002). A further aspect of female choice for male genetic ‘‘quality’’ concerns genetic compatibility. This is of particular interest in species where individual females show variation in mate choice. If mating preferences are not uniform across females, then this suggests that rather than specific

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‘‘good genes,’’ male genes that are ‘‘good’’ for one female are not necessarily those that are best for another female (Brown, 1997). For example, females may choose males with dissimilar major histocompatibility complex (MHC) alleles (Penn and Potts, 1999). Very little work has investigated the role of genetic compatibility in primate mate choice outside rhesus monkeys (Sauermann et al., 2001). However, shared MHC class I antigen between parents is associated with a greatly increased risk of pregnancy loss in pigtail macaques (Macaca nemestrina: Knapp et al., 1996). Female choice for genetic compatibility suggests that male ornaments and displays will be of less importance than mechanisms such as odor cues (e.g., Wedekind et al., 1995), or post-copulatory selection (see below). However, MHC genotype is associated with variation in both male spur length and male viability in pheasants (Phasianus colchicus), suggesting that male secondary sexual characteristics may be related to genetically-determined disease resistance (von Schantz et al., 1996). There is also a possibility for selection for heterozygosity in offspring in litterbearing species that favors female promiscuity (Brown, 1997). 3. Female Choice in Humans A great deal of research has examined mate choice in humans (reviewed by Thornhill and Gangestad, 1996; Gangestad and Thornhill, 2003). Briefly, women appear to select partners that will devote resources to potential offspring and value indicators of resources, status, and investment in potential mates more than physical attractiveness and youth (Buss and Schmitt, 1993; Jensen-Campbell et al., 1995). Symmetrical appearance is also important, particularly in short-term partners: Men with relatively low fluctuating asymmetry (FA) are more attractive to women, have more sexual partners, more extra-pair copulations, and begin their sexual careers earlier than less symmetrical men (Thornhill and Gangestad, 1994; Gangestad and Thornhill, 1997). Female preferences change across the menstrual cycle (Gangestad and Thornhill, 2003). Outside the fertile phase, females prefer features linked to long-term investment. However, during the fertile phase, females show preferences for the scent of more symmetrical men and for more masculine faces (Gangestad and Thornhill, 1998). This has been taken to suggest that females have a preference for a long-term partner for investment in offspring, and for short-term partners to obtain ‘‘good genes.’’ There is a negative correlation between male attractiveness (measured as FA) and investment in offspring in human males (Gangestad and Thornhill, 1997); females seeking investment and protection from sexual coercion (including infanticide) therefore face a trade-off with mate attractiveness. It has been suggested that, by sharing extra-pair copulations with men that exhibit


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relatively low FA (Thornhill et al., 1995) during their fertile period, women may be selecting attractive sires while raising the offspring with less attractive but resource-providing long-term partners. Critical caution is required, however, when interpreting the results of these and other studies of mate preferences in humans. Most reports are based on college student responses to questionnaires, and it is highly questionable whether such responses from (largely) non-reproducing individuals can be considered as true evidence for sexual selection. We are not aware of any study in which human participants that might actually be considering child-bearing have been asked questions that distinguish between preferences for partners for recreational sex versus partners with whom they would choose to conceive and rear a child. Furthermore, questionnaire responses are far from the observations of mating patterns, paternity analyses, and evidence of lifetime reproductive success that are required to truly investigate sexual selection. Convincing evidence of the action of sexual selection in humans will require studies employing the same strict criteria used in studies of other taxa (e.g., Snowdon, 2003). 4. Questions for the Future Female choice represents a challenging area for research in primates with many questions remaining to be resolved. However, limitations of generation time and litter size (and therefore sample size), as well as interacting male and female strategies, make it difficult to test theoretical predictions. Future research into female mate choice in primates will require carefully designed investigations and should include: studies of mating behavior combined with paternity tests to investigate the reproductive outcomes of male and female mating strategies (e.g., Pereira and Weiss, 1991; Kuester et al., 1994; Fietz et al., 2000; Constable et al., 2001; Soltis et al., 2001; Kappeler et al., 2002; Wimmer and Kappeler, 2002); experimental investigation of female preference for male display and ornamentation; the costs of female mate choice (e.g., Gowaty, 2003); and whether female mate choice for particular male phenotypes actually affects female reproductive success (reviewed in Gowaty, 2003). Studies of female choice must also take into account the timing of ovulation because female strategies may involve choice for different males dependent on reproductive status. Information about female hormonal cycles, in addition to behavior and paternity, is therefore required (e.g., Soltis et al., 2001). Female choice may be easier to investigate in species that show female dominance (Kappeler, 1993b), as female choice should be less constrained by male tactics (Pereira and Weiss, 1991). However, even in these species, male-male competition may limit the field of choice, such that only certain males are available (e.g., Kraus et al., 1999; see Paul, 2002). Finally, studies

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of human mate choice, although numerous, are currently often less direct than those of mate choice in other species and will benefit from the application of the same fundamental criteria required for the demonstration of the action of sexual selection in other taxa, including evidence that mate preferences impact on reproductive success (Snowdon, 2003). E. Cryptic Female Choice Cryptic female choice (the influence of female behavior, morphology, and physiology on post-copulatory competition between the sperm of multiple males) is poorly documented in primates, although there are theoretical reasons to expect it to be common (Dixson, 1998a; Birkhead and Kappeler, 2003). Female primates commonly mate with more than one male per receptive cycle, leading to the presence of sperm of more than one male in the female reproductive tract at the right time. Cryptic female choice could be one mechanism contributing to the solution of the female dilemma; females could both mate with multiple males (confusing paternity) and bias the paternity chances of those males via postcopulatory mechanisms. Post-copulatory interactions among sperm of different males, potential differential interactions between sperm and the female reproductive tract, as well as details of the sperm-egg interactions, are comparatively littleunderstood among primates (Primakoff and Myles, 2002) perhaps because of the heavy reliance on invasive methods for obtaining such data. Proximate questions about potential mechanisms of cryptic female choice in primates were posed long before the topic became popular in other taxa (Quiatt and Everett, 1982), but still very little relevant information can be found under this key word. Indirect evidence from a recent study of rates of molecular evolution of genes coding for sperm-associated proteins clearly indicated that these genes exhibit much higher rates of nonsynonymous substitution in promiscuous primates (Wyckoff et al., 2000). This difference has been interpreted as indicating that ‘‘potential competition among sperm from different males has contributed to the accelerated evolution of genes involved in sperm and seminal fluid production’’ (Wyckoff et al., 2000, p. 305) but cryptic female choice provides an equally plausible and not incompatible mechanism. Because the present data are limited to the great apes, more data from additional taxa are required for a stronger test of this hypothesis. Once a male has succeeded in copulating with a female and has deposited sperm in her vagina, then the sperm must navigate the female reproductive tract to reach the ova. This is far from being a simple ‘‘sprint race,’’ and the female tract puts a variety of anatomical and physiological


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‘‘hurdles’’ in the way of the male gametes (Dixson, 1998a). The possibilities for the operation of cryptic female choice are multiple, including the length and complexity of the vagina, uterus and oviduct, and the composition of female secretions. Comparative investigations of reproductive physiology in primate species where females mate with one or several males per receptive cycle will be of great interest in examining such questions. Unfortunately, the evidence required to test predictions concerning the action of cryptic female choice is currently not available (for a review of the available evidence, see Dixson, 1998a; Birkhead and Kappeler, 2003). The strongest indirect evidence for a mechanism of cryptic female choice in primates is provided by the observation that females of several species of anthropoids (mostly macaques, baboons and chimpanzees, also humans) exhibit orgasm (Allen and Lemmon, 1981; Dixson, 1998a). It should be noted that the taxonomic distribution of female orgasm remains poorly documented and that it may be limited to Old World primates. Physiological measures during artificially induced orgasms have demonstrated the occurrence of the same vaginal and uterine contractions that characterize human orgasm (Burton, 1971; Goldfoot et al., 1980; Allen and Lemmon, 1981), which in turn are thought to accelerate and facilitate sperm transport towards the cervix and ovaries (Smith, 1984). Interestingly, the occurrence of female orgasm is highly variable, both among and within females. The adaptive nature and underlying physiology of this variation remain poorly understood, even in humans (Mah and Binik, 2001). Hrdy (1996) suggests that reaching orgasm requires cumulative stimulation from multiple sexual encounters and, at least in Japanese macaques (Macaca fuscata), the frequency of orgasm is indeed positively related to the number of mounts and pelvic thrusts, and thus the duration of copulation (Troisi and Carosi, 1998). Importantly, when the level of physical stimulation was statistically controlled, female orgasm was observed more often in macaque pairs including high-ranking males (Troisi and Carosi, 1998). A comparable effect of social status of female orgasm rates has also been reported for humans (Thornhill et al., 1995). Orgasm therefore has the potential to be used selectively by females to facilitate fertilization of their eggs by particular males (Smith, 1984; Thornhill et al., 1995). This hypothesis is indirectly supported by the observation that female orgasm apparently does not occur among prosimians, which have penises with extremely mechanically-stimulating appendages, but rather among Old World primates, where the potential for coercive matings by multiple males is highest (van Schaik et al., 1999; Nunn and van Schaik, 2000). Looked at in this way, female orgasm in

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primates may represent an evolutionary response to male sexual coercion that provided females with an edge in the dynamic competition over the control of fertilization (Hrdy, 2000b). F. Competition Between Females? Female reproductive success is closely linked to resource availability, and reproductive competition between females is expected where access to resources, including food, mates, and help with infant care is limited. Evidence that female-female competition occurs for mating opportunities comes from a variety of primate species and mating systems. Where access to males is limited and/or males vary in quality (genetic quality, resources required by females for reproduction, and care of offspring), female primates are expected to compete for mating opportunities. In uni-male, polygynous systems, a male’s sperm may be limited, and high-ranking females prevent low-ranking females from mating through aggression and harassment. For example, female patas monkeys (Loy and Loy, 1977), geladas (Dunbar, 1984), Hanuman langurs (Sommer, 1989; Sommer et al., 1992), and gorillas (Watts, 1990) compete for conception; in captive hamadryas baboons, the probability of conception decreases with the number of females cycling simultaneously (Zinner et al., 1994). In multimale, multi-female groups, dominant females may also aggressively interrupt matings involving subordinate females (Loy, 1971). In brown capuchins, the simple presence of dominant females inhibits subordinate females from interacting with males, even in the absence of aggression (e.g., Janson, 1984). In Hanuman langurs, it has also been suggested that post-conception (and therefore non-conceptive) estrus may represent female-female competition for sperm, acting to reduce the probability of conception in rival cycling females and thus to reduce the future number of unrelated competitors for resources (Small, 1988; Sommer, 1989). In multi-male, multi-female species, high-ranking females have priority of access to nutritional resources (e.g., Barton and Whitten, 1983; van Noordwijk and van Schaik, 1987; Altmann and Muruthi, 1988). Improved nutrition leads to superior body condition (Strum, 1991), and where foods are clumped or restricted in distribution, higher-ranking female primates tend to have greater reproductive success than do lower-ranking females. This reproductive advatange is due to an earlier age at sexual maturity and first reproduction (leading to a longer reproductive lifespan), shorter interbirth intervals (increased rate of offspring production), and/or higher offspring survival (e.g., Bulger and Hamilton, 1987; Harcourt, 1987; Altmann et al., 1988; Smuts and Nicolson, 1989; Bercovitch, 1991; Bercovitch and Strum, 1993; Pusey et al., 1997; Wasser et al., 1998;


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van Noordwijk and van Schaik, 1999; Setchell et al., 2002; Johnson, 2003). However, Packer et al. (1995) found that high-ranking females also had a higher probability of miscarriage and fertility problems. Higher-ranking females may also produce offspring that are larger for their age (Setchell et al., 2001; 2002; Johnson, 2003), perhaps because individuals of higher status can allocate more resources to reproduction and infant survival than can mothers of lower status (Altmann, 1980; Clutton-Brock et al., 1982; Simpson et al., 1981; Gomendio, 1990; Pusey et al., 1997). Finally, social as well as nutritional stress may play an important role in the lowered reproductive success of low-ranking females (Gomendio, 1990; Dunbar, 1988). Cooperative breeding in callitrichids leads to intense female reproductive competition. Males of these species contribute to infant care, and additional care-givers (up to a total of five) increase infant survival (Snowdon, 1996). Individual females act to increase the survivorship of their own offspring at the expense of those of other females. Reproductive skew is high amongst females; high-ranking females interrupt the copulations of other females, and reproductive function is suppressed in subordinate females (Abbott et al., 1990; Dixson, 1998a). In the wild, where reproductive suppression may be less efficient, subordinate females may occasionally reproduce, leading to shared resources. In such cases, dominant females may kill the offspring of subordinate females (Digby, 1995; Lazaro-Perea et al., 2000). In this way, the infanticidal female benefits by reduced competition for resources, including helpers and food (Hrdy, 1979). Infanticide reduces the number of offspring requiring care, meaning that helpers invest more in the remaining infants. The targeted female may even suckle the offspring of her infanticidal rival (Digby 1995). In this case, it appears that the benefits gained by the infanticidal female are greater than the loss of inclusive fitness involved when the offspring belongs to a related female. Reproductive suppression in subordinate female callitrichids may thus act to avoid wastage of reproductive effort, such that females do not invest in offspring that will not survive (Digby, 1995). Direct female infanticide, whereby one female kills the infant of another, is rare in non-cooperatively breeding primates. However, Digby (2000) notes a few cases, including a mother-daughter pair of chimpanzees that are known to have killed three infants and are suspected of killing up to seven others over four years (Goodall, 1986), as well as a case of dominant females attacking the infants of subordinates in multi-male, multi-female species (Tonkean macaques, Macaca tonkeana: Muroyama and Thierry, 1996; yellow baboons: Wasser and Starling, 1986; black lemurs, Eulemur macaco macaco: Andrews, 1998). In general, killing of another female’s offspring in multi-male, multi-female species results in little or no benefit to

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the infanticidal female, and where females are philopatric, females are likely to be closely related to other females in the group. However, ‘‘indirect infanticide’’ is comparatively more common than direct physical aggression against infants, and includes ‘‘kidnapping’’ of unweaned infants by dominant females, leading to death from starvation or dehydration, and general harassment of subordinate females that leads to cessation of lactation and infant starvation. The benefits accruing to the dominant females in these cases may be related to the maintenance of dominance or to the elimination of future rivals to the infanticidal female or her own offspring (Digby, 2000). The protective maternal style of subordinate females (Altmann, 1980) may act to protect their infants from such harassment. G. Investment in Offspring and Sex Ratio Manipulation Females provide parental care in the large majority of primate species, raising the question of whether females allocate their parental investment according to aspects of female condition (Trivers and Willard, 1973) or offspring quality, such as traits of the sire or the sex of the infant (Qvarnstrom and Price, 2001). The question of whether female primates are able to facultatively adjust investment in offspring or manipulate birthsex ratios has been the subject of numerous investigations in primatology (e.g., reviews by van Schaik and Hrdy, 1991; Silk et al., 1993; HiraiwaHasegawa, 1993; Brown, 2001; Bercovitch, 2002). Investment in an individual offspring enhances that offspring’s chance of survival, while at the same time diminishing the parent’s ability to invest in future reproduction by reducing survivorship and/or fertility (Fisher, 1930; Trivers, 1972). Investment is thus predicted to be sex-biased where one sex is less costly to rear, or where investment in one sex provides greater fitness returns in terms of numbers of descendants. Trivers and Willard (1973) proposed that females should differentially distribute investment between male and female offspring, predicting that mothers in good condition should bias their investment towards sons while mothers in poor condition should bias investment towards daughters. This is based on the assumptions that a mother’s investment influences the condition of her offspring into adult life, and that (in polygynous species) adult body condition has a greater influence on male reproductive success through improved competitive ability than it does on female reproductive success. Greater individual variability in reproductive fitness between males than between females means that investment in sons will yield a greater return than will investment in daughters. Female social rank is often used as a proxy for female condition in primates, predicting that higher-ranking females should invest more in sons, while lower-ranking


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females should invest more in daughters (e.g. Meikle et al., 1984). However, an alternative interpretation of the Trivers and Willard model is that high-ranking females in philopatric species should invest in daughters that will inherit their own high rank and high reproductive success. Lowranking females, on the other hand, should invest in sons because males disperse from their natal group, and their adult rank (and therefore reproductive success) is thus less likely to be influenced by their mother’s rank (e.g., Altmann, 1980; Silk et al., 1981; Simpson and Simpson, 1982). Various other models have been proposed as to how and why primate females should differentially distribute investment between male and female offspring, giving rise to differing predictions. These predictions include models of local resource competition (Clark, 1978; Hamilton, 1967; Silk, 1983, Gowaty and Lennartz, 1985; Johnson 1988; Hiraiwa-Hasegawa, 1993) and population adjustment (Leigh, 1970; Maestripieri, 2001; Wasser and Norton, 1993). Support for each model has been found in some studies of some primate species, and Bercovitch (2002) cautions that we should not expect all primates to behave the same way. Sex-biased maternal investment may occur as either facultative adjustment of secondary sex ratios, or as biased maternal expenditure during the pre- and post-natal period. Many studies of primates have investigated various aspects of maternal investment, but the question of whether primate mothers differentially allocate investment to one sex or the other has proven extremely difficult to approach (Brown, 2001; Bercovitch, 2002). Bercovitch (2002) has identified at least 7 fundamental issues that remain unresolved. These are that: (1) as yet a convincing proximate mechanism by which female primates could adjust the sex ratio of their offspring has not been identified; (2) only one study examines whether sex-biased maternal investment actually contributes to variation in offspring reproductive success, and in this study the contribution to variance is extrememly low (about 2%, Bercovitch, 2002); (3) most reports of sex ratio bias come from captive studies, and findings are often contradictory. We also lack knowledge of: (4) how social and demographic factors influence maternal investment; (5) how female dominance rank influences investment patterns; and (6) the influence of maternal age on patterns of investment. Finally, (7) there are the problems of sampling error associated with small sample sizes and pooling of cohorts. This final point is echoed by a meta-analysis by Silk and Brown (2003), who found that reports of biased sex ratios might simply be an artifact of small sample sizes. As sample size increased across different studies, the deviation of sex ratio from 1.0 decreased, suggesting that sex ratio results might simply be due to sampling error (Silk and Brown, 2003). In summary, Bercovitch’s (2002) critical review states that ‘‘the possibility remains that many

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primates are investing the maximum amount of resources possible into parental care and are not engaged in a process of sex-biased parental investment’’ (p. 917). H. Summary of Sexual Strategies in Female Primates Current evidence suggests that female choice for male quality may be less important than female counter-strategies against male coercion, infanticide in particular. Female primate behavior tends to increase the number of males mated with (Hrdy, 1981, 2000a; Small, 1993). This polyandrous mating can be seen as being against female choice (Small, 1989), but, by mating with different males at different times during the reproductive cycle, a female may be able to combine paternity confusion with choice for particular mates. Many questions remain to be resolved concerning the sexual strategies of female primates. For example, why do females of strictly seasonal species, and where females are dominant over males, such as most lemurs (Richard, 1987), mate multiply? In such species, male infanticide will either not shorten a female’s time to resumption of cycling, or females can be expected to have free choice without sexual coercion, respectively. Possible explanations for the existence of multiple mating in these species include infanticide avoidance and cryptic female choice. Although infanticide does not shorten a female’s time to resumption of cycling, it may benefit males by increasing a female’s investment in the next season’s litter, while mating multiple times allows females to select for ‘‘good genes’’ or genetic compatibility via cryptic female choice (Jolly et al., 2000). Female reproductive strategies can act in tandem with male strategies; for example, by reinforcing reproductive skew towards dominant males if females show preference for dominant males, or by choosing males with characters that reflect dominance (e.g., cheek flanges in orangutans and red color in mandrills: Setchell, 2003). However, female strategies may also be in opposition to male-male competition; for example, female choice for males of other ranks or novel males (e.g., Davies, 1992; Manson, 1992). This latter case brings the sexes into direct conflict over reproduction, as we will see in the following section.

VII. Conflict Between the Sexes Male and female reproductive strategies are intimately linked in primates. They are also inherently in conflict as the interests of males and female diverge. Sexual conflict can be seen as an arms race where the


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evolution of strategies in one sex leads to counter-strategies from the other, which in turn lead to counter-counter-strategies in the first (Parker, 1979; Clutton-Brock and Parker, 1995). This intraspecific red queen phenomenon is well illustrated by the evolution of male infanticide and related counter-strategies in multi-male, multi-female primate species (van Schaik, 2001; van Schaik et al., 2003). Where sexually selected male infanticide (male strategy) poses a threat to the survival of offspring, females have responded with various behavioral and physiological counterstrategies to confuse paternity (female counter-strategy). In a further twist to the female’s dilemma, polyandrous mating by females dilutes the dominant male’s likelihood of paternity, contravening his own reproductive strategy. Thus, male sexual coercion has evolved to restrict female reproductive behavior (male counter-counter-strategy). To avoid this risk, females must give the dominant male sufficient paternity confidence so that he will protect infants from potentially infanticidal attacks from other males while simultaneously providing other males with enough probability of paternity to ensure that they will not kill the offspring if they become dominant. This leads to the evolution of further female strategies (female counter-counter-counter-strategies), including a lengthened follicular phase and sexual swellings to bias and confuse paternity in species where males are larger and can attack females (van Schaik, 2001; van Schaik et al., 2003). Sexually-selected infanticide is a prime example of sexual coercion. Other male coercive tactics in primates include physical attack, intimidation, harassment, and interruption of copulation and forced matings (Smuts and Smuts, 1993). Although primate examples featured heavily in the comprehensive review by Smuts and Smuts (1993), in which they suggested that sexual coercion was as important an evolutionary force in sexual selection as inter-sexual competition and mate choice, with the exception of the large literature that has developed concerning male infanticide, our knowledge of other male coercive strategies has not greatly increased since then (but see Manson, 1994; Soltis et al., 1997b; Soltis, 2002; Fox, 2002). This is an important area for future research, where primate societies can provide good opportunities for identification and detailed studies of additional mechanisms (see van Schaik et al., 2003). Sexual coercion and female counter-strategies in response to coercion are examples of pre-copulatory sexual conflict, involving mating decisions; however, sexual conflict may equally operate at the post-copulatory level, involving ejaculate manipulation in males, and/or sperm selection by females. As a final example, although primates are not obvious model species for the investigation of sexually antagonistic coevolution at the genetic level, studies in humans have shown that sexual conflict exists within fetal cells, between genes that are expressed when maternally-derived,

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and those that are expressed when paternally-derived (Miozzo and Simoni, 2002; Tycko and Efstratiadis, 2002). Termed ‘‘genomic imprinting,’’ paternal genes and maternal genes ‘‘fight’’ over the fetus’s size. Male genes act to promote the growth of the fetus at the expense of the mother, while maternal genes act to ration investment in the fetus so as not to compromise her investment in future offspring that may not be sired by the same male. Which sex prevails in the evolutionary arms race, and controls mating and reproductive outcomes, will depend on environmental constraints, including physical (e.g., climate), biotic (e.g., resource dispersion, predation pressure), and social (e.g., population density) factors (Kappeler and van Schaik, 2002). Indeed, the extent to which the strategies of males or females determine fertilization can differ between two studies of the same species (Soltis et al., 1997a, b, 2001). The widespread nature of polyandrous mating by females across the primate order suggests that female strategies such as unpredictable ovulation, advertisement, lengthened receptive periods, and female choice act against the ability of males to monopolize females. Where females dominate males (e.g., lemurs: Richard, 1987; Kappeler, 1993b), relatively free female choice might be expected to be an important factor in reproductive outcomes, whereas at the other end of the continuum, in species where females are dominated and sexually coerced by males (e.g., gorillas), males might be expected to exert more control. Here, a female’s strategy may be to associate with a powerful male in order to avoid infanticide (Harcourt and Greenberg, 2001). Mating systems in primates, as in other taxa, can thus be viewed as evolutionarily dynamic resolutions of conflicts of interest between males and females (e.g., Gowaty, 1994; CluttonBrock and Parker, 1995; Choe and Crespie, 1997; Chapman et al., 2003).

VIII. Conclusions and Future Directions Studies of sexual selection in primates have long been dominated by examination of male contest competition over copulatory access to females, an emphasis that has tended to eclipse the wide diversity of sexually selected strategies and tactics that occur in both sexes of this order. Underlying this diversity is the extent to which males are able to monopolize females, which is dependent on the dispersal and grouping patterns of female primates, in turn driven by the distribution, abundance, and quality of limiting resources (Emlen and Oring, 1977). Females thus exert a strong influence on the ability of males to monopolize matings and fertilizations, but female strategies are likewise limited by those of males. Male and female primate reproductive strategies are inherently conflicted,


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leading to an escalated arms race of strategy and counter-strategy. This realization and, in particular, the recognition of the important role of female strategies, should contribute to a better understanding of the diversity of primate mating systems, and ultimately social systems, as representing a dynamic interplay between male and female strategies (see also Kappeler and van Schaik, 2002). Primatologists need to move away from the classification of mating systems as monogamous, polygynous or polyandrous and to recognize that the reproductive agenda differs both between the sexes and within individuals of the same sex (Gowaty, 2003). A. Primates and Non-Primates Sexual selection operates as strongly on primates as it does on other organisms, with profound implications for primate social systems (e.g., Crook, 1972; Clutton-Brock and Harvey, 1977; van Schaik and Kappeler, 1997). Both sexes compete for mates and their gametes, and both males and females exhibit mate choice. However, the sexual selection hypotheses examined and theoretical models constructed for other taxa may not always be applicable to primates. In particular, primate mate choice may be more difficult to observe than mate choice in birds, fish, or invertebrates, as mating decisions are likely to be based on long-term knowledge of potential mates rather than on arbitrary ornaments (Kappeler and van Schaik, 2002; Snowdon, 2003), with the possible exception of the striking male ornaments observed in some primate species with poorly-individualized relations. The sexual interests of males and females can be expected to diverge in all taxa, leading to a conflict of interest between the sexes (Parker, 1979; Smuts and Smuts, 1993; Gowaty, 1997). Selection favors males with traits that coerce females to mate with them while favoring traits that allow females to select the male that fertilizes their ova. This ‘‘arms race’’ between males and females has led to an overlaying of strategies, counterstrategies, and counter-counter-strategies in primates that sets them apart from the organisms generally studied by students of sexual selection, presumably because the slow life history and reproductive biology of primates makes them especially vulnerable to sexually-selected male infanticide (van Schaik, 2000). B. Future Directions The selective force of male infanticide driving females to mate with multiple males is a major focus of research in primate sexual selection. However, we should not expect a single selective force to explain the

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amazing diversity of female sexual strategies that we observe, and the explanatory power of infanticide should not blind us to other potential explanations. For example, the evolution of strategies such as infant care by males or female infanticide in callitrichids will require different explanations linked to cooperative breeding. There are many areas with exciting potential for novel studies of sexual selection in primates. In this final section, we outline some suggestions for future research that will allow us to reach a deeper understanding of reproductive strategies and sexual selection in primates. 1. Untangling the Influence of Overlaying Strategies The overlaying of strategy, counter-strategy, and counter-counterstrategy in primates means that separating the effects of male and female strategies on mating and reproductive success, as well as identifying the ultimate factors underlying reproductive strategies, can be extremely difficult (e.g., Soltis et al., 1997a,b). The variables that we are able to measure are not the original selective forces, but are the consequences that remain despite the counter-strategies that evolved to reduce the effect of the reproductive strategy. For example, where male contest competition is important, males have evolved to be larger and more powerful. However, the effect that the largest, most competitive male sired the majority of offspring has selected for alternative mating tactics in other males and for counter-strategies in females. Thus, under natural conditions, the largest male is not necessarily expected to have a higher life-time reproductive success than males employing alternative mating tactics. Paradoxically, where female counter-strategies to male infanticide are effective, the observed rate of infanticide will be low and infanticides may never be observed in field studies. Teasing apart these selective pressures is difficult and perhaps impossible without experimental manipulation (e.g., of the composition of captive groups). An alternative solution is to use comparative analyses and proxy measures of ‘‘risk’’ (e.g., van Schaik et al., 1999; 2000), rather than the observed occurrence of events such as infanticide. 2. Interdisciplinary Studies In order to understand the causes and consequences of competition for mates, mate choice and sexual conflict in primates, detailed, integrative studies will be required of the relationships among mating behavior, morphology, physiology (including endocrinology), and genetically determined paternity. Study of variation between individuals in reproductive behavior, fertilization success, and offspring success will be important in


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establishing the selective pressures and mechanisms underlying the operation of sexual selection (Gowaty, 2003). 3. Experimental Approaches Carefully designed experimental studies which eliminate alternative hypotheses or quantify the relative importance of different selective pressures are needed for a clear understanding of sexual selection in primates. We must attempt to explore not only ultimate causes, but also the proximate mechanisms underlying reproductive strategies. It may be difficult to experimentally manipulate primates in the ways we manipulate fish, invertebrates, or birds. However, humane, minimally-invasive experimental research is possible both in the field and in captivity. This research will be necessary if studies of primates are to attain the level of those concerning other taxa (Snowdon, 2003). Critical, scientific validation, and more realistic research paradigms are perhaps particularly lacking in current studies of sexual selection in humans. With the exception of those on sexual swellings in female primates, very few studies have concentrated on sexually dimorphic visual, acoustic, and chemical signaling. Due to the conflicting strategies and counter-strategies involved in the evolution of signals, studies to elucidate the existence and relative importance of differing selective pressures will require careful design, and captive experiments (along the lines of Bielert and van der Walt, 1982; Bielert and Anderson, 1985; Bielert and Girolami, 1986; Bielert et al., 1989; summarized in Snowdon, 2003) will probably be required to investigate differential mate preferences. Carefully designed experimentation will also be particularly useful in the study of sperm competition, which currently lags behind that in birds, insects, and mammals in general, with many areas remaining unexplored (Gomendio et al., 1998). For example, pilot studies have indicated that controlled matings are possible with certain small prosimians (Eberle, Perret and Kappeler, unpublished data), allowing experimental studies of the mechanisms of sperm competition. 4. True Estimates of Lifetime Reproductive Success Tests of sexual selection hypotheses are currently limited by the use of behavioral measurements to estimate selective pressures (Plavcan, 2003) because true estimates of skew in both male and female lifetime reproductive success are currently unavailable for most primate species (van Noordwijk and van Schaik, 2003). Many studies utilize mating effort or timing of copulation as a proxy for an evaluation of sexual selection. However, comparative lifetime reproductive success between individuals is

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the best and truest measure of the strength of sexual selection. Choices made at the time of fertilization that lead to viable offspring are the only ones that matter when addressing issues of sexual selection. Such data are slowly accumulating from long-term studies and may already be available from some captive colonies. Noninvasive methods (using feces, hair, urine, semen, and food ‘‘wadges’’: Goossens et al., 2003) now exist for paternity determination (e.g., Morin et al., 1994; Constable et al., 2001; Vigilant et al., 2001; Utami et al., 2002), meaning that some of the data that are currently missing can now be obtained noninvasively. Analysis of the entire career of wild individuals will allow us to determine the relative pay-offs of alternative tactics, the influence of development on lifetime strategies, and how tactics may change over a lifetime (Setchell and Lee, 2003). 5. Broader Species Representation More data concerning more species, in captivity and in the wild, are required to test predictions arising from sexual selection theory and to examine the relative importance of different mechanisms in contributing to variance in skew within populations, within species, and across species. This will lead to more theoretical models (e.g., Harcourt and Greenberg, 2001; Soltis and McElreath, 2001) and more comparative studies to test sexual selection hypotheses. Eventually we will be able to make more use of meta-analyses (e.g., Bercovitch, 1991; Cowlishaw and Dunbar, 1991; de Ruiter and van Hooff, 1993; Nunn and Barton, 2001; Alberts et al., 2001; Brown and Silk, 2002) similar to those available for other taxa (e.g., Gontard-Danek and Møller, 1999; Møller et al., 1999; Jennions et al., 2001). Like Harcourt (1998), we suggest that primatologists can, and have, learned from non-primate socio-ecologists. Although there is still very little overlap between the specializations, primatologists can look to existing models developed for other taxa to make predictions and interpret data. Local population density and sex ratios will influence levels of competition and constrain mate choice possibilities. Studies of different groups and populations of the same species will allow determination of the influence of local demographic conditions on reproductive strategies (Strier, 2000). For example, the population density of females and rival males may influence the developmental strategy of male orangutans (Maggioncalda et al., 1999). Such contingencies need to be studied explicitly or be included in other analyses. Finally, studies of sexual selection in primates should not be limited to highly sexually dimorphic species. All primate mating systems are made up of male and female reproductive strategies; great insight is to be gained


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from the investigation of diverse taxa. A broader species representation will provide greater comparative perspective. Studies should include primate species for which evidence of sexual selection appears to be minimal. In addition to pair-bonded species, comparisons of sexually monomorphic and dimorphic anthropoids, male-bonded species, and prosimians will be valuable. For example, genetic evidence has revealed that not all socially monogamous species are reproductively monogamous (Palombit, 1994; Reichard, 1995; Fietz et al., 2000; Sommer and Reichard, 2000), suggesting that reproductive strategies may differ from those previously assumed to exist in such species. The callitrichids pose further interesting questions with regard to sexual strategies, where males provide substantial care for offspring and strong reproductive competition occurs between females. Finally, lemurs, with their independent evolutionary history, offer a useful opportunity to test theoretical predictions and convergence with anthropoids (e.g., Kraus et al., 1999; Ostner et al., 2002; Wimmer and Kappeler, 2002), and other sexually monomorphic species. Evidence suggests that mechanisms of intrasexual selection may differ between gregarious lemurs and anthropoids, but exactly how they differ is unclear (van Schaik and Kappeler, 1996; Wright, 1999). Further comparative studies may help to elucidate the underlying causes of these differences among higher taxa. Indeed, much remains to be learned about sexual selection in relation to monkeys.

IX. Summary The causes, mechanisms, and consequences of mate choice and competition for mates are currently among the most intensively discussed topics in evolutionary biology. However, primates are notably underrepresented in this debate. In this review, we briefly summarize the main concepts of modern sexual selection theory and examine the evidence for the operation of sexual selection in primates. Traditional classifications of mating systems suffer from the problem of not considering reproductive strategies of both males and females equally and are biased by a strong male perspective. We therefore discuss the male and female perspective separately before examining the interaction of male and female strategies and sexual conflict. By using a comparative and theory-oriented approach to examine and integrate recent developments in primate sexual selection studies, we aim to draw some general conclusions about sexual selection in primates; identify reasons why primates have been neglected in particular areas of sexual selection research; and stimulate future research on all aspects of sexual selection in primates.

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Acknowledgments We thank Carel van Schaik, Claudia Fichtel, and Alan Dixson for numerous stimulating discussions of sexual selection in primates, Marc Naguib for the invitation to contribute this paper, Eckhard Heymann for pointing out some callitrichid references, and Charles Snowdon, Marc Naguib, Peter Slater, and an anonymous reviewer for their constructive comments on an earlier version of this manuscript.

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Genetic Basis and Evolutionary Aspects of Bird Migration Peter Berthold max planck research centre for ornithology vogelwarte radolfzell, schlossallee 2, d-78315 radolfzell, germany

I. Introduction Bird migration is a phenomenon of superlatives, intensely interesting to humanity for millennia and probably since primeval times. With about 50 billion individuals migrating every year along a network of routes that encompass the entire earth, bird migration is observable universally throughout the year. People in practically every geographical region are constantly in contact with it, and most will eventually consider the questions that are at the core of migratory scientific research (Berthold, 2001). To begin with, why do birds migrate at all, and given that they do, why do they travel such vast distances? Some of them cover 30,000 to 50,000 km annually, or approximately the circumference of our planet, and non-stop flights may be as long as 7,500 km. How do they manage this? How can they cross oceans and deserts in relative safety and fly over mountains as high as 10,000 m without suffering altitude sickness? There are partially migratory populations, with some members that spend the winter abroad while others remain in the breeding grounds—what determines who goes and who stays? What tells the migrants when to depart and when the journey is over, and what keeps the migration in progress for a few hours in some cases but for more than half a year in others? How can migratory birds orient themselves so precisely over thousands of kilometers—for instance, on a journey between their nest in a farmer’s barn within the breeding area and a particular branch on a tropical tree for roosting while in the winter quarters—with pinpoint navigation sharp enough to locate both destinations every year? Furthermore, what enables their amazing temporal precision every year, sufficient for many of them to schedule the migration almost down to the day, so that 175 Copyright 2003 Elsevier Inc. All rights reserved. 0065-3454/03 $35.00

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one could set the calendar by them (indeed, these have been called ‘‘calendar birds’’)? Now there is something new to ask: What makes them able to adjust so rapidly to the changes in environmental conditions currently being caused by global warming? This ability is especially astonishing in the case of the many songbird species, most of which have their migratory experience limited to their lifetimes (a little over a year) and nevertheless behave as the times demand. Bird migration is superlative not only in terms of multitudes, distances, physiological adaptations, orientation performance, and the like, but has also been extraordinarily well-studied. The reason is that birds are the most attractive group of organisms we know. No other animal has captivated so many enthusiasts and especially amateur researchers worldwide—in the USA and Europe alone they now number in the millions. The attractions of these animals are obvious: appealing body shape, colorful plumage, conspicuous and sometimes beautiful song, graceful movements—especially in flight—as well as many other aspects of their behavior and ubiquitous presence. Not only do we know them as constant companions in our settlements, but we also encounter them regularly on our travels to remote deserts, mountains, and fields of arctic ice. The result of all this is that ornithology has become a unique ‘‘scientia amabilis,’’ such that over the centuries migration has been more thoroughly studied than almost any other natural phenomenon. This has had two main outcomes. On one hand, an unequalled database of migratory information has been created, extending far back into the past. This enables us to rapidly recognize changes when they occur—for example, a later-than-usual onset of migration, or the adoption of new winter quarters. On the other hand, we are now faced with an abundance of hypotheses and theories, especially about the evolution of migration, its controlling mechanisms, and the orientation of migrating birds. Some of these have propelled the research forward, but others have held it back. The emphasis on experimental studies in the last three decades or so has brought decisive advances in many areas, such as in our understanding of how migration is grounded in genetics and evolution. The following overview is concerned mainly with these two aspects of biology.

II. The Broad Palette of Theories on Control Mechanisms and Evolution Today those who study bird migration largely agree that the main reason for undertaking a migratory journey is ultimately related to feeding conditions. However, these conditions affect the birds in two distinct ways.

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One is that a sudden, temporary lack of food causes the birds to leave, such as in the case of insectivorous species at the higher latitudes. Secondly, the birds seek out regions in which at certain seasons the food supply is particularly abundant and other conditions are favorable for breeding or molting; for instance, large expanses of tundra are targeted by geese and waders (Berthold, 2001). Opinions concerning the origin of bird migration differ widely. Rappole (1995) summarized all the theories related to the evolution of bird migration in eight categories, ranging from the continental drift theory and ice age theory to a migration threshold model. The former postulate is that major geological changes might have been the chief factors initiating migration, while the last one is concerned with the idea that any bird can become migratory if the environmental conditions deteriorate sufficiently to cross a genetically determined ‘‘migration threshold.’’ However disparate the various theories may be, according to Rappole (1995) they are identical with respect to the central points: ‘‘The one factor that all these theories have in common is an ancestral sedentary population’’ and ‘‘All of the theories begin with something that causes the ancestors to move.’’ This implies that there was a ‘‘behavioral jump’’ from the sedentary to the migratory condition. Two explanations have been proposed for this jump: chance mutations and a stepwise development from dispersal through facultative migration to obligate migration (e.g., Terrill, 1990). It has also been postulated that migratory behavior developed several or even many times independently during the evolution of birds, in various systematic groups and in various regions of the earth (Farner, 1955). Neither explanation is void of error. Regarding mutations, if we accept the postulated polyphyletic origin of migration, we have to ask how this trait could have occurred so often independently in different lineages. Furthermore, if mutations were responsible, how could species and populations switch between migratory and sedentary behavior, often rapidly, as has been demonstrated in a number of species (e.g., the serin, Serinus serinus: Mayr, 1926) and as is now occurring increasingly often in the course of global warming? Regarding the postulated sequence from dispersal to obligate migration, Rappole (1995) points out the following problem: ‘‘Yet, for the phenomenon to be migration, as opposed to dispersal, not only must something force the individual bird away from its point of origin initially, but something must also push it back to its point of origin later in the annual cycle. Also, this something must act over and over again.’’ Although Rappole (1995) sees this ‘‘something’’ as the ‘‘deterioration of weather in the temperate zone,’’ there is a problem here: Given that many periodic seasonal to-and-fro migrations are clearly largely independent of the weather (Berthold, 2001), how could migration

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become an endogenous program, as it is known to be (see next section)? Furthermore, modern phylogenetic analyses based on molecular biology show that when migratory behavior has once been acquired—whether by mutation or evolutionary sequence—it is not simply passed on by inheritance in evolutionary lineages but can be extinguished as well as subsequently revived (Helbig, 2003; Joseph et al., 2002). There are also problems in explaining the behavioral change between migrating and not migrating on the basis of learning (phenotypic plasticity), because many songbirds never reach the age of two years and hence can neither collect nor make use of experiences distributed over long periods of time. All these obstacles to understanding were swept out of the way by a simple, new theory of bird migration derived from the results of studies on warblers and redstarts that incorporated genetics and experimental evolutionary biology; it is presented in Section VIII. In conclusion, two more points regarding the evolution of bird migration should be mentioned here because they will be important later for understanding the new theory. Researchers on bird migration nowadays generally agree that migratory behavior (i) arose very early in the evolution of birds, evidence for which includes fossil finds, and (ii) first developed under tropical-subtropical conditions and not under the pronounced seasonal conditions typical of higher latitudes, to which birds were later increasingly exposed (Rappole, 1995; Berthold, 2001). Until genetic studies became a medium for biological research, a degree of uncertainty similar to that regarding the evolution of bird migration existed with respect to the mechanisms controlling the migration itself. The various assessments of the roles of endogenous and exogenous control mechanisms have been quite contradictory, as can be demonstrated with reference to obligate partial migration. This is a widespread mode of life, exemplified by American or European robins (Turdus migratorius, Erithacus rubecula), in which part of the population regularly migrates away from the breeding grounds while the rest of the birds spend the winter there as permanent residents. Since the 1930s two completely opposite hypotheses were formulated to explain the phenomenon. The ‘‘behavioral-constitutional hypothesis’’ postulates a noninherited, facultative determination of migratory behavior, depending on population density, resource availability, and especially constitution and social rank. Migrants are understood to be the losers in disputes between individuals, whereas winners are thought to stay as residents. According to the ‘‘genetic hypothesis,’’ the decision of whether an individual will be migratory or sedentary is already made in the egg by combination of the parental genetic inputs (for details see Berthold, 2001; and Section V.H).


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III. The Discovery of Circannual Rhythms: The Challenge to Genetic Studies As long ago as 1702, von Pernau surmised that bird species at higher latitudes that begin their outward migration very early in the year—for instance, in July/August—are not simply ‘‘driven away by hunger and cold,’’ but rather there is ‘‘a hidden drive forcing them [to depart] at the right time,’’ which often proves to be when the summer half-year is at its peak. Nevertheless, it took until the 1960s for ideas about endogenous control of bird migration (and also about annual periodicity of organisms in general) to develop sufficiently so that a systematic search for underlying mechanisms was instigated. Such periodicity was first documented beginning in 1960, with publications on molluscs and mammals, and then from 1967 on researchers in our institute produced evidence that birds possess so-called circannual rhythms such as endogenous annual cycles and internal calendars as special forms of biological clocks (Gwinner, 1967; Berthold et al., 1971). These physiological body rhythms, the development and control of which in the organism have not yet been satisfactorily clarified (Gwinner, 1986), nevertheless control the course of many events with annual periodicity in a multitude of different animals from coelenterates to mammals, and also in plants. In birds, the existence of circannual rhythms (from the Latin circa [about] and annus [year]) has been established in about 30 species. In about 20 migrant bird species of various systematic groups and for birds on five continents they have been demonstrated to control all essential events of migration, such as the development of migratory activity and migratory fattening (Figure 1), and they are also involved in the control of migratory orientation, seasonal food consumption, food preferences, annual hormonal cycles and certainly other migratory events as well (Gwinner, 1986; Berthold, 1996). Given that they also control other annual processes such as reproduction and molt, which in turn profoundly affect migratory behavior, their overall influence on processes of migration appears to be substantial. Although, as mentioned above, the nature of the oscillators underlying circannual rhythms has not yet been analyzed, so there is little if any doubt that these rhythms are genetically controlled. For example, circannual rhythms are present and functional in the youth of mammalian hibernators, even though the parental animals have been kept under constant environmental conditions (Gwinner, 1986). Moreover, circannual rhythms in migratory birds do not merely initiate individual processes such as migratory activity or fattening, but evidently also control their temporal patterns, at least to some extent (Fig. 1). In view of these findings, it seemed to me highly likely that basic processes and characteristics of bird migration are

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1st year 6

2nd year

3rd year

Testes length (mm)

3 0 600

Restlessness (hops)

300

OM

RM

OM

RM

0

35

Body mass(g)

25 15 Moult M

J

S

N

J

M M J Time (months)

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Fig. 1. Endogenous annual periodicity (circannual rhythms) of (from top to bottom) testes length, migratory activity (restlessness, nocturnal locomotor activity), body mass, and molt of a male garden warbler. The hand-raised bird hatched at the end of May was transferred to constant conditions (a light-dark regime of 10:14 hrs) in June (arrow), and was kept there for 10 years; the results depicted are from the first three study years. OM ¼ outward migration period, RM ¼ return migration (after Berthold et al., 1971).

inherited (directly controlled by genetic factors). To explore this possibility, a new research field had to be developed devoted to experimental genetics of avian migration. The first task was to perform classical crossing and selection experiments in order to test the extent to which genetic factors are involved in controlling migration so that if the results were positive, in-depth studies could be undertaken.

IV. The Search for and Selection of Bird Species Suitable for Testing At an early stage, in the ‘‘warbler program’’ set up in our institute (e.g., Berthold et al., 1970) to investigate the biology of one bird group as comprehensively as possible, it had come to our attention that the blackcap (Sylvia atricapilla) was an outstandingly suitable candidate. Of the diverse forms of migratory behavior known to exist in the Eurasian-African system


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of migratory birds, the various widely-distributed populations of blackcaps exhibit more than any other species (Figure 2). In the Mediterranean region of Europe and in North Africa they are characterized by short-distance and partial migration (with migratory and sedentary individuals within the same population), in central Europe by medium-distance migration, and from Scandinavia to Siberia by long-distance migration, while some populations are entirely sedentary (on the Cape Verde Islands, Madeira and the Azores). The migration directions depend on the population, ranging from southeast through south and west to west-northwest. Two migration divides separate, to a great extent, the mainly central European group that migrates to the southwest and southeast (largely circumventing the Alps) from the

T T

T T P

T

R

R P R

Fig. 2. Schematic representation of the life styles and migration routes of blackcaps. T ¼ total migrants, P ¼ partial migrants, and R ¼ residents; thick arrows ¼ main migratory directions, thin arrows ¼ secondary directions, dashed line ¼ outer limits of breeding range; hatched areas ¼ wintering grounds; black circles ¼ provenance of test birds (see text) studied at the Vogelwarte Radolfzell (after Berthold, 1999).

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northwest migrants – the latter on their way to overwinter in the British Isles, a recent development (Section IX.B). Furthermore, blackcaps are fairly common throughout their range, so that birds can be collected for experiments from the entire distribution (Berthold, 2001). Because blackcaps have been popular cage birds for centuries, the best conditions for keeping them are well known and nowadays are unproblematic; furthermore, before our studies began, amateurs occasionally had experience in breeding them as single pairs or a few pairs together (Berthold et al., 1990). In 1970 we began our own breeding program, and after pilot experiments over seven years we were in a position to breed blackcaps successfully on a regular and fairly large-scale basis. To give an impression of the size of the program: by now we have hand-raised and investigated over 3000 individuals from 10 different areas (Fig. 2), and nearly 1800 individuals have been bred in our aviaries. For it to be possible to breed considerable numbers of originally wild migratory birds in aviaries, quite a few prerequisites had to be fulfilled, and we worked out the subtleties involved step by step. Among the most important were preparing suitable aviaries with an appropriate microclimate, so that the birds would accept them for breeding; introducing the potential breeders to the aviaries at a very early stage, so that they would settle in and be ready to breed at the species-specific time and long enough before the summer molt; gradually allowing first the females and only thereafter the males to become accustomed to the aviaries, so as to avoid territorial battles with a lethal outcome; and feeding at multiple sites to prevent monopolization of the food source, mainly by males (for a detailed list of the permissive factors for successful breeding of blackcaps in aviaries see Berthold et al., 1990). In recent years we have extended our breeding experiments to several other species to learn what happens when the crossing is not intraspecific— with birds from different populations, as in the case of the blackcap—but interspecific. Redstarts (Phoenicurus), for instance, are suitable for this purpose: Members of this genus exist in a number of closely-related species all over Eurasia and in northern Africa, and at least some of these forms are known to interbreed in the field to some extent and to produce fertile hybrids as well as back-crosses. Such hybridization is reported to occur every year among the common and black redstarts (Phoenicurus phoenicurus, P. ochruros), which are sympatric in Europe (e.g., Grosch, 2000). We use these primarily for genetic studies and have bred about 100 individuals in the last ten years. At present we are hybridizing two other species: the scarlet rosefinch (Carpodacus erythrinus), which is one of the few long-distance and nocturnal migrants among the granivorous songbirds, and the domestic canary (Serinus canaria). The aim here is to test the extent to which the


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characteristics of migratory birds can be crossed into a form that is nonmigratory and, furthermore, domesticated.

V. Genetic Control A. The Approach In an initial experiment (1978 and 1979) we succeeded in demonstrating, by crossing blackcaps from Africa (Canary Islands, partial migrants) and Europe (southern Germany, exclusive migrants), that the populationspecific time program of migratory activity is inherited (genetically controlled; Berthold and Querner, 1981). The results also provided strong evidence that the migratory behavior (the ‘‘migratory drive’’ of the former literature) as well as morphological features and juvenile development associated with migration are likewise inherited (see later). Above all, however, these genetic studies proved the usefulness of our most important method of investigation: the measurement of migratory activity as ‘‘migratory restlessness’’ (Zugunruhe) in recording cages. It had been known for centuries—especially among bird enthusiasts—that at the times of year when their migration normally occurs, night-migrating bird species such as the blackcap become restless at night even when they are kept in a cage, aviary, or enclosed room. A number of our earlier studies had progressively confirmed that this nocturnal restlessness is definitely a form of true ‘‘migratory activity,’’ because it closely mimics the course of migration in free-living conspecifics (reviews: Berthold, 1996, 2001). Now that this recorded migratory activity of caged birds has been shown to have a genetic basis, its innate nature is confirmed; hence the recording of such activity is a reliable instrument for experiments on the migratory behavior of birds. This conclusion is corroborated by investigations of exactly what the migratory restlessness represents. By making video tapes of nocturnally active warblers under infrared light that is invisible to the birds, we were able to show that migratory restlessness (Zugunruhe) is confined mainly to so-called wing-whirring: fluttering the wings at high frequency but low amplitude while sitting on a perch (Fig. 3). We also showed that the time spent in this ‘‘migrating while seated,’’ multiplied by the species typical flight speed, would be just sufficient to bring the birds to their specific winter quarters; that is, it is the expression of an endogenous time program (review: Berthold, 2001; Section V.E). Thus it was adequately demonstrated that nocturnal restlessness in blackcaps and other investigated species expresses migratory activity, and we could use this recording method to test all the fundamental parameters of the behavior of migrants

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Fig. 3. A blackcap showing the typical movements during the nocturnal phases of migratory restlessness (Zugunruhe): wing whirring (from video recordings in infrared light; for details see text and Berthold et al., 2000).

and sedentary birds with respect to their genetic bases. The results are sketched briefly in the following sections.

B. Migratory Behavior Early departing long-distance migrants have often been termed ‘‘instinct migrants’’ on the assumption (unproven at that time) that they were induced to migrate by endogenous factors (as had already been supposed by von Pernau, 1702; see Section III). They were regarded as being in a different category from ‘‘weather migrants,’’ the migration of which began later and in some cases at irregular times, and hence was thought to be triggered by exogenous factors such as the seasonal decline of food availability or ambient temperature. But even for the ‘‘instinct migrants’’ the possibility could not be ruled out that some exogenous factors, such as the decline of a certain prey species, might have a triggering influence. Therefore experiments were needed to test the idea that migratory activity exists in the sense of an ‘‘instinctive behavior’’ (Berthold, 2001). We were able to produce just such a demonstration in two types of experiments on blackcaps, including some late-migrating partial migrants. In a first experiment we crossed blackcaps from southern Germany, which


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are exclusively migratory (more than 99% migrants), with conspecifics from the Cape Verde Islands, which do not migrate at all. In the offspring we found that about 40% of the individuals were migratory (i.e., displayed migratory restlessness like their migratory German parents). This indicates that the migratory activity can be genetically transmitted into the offspring of a nonmigratory population. Since migratory activity was observed in only about 40% of the offspring, this activity is most likely a polygenic trait, presumably with a threshold (Section VI), because if it were a singlelocus system, all the F1 hybrids would have been expected to show some migratory activity. And migratory activity is also certainly not a simple dominant trait because if it were, all the hybrids should have engaged in it. Very similar results demonstrating inheritance of migratory behavior were obtained from cross-breeding experiments with nonmigratory blackcaps from Madeira and migratory conspecifics from Germany and Russia (unpublished). For the strength of genetic determination of migratory features see Section VI.B. Another interesting result was that the amount of migratory activity displayed by the active 40% of the hybrids was almost exactly intermediate between the amount exhibited by the migratory German population and the zero level of the Cape Verde group (Berthold, 2001). This corresponds with the result of the above-mentioned cross-breeding experiment with migrants from Germany and the Canary Islands. Finally, when the individuals with migratory activity were tested with respect to orientation behavior, they showed a significant directional preference. Since this preference was in good agreement with the principal axis of migration of the migratory German parental population (NE-SW for the outward journey and SW-NE for the return), it seems a reasonable conclusion that the population-specific directional preference was genetically transmitted together with the migratory activity (in a so-called migration syndrome, Section VI), and that orientation behavior is also inherited (see Section V.D). In a second type of experiment, a partially migratory population was converted to either sedentariness or migratoriness by selection alone, again indicating that migratory behavior is inherited (for details see Section V.H). C. Date of Departure One experiment in particular gave us strong indications that the onset of migration—the date of departure is to a large extent endogenously and thus presumably inherited, at least in inexperienced songbirds, migrating for the first time. When we compared the onset of migratory activity (restlessness) during the autumn migratory period in hand-raised individuals of 19 different songbird species and populations (Sylvia, Phylloscopus

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and Acrocephalus warblers, redstarts, some seed-eaters, etc.) with the onset of actual migration of birds of the same populations in the wild (at a trapping station), we found a very close relationship indicated by a correlation coefficient of 0.967. This high degree of agreement indicates that the same (endogenous) factors that release migratory restlessness in caged birds (living under largely constant environmental conditions) also essentially trigger the onset of migration in wild conspecifics, and that in this case modifying environmental factors play a minor role, if any (Berthold, 2001). We were sufficiently impressed by this indication of a possible genetic control of departure dates that we designed a test using redstarts. Of the two redstart species in Europe, the common redstart is an earlydeparting long-distance migrant, leaving central Europe in August for its winter quarters south of the Sahara (Figure 4). The black redstart is a latedeparting short- to medium-distance and partial migrant, which leaves its central European breeding grounds in October/November and overwinters mainly in the Mediterranean region. Both species are nocturnal migrants— like the blackcap—so that their migratory activity in captivity can easily and reliably be recorded. Its onset occurs exactly at the same time of the year as the initiation of migration in free-living redstarts (Berthold, 1985). When the two species were experimentally hybridized, the migratory activity of the F1 individuals was largely intermediate between the values found for the parental species (Figure 4). It can be concluded from this result that the date of onset of migratory activity is also inherited. There are strong indications that this level of inheritance applies to many other species (Berthold, 2001) and populations within given species that live next to one another but are largely separated by breeding areas at different altitudes (‘‘altitudinal races,’’ of the garden warbler Sylvia borin: Widmer, 1999). Genetic factors also affect the duration of migratory activity and its termination, as Figure 4 demonstrates. However, in the case of the two redstarts the evidence is not so conclusive, as both species end migration at the same time; better examples are presented in Section E. D. Migratory Direction It has long been hypothesized that the directions in which migratory bird species migrate are ‘‘endogenously programmed’’ or inherited. This idea was based on at least six different types of observations: (1) recoveries of ringed birds show that within a given species, even one in which the individuals migrate alone and at night, the direction is constant, flight normally being confined to relatively narrow corridors; (2) inexperienced migrants tested in orientation cages regularly exhibit population-specific


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Fig. 4. Black redstarts, as short-distance migrants, migrate about 1000 km from southern German breeding grounds to Mediterranean winter quarters (dotted areas); common redstarts from the same area migrate about five times further, to destinations south of the Sahara (after Berthold, 2001). Below: Mean values and standard errors of time course of migratory activity (restlessness) in hand-raised common redstarts (lower white bar), black redstarts (upper white bar), and their hybrids (black bar) during the first outward migration period. 0 ¼ date of hatching of the experimental groups (after Berthold and Querner, 1995).

directions; (3) when first-time migrants (of a few species like the European starling Sturnus vulgaris or white stork Ciconia ciconia) were displaced in the field, the resulting migratory directions paralleled those of their parental populations; (4) inexperienced individuals of the cuckoo (Cuculus

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canorus) prefer distinct migratory directions (from central Europe southwards, to winter quarters in central Africa), independent of those taken by their various migratory foster parents and even when the parents are nonmigrants; (5) seasonal shifts in migratory directions of some species are also shown by inexperienced individuals in captivity (later), and (6) even irregular migrants, whenever they do migrate, regularly move in specific directions although their last trip may have been several years ago (for review see Berthold, 1996, 2001). In four experiments with blackcaps, we were able to show that a migratory bird’s choice of direction can indeed be inherited. The first one was the experiment described above (Section V.B), in which migratory blackcaps from southern Germany were crossed with sedentary birds from Cape Verdes. When the migratorily active hybrids were tested for directional preferences during the autumn and spring periods in which they develop migratory activity, they preferred a NE-SW axis that was in good agreement with the principal axis of migration of the migratory German population. Thus the preference for a specific migratory direction had been genetically transmitted together with the migratory behavior (migration syndrome; Berthold, 2001; Section VI). In a second experiment, blackcaps from the two sides of the central European migration divide (see Fig. 2) were crossbred, one parent exhibiting a SE migratory direction and the other a SW direction. The hybrids showed intermediate orientation (Fig. 5). Furthermore, SE migrants perform a seasonal shift in their migratory directions towards the south (these in captivity and in the wild), to ensure that they will arrive in their southern African winter quarters and not fly over the Arabian peninsula into the sea. SW migrants do not shift direction in this way, because the majority terminate their journey upon reaching the Mediterranean region. The hybrids of the two populations shifted slightly, a clear indication that even the extent of this change in direction is genetically programmed and inherited (compare the October and November data in Fig. 5). A third case concerns central European blackcaps, which since the 1960s have been increasingly wintering in the British Isles. Their novel migratory direction—determined by selection, as an experimental study has shown—is already being passed on to their offspring (Section IX). And finally, in a fourth experiment it was shown that hybrids produced by individuals that winter in England and those that still migrate to the Mediterranean demonstrate intermediate migratory directions (Helbig et al., 1994). In view of these experiments with blackcaps, migratory direction is inherited, probably as an additive trait, the expression of which is most likely controlled by a number of different genes (Section VI).


N

N October

O S

November

O

W

189

W

S

Fig. 5. Directional choice of hand-raised blackcaps in orientation cages in October (left) and November (right). Solid triangles ¼ birds from southern Germany; open triangles ¼ birds from eastern Austria; dots ¼ hybrids of the two populations; long solid triangles ¼ average direction (after Helbig, 1989).

E. Termination of Migration and Goal Finding: The VectorNavigation Hypothesis It is clear from many observations and above all from bird banding and ringing recoveries that the winter quarters of migratory birds, like their breeding grounds, are normally species-specific, even population-specific. For a long time it was a mystery how European cuckoos, for instance, could arrive collectively at their central southern African winter quarters even though individual cuckoos had been raised by many different types of parents, such as nonmigratory winter wrens (Troglodytes troglodytes), partially migratory European robins with their migratory fraction mainly oriented towards the Mediterranean, or marsh warblers (Acrocephalus palustris) wintering exclusively in SE Africa. This goal-directedness was equally mysterious in the case of the very numerous first-time migrants of species in which individuals migrate alone and, as a rule, well before the departure of their parents and of other breeding conspecifics already experienced in migration. Not surprisingly, people resorted to some rather improbable explanations of this ability. One idea was that these first-time migrants had an innate ‘‘knowledge’’ of some characteristics of their destinations, such as the pattern of stars above the winter quarters. However, if such birds are taken to their winter quarters before the onset of their autumn migratory period, they continue to exhibit migratory restlessness just as long as do their conspecifics remaining in the breeding grounds, which

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shows that the hypothesis of star-pattern navigation is not valid (Gwinner, 1971; Berthold, 2001). In the past 25 years or so, a great number of experiments have corroborated the alternative notion that once a bird was travelling in a specific, inherited direction, an endogenous program could automatically guide it to the winter quarters by terminating migration after a specific time. In this ‘‘vector-navigation hypothesis’’ the crucial vector is composed of the programmed migratory direction (Section V.D) and an endogenously produced amount of migratory activity, such that the bird continues to migrate for just the amount of time (days, weeks, or months) required to cover the appropriate distance. A navigation mechanism of this kind was postulated as early as 1923 by von Lucanus, but it did not seem very plausible until the following experimental findings became available. In the first test involving about 30 species and populations, mainly songbirds, we showed that the amount of migratory activity produced (measured as migratory restlessness in captive individuals as described previously) is closely correlated with the migration distance. Furthermore, two different methods of analysis have revealed that the total amount of migratory activity (restlessness) during the first outward migration period would, if it occurred as migratory activity in the wild, carry inexperienced migrants from their breeding grounds to their wintering areas. From ringing recoveries of leaf warblers (Phylloscopus) Gwinner (1968) calculated distance performances for different stages of their outward migration, correlated these results with corresponding values of migratory restlessness, and derived theoretical migration distances by extrapolating from the total amount of restlessness during the whole autumn migratory period. The result was that flight activity equivalent to the recorded restlessness would have brought the investigated species precisely into the center of the species-specific winter quarters. In the garden warbler, Berthold and Querner (1988) recorded and analyzed restlessness using video recordings under infrared light conditions at night. This procedure revealed that restlessness is almost exclusively expressed by wing whirring (the generation of high-frequency wing beats of low amplitude while perching [Section V.A]). If the total time spent in whirring activity is multiplied by the average flight speed of the species, the resulting distance would again place the birds in the center of their speciesspecific wintering grounds. From these results it has been deduced that migratory activity represents an endogenous program of the migratory course (Berthold, 2001). Subsequent to these findings we showed unequivocally in two crossing experiments that the temporal patterns of migratory activity are indeed endogenous time programs for migration: They are inherited. One of the


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experiments was done with blackcaps obtained from two populations: medium-distance migrants from southern Germany and short-distance migrants from the Canary Islands. In the other, two species of redstarts were crossed: black redstarts, which are short- to medium-distance migrants, and common redstarts, which are long-distance migrants (Section IV). In both cases the hybrids exhibited intermediate amounts of migratory activity, demonstrating genetic influence (Fig. 6). Thus, at least blackcaps and redstarts are equipped with programs related to the course of the migration that can be inherited as population- or species-specific features, respectively. In addition, temporal distribution of migratory activity during the course of the migratory period also appears to be programmed in relation to environmental requirements of the migratory route and journey. Eurasian long-distance migrants that normally cross the Sahara Desert towards the middle of their autumn migratory period show a distinct peak of migratory activity in caged individuals during this time, just when free-living individuals are performing their most intensive migratory flights. This holds true for species of various systematic groups (Berthold, 2001). Other species, such as the barred warbler (Sylvia nisoria), that migrate around the Mediterranean and the Sahara, show evenly distributed migratory activity. In the case of short-distance migrants that start their migration relatively late in the year, migratory activity is maximal towards the end of their short periods of activity. The marsh warbler, migrating rapidly from central Europe to northeast Africa but then continuing slowly on its long way to southern Africa—a phase that lasts until the end of the year and may even include a short resting period—shows a two-peaked and extremely extended pattern of migratory activity (Berthold, 2001). The experiments and observations described above made the vectornavigation hypothesis progressively more likely, so that today it has become generally accepted. Furthermore, at present no plausible alternative hypothesis is available. The means by which inexperienced birds, migrating for the first time and often travelling alone, find their way ‘‘automatically’’ to their specific winter quarters on the basis of an inherited spatiotemporal program (as postulated by this hypothesis) can be described in highly simplified terms as follows. Birds in this category can be considered as functioning like toy cars with mechanisms wound up to different degrees, which are set free while facing in different directions. That is, their travel is describable by different vectors composed of running time and direction, and as a result they come to a halt in quite different destination areas (in the case of birds in the field, when the endogenously generated migratory activity is extinguished). Within these fairly large destination areas they choose their specific wintering site. Then in later

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10

8

6 SG

Migratory restlessness (1/2 h)

4 CI x SG

2 CI 0

10

8

6 CR BR x CR

4

2

BR

0 0

50

100

150

200

Times (days) Fig. 6. Above: patterns of migratory activity (restlessness) of hand-raised blackcaps from two populations and their hybrids during the first outward migration period. SG ¼ Southern Germany, CI ¼ Canary Islands. Depicted are mean values and standard errors for decades; 0 ¼ onset of migratory activity (after Berthold and Querner, 1981). Below: corresponding patterns of black redstarts (BR), common redstarts (CR), and their hybrids (after Berthold et al., 1996).

seasons—if they survive—they can head for and locate this site by goal orientation (just as they find the natal breeding area) since now the site is already well known. For possible mechanisms of goal orientation (or genuine navigation), applicable by older, experienced birds, see Berthold (2001).


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F. Juvenile Development Migration is quite costly to a bird in terms of both time and energy, so its place in the schedule of processes of annual periodicity must be arranged correspondingly. Moreover, because migration often makes severe demands on flying ability and on the capacity for thermoregulation, intact plumage is essential for most migratory flights. These requirements must be fine-tuned for compatibility with other annual processes for success in reproduction, molt, and in the case of young birds migrating for the first time, the entire juvenile development. From our warbler studies and many other investigations the following rule can be derived: The earlier a bird species or population departs for the winter quarters (and in most cases, the further it must travel), the more rapid is its juvenile development, especially the juvenile molt, and hence the greater the overlap between individual developmental processes. In particular, a detailed comparative study of blackcaps, garden warblers, and barred warblers has further demonstrated the following. In birds that depart very early, the accelerated juvenile development begins while the bird is still an embryo (Berthold, 1988). Even within a species, individuals that hatch late in the year develop much more rapidly than their conspecifics born earlier. This is due to a photoperiodically controlled ‘‘calendar reaction,’’ such as the effect of the shortening of days after the summer solstice. This acceleration can also be elicited in individuals that have hatched early if they are then kept or raised under short-day conditions (Berthold, 1988). The differences in juvenile development of species or populations that migrate at different times, however, are inherited. Experimental results documenting this are available for four bird species—blackcap, the two redstarts, and stonechat (Saxicola torquata). In cross-breeding experiments, whether between different populations (blackcaps, stonechats; Berthold, 2001; Gwinner and Neusser, 1985) or between different species (common and black redstart, Berthold et al., 1996), the offspring undergo a juvenile molt of intermediate duration (Fig. 7). In the garden warbler, there are strong indications of inheritance over the course of the entire juvenile development. In garden warblers from Finland, which stay in their breeding grounds for shorter periods than conspecifics in Germany, the processes of juvenile development were found to be more rapid, or to have a greater initial intensity. When handraised individuals were kept in constant photoperiodic conditions or in conditions simulating those normally experienced by birds of the other populations, differences in the juvenile development as small as a very few days remained discernible (Berthold, 1996). Furthermore, sibling effects and heritability estimates for different traits of juvenile molt in

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BR

BR x CR

CR

0

50

100 Time (days)

150

200

Fig. 7. Mean values and standard errors of time course of juvenile molt in hand-raised common redstarts (lower white bar), black redstarts (upper white bar), and their hybrids (black bar). 0 ¼ date of hatching of the experimental groups (after Berthold et al., 1996).

both stonechats and garden warblers demonstrated high genetic variation, clearly indicating substantial genetic influence (Helm and Gwinner, 1999; Widmer, 1999). G. Migratory Disposition and Prerequisites Before a migrant departs, it normally enters a special physiological state called ‘‘migratory disposition.’’ This state of readiness to migrate comprises hormonal, behavioral, and metabolic adaptations, the latter related chiefly to fat metabolism. Most characteristic of migratory disposition is a distinct body-mass increase due to the distribution of fat to serve as fuel and the deposition of protein to maintain physiological processes. In small birds performing long-distance migrations, migratory fattening often results in a doubling of the body mass, whereas in medium- to short-distance and partial migrants, fattening is less pronounced or even absent (Berthold, 2001). Of the many characteristics of migratory disposition, only two have so far been examined with respect to genetic control: body mass development and fat deposition. Because body-mass changes are relatively indistinct in blackcaps that migrate over medium and short distances, we chose redstarts for a cross-breeding experiment addressing this question. Particularly suitable for this purpose are the common redstart and black redstart. The common redstart, which migrates from central European breeding grounds to winter quarters far away (about 5000 km south of the Sahara), greatly increases its body mass by intensive fat deposition, beginning during the juvenile molt and continuing for more than 4 months

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(Fig. 8). On the other hand, the black redstart, a short- to medium-range migrant starting from the same breeding grounds, travels only about 1000 km to its Mediterranean winter quarters. But it precedes this by a twomonth accumulation of less fat so that its body-mass increase is only moderate for the migration. Hybrids raised in aviaries were intermediate in the shape of their body-mass curves (Fig. 8) as well as in the size of their fat depots (Berthold et al., 1996). Blackcap hybrids of long-distance migrants from Russia and nonmigrants from Madeira gave similar results (unpublished data). Most probably, many more features associated with the migratory disposition are inherited: the choice of food observed in many bird species, including the frequent seasonal shifts from insectivorous to vegetable diet during the migratory period, or the spontaneous habitat selection in staging areas on the basis of ‘‘Gestalt perception.’’ The same applies to morphological features such as the length, shape and pointedness of the wings. In this context, the hybridization of redstarts yielded interesting results. For instance, the black redstart has a long sixth primary with a notch on the outer web which is absent in the shorter sixth primary of the common redstart. Hybrids are intermediate in both primary length and depth of the notch. For more details see Berthold (1999) and Berthold et al. (1996).

Body mass (g)

15

10 CR

BR x CR

5

BR 0 J

A

S

O

N

D

J

Time (month) Fig. 8. Mean values and standard errors (for approximately weekly intervals) for time of body mass development (above all reflecting fat deposition) in hand-raised black redstarts (BR), common redstarts (CR) and their hybrids during the first outward migration period (after Berthold et al., 1996).

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H. Partial Migration Partial migration has long been of the greatest interest to naturalists, primarily because they hoped that by understanding it they would also gain fundamental insights into the origins of migration generally. This applies in particular to obligate partial migration, the main form considered here, in which some of the individuals of a population or species leave the breeding grounds every year, whereas the others stay there permanently. Partial migration can take the birds to remote winter quarters or merely to areas more favorable for feeding, etc. Facultative partial migration, in which the migrants do not leave the breeding region every year but only at irregular intervals, is of less interest for present purposes. A considerable number of special cases of obligate partial migration have been given names of their own—depending on how many birds migrate away from the various populations—but these have not been adopted as standard in the literature and hence will not be mentioned further here (but see Berthold, 2001). The typical obligate partial migration was described by the medieval emperor Friedrich II, and as long ago as 1758 Linnaeus named the chaffinch Fringilla ‘‘coelebs’’ (celibate) because in the northern (Swedish) breeding grounds only males stay throughout the winter (Berthold, 2001). Ringing results have elucidated that partial migration as a whole is a very complex polyphenism of migratory and sedentary habits which differ with respect to time, distribution, sex, and age. Lack (1943/1944) already realized this and foresaw that ‘‘partially migratory species reveal a problem of remarkable complexity, and one which appears capable of full solution only with the help of large-scale and very difficult experiments.’’ There was still a long way to go, and initially two contradictory and controversial hypotheses were proposed about the control of obligate partial migration in birds—the ‘‘genetic’’ hypothesis and the ‘‘behavioralconstitutional’’ hypothesis. These are to be understood as extreme attempts to explain a control which, in fact, may well include both genetic and environmental factors. These hypotheses were discussed in many publications before experimental studies provided clear bases for a conclusion. As explained in Section II, the genetic hypothesis (Landsborough Thompson, 1926; Nice, 1933, 1937; Lack, 1943/1944) states that the decision as to whether a nestling will later be a migrant or resident individual is made in the egg by the combination of parental genes. From a contemporary point of view it claims that partial migratory behavior is a polygenic trait. For this reason even migratory parents can, to a certain extent, produce nonmigratory offspring and vice versa, and a single clutch might often produce both migratory and nonmigratory offspring (Nice, 1933, 1937). The behavioral-constitutional hypothesis (Miller, 1931;

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Kalela, 1954; Gauthreaux, 1978; Lundberg, 1988) proposes that weaker individuals are displaced during post-breeding skirmishes over food and temporary territories, and are eventually forced to migrate away, whereas stronger individuals are able to stay in the breeding area. Although individual constitution is influenced to a large extent by genetic factors, this hypothesis claims that it is primarily exogenous factors such as food availability, population density, and dominance structures that determine migratoriness or residency (for reviews see Dingle, 1996; Berthold, 2001). Starting in 1977 we tested the two main hypotheses for the first time, using the partially migratory blackcap population from southern France, of which 75% were migrant and 25% resident (Figure 9). The partially migratory habit of the population in the wild is well-established by ringing and retrapping results, and the ratio of migrationally active to inactive individuals was determined by testing for migratory restlessness (Berthold et al., 1990, Section V.A). In a two-way selection experiment, selective breeding with resident birds yielded a proportionally higher number of resident birds as compared with the parental stock, and a corresponding result was obtained for migratory birds. The result of this selection Selective breeding of nonmigrants

0

48 65

5 41

% of migrants

76 52 50

267

59

Selective breeding of migrants 62

47

100 P

F1

F2

F3

F4

F5

F6

Generations Fig. 9. Results of a two-way selection experiment on partially migratory blackcaps from southern France (composed of about three quarters migratorily active and one quarter inactive individuals). Nonmigrants were bred up to the F6 generation, migrants up to the F3 generation. Solid lines ¼ results of selection experiments; broken lines ¼ mathematical functions with best fit; 267 ¼ number of hand-raised birds of parental stock; other numbers indicate how many individuals have been bred in different generations (after Berthold et al., 1990).

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experiment was very striking, as the percentage composition of the F1 generation was significantly different from that of the parental generation (Fig. 9). Thus, there was already a strong selection response in the F1 generation, clearly indicating that genetic factors are immediately involved in the control of both behavioral traits, migratoriness and sedentariness. In view of the clear results obtained in the F1 generation, we would expect a continuation of the two-way selection experiment to produce a rapid further increase in migratoriness or sedentariness. The actual result was amazing. After only 3 generations the original partial migrants became pure migrants and after only 6 generations (almost) pure residents (see Fig. 9). The outcome is a unique demonstration of the speed with which vertebrates can change their behavior on a genetic basis. This finding also suggests that partial migration has an enormous microevolutionary potential, which will be further treated in Section VII. In the meantime, similar results confirming the genetic influence in the control of obligate partial migration have been obtained for six other species (European robin, European blackbird Turdus merula, stonechat, grey-breasted silvereye Zosterops lateralis, song sparrow Melospiza melodia, and great crested grebe Podiceps cristatus; for review see Berthold, 2001). Evidently, genetic influence plays an important role in the control of migratory and nonmigratory behavior of at least seven different obligate partially migratory species, and no contradictory finding has been reported for any other species so far. I. Interaction with Other Annual Cycles As was pointed out in the context of juvenile development in Section V.F, the place of migration in the schedule of annual processes must be arranged in such a way that its physiological and energetic prerequisites for migration are fulfilled, so that migration itself can proceed smoothly. The life of a migrant is characterized by four or five vital annual processes, namely the spring and autumn migration, the breeding period, and generally two molt periods, although occasionally there is only one molt period. Processes of molt are scheduled in such a way that normally no migrant has to fly with gaps in its wings, and the feather quality is high during migration. For instance, molting of wings and tail is either completed before departure, started after arrival at the wintering grounds, or sometimes undertaken at intermediate stopover sites. Many species can interrupt their molt: Wing and tail molt are started at the breeding grounds and discontinued during migration, and the remaining old feathers are finally replaced at the winter quarters. (For other more special cases see Berthold, 2001.) The molt of body feathers is also largely incompatible


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with migration, especially in the case of long-distance migrants. In order to cross ecological barriers, birds often must fly at an altitude of several thousand meters, and in this case intact plumage is also important for thermoregulation. In many migrants specific adaptations are needed in order to fit a successful reproductive period in between two consecutive migratory periods. This applies in particular to intercontinental long-distance migrants, which may be en route for up to ten months. Since birds generally have a pronounced gonadal cycle with an increase of testicular and ovarian size by a factor of over a thousand in time for the breeding season, the time spent on the breeding grounds may often be too short to allow for both complete gonadal development and successful breeding. Therefore most, if not all, categories of migrants initiate their gonadal development on the wintering grounds, before the homeward migration. However, the gonads do not achieve complete maturity during the trip home, probably in part because it would consume extra energy to transport fully developed gonads, and also because during migration there is evidently an antagonism between gonadotropins and hormones involved in metabolism. Several rules of thumb seem to apply here: (1) that gonadal development at arrival on the breeding grounds is more advanced in late migrants, which arrive shortly before breeding, (2) that gonadal development before arrival is more pronounced in males than in females and (3) that the main gonadal development seems to take place rapidly, often in a few days, after arrival at the breeding grounds. Furthermore, it appears that long-distance migrants, which have less time to spend in the breeding area, have shorter breeding periods than medium- and short-distance migrants. Therefore they often raise only one brood, although if this is lost they can in some cases produce a substitute (Berthold, 2001). The adaptations to migration outlined here, in molt and in the reproductive cycle, are also mostly present in captivity and even under constant experimental conditions (Gwinner, 1986; Berthold, 1996). Accordingly, they are substantially controlled by circannual rhythms and hence are most likely inherited, probably even in their details. But beyond the period of juvenile development (Section V.F), very little information is available about the interaction of migration with other annual processes in terms of genetic control. We carried out an experiment in which the annual periodicity of migratory blackcaps from Germany was compared with that of nonmigratory conspecifics from the Cape Verde Islands and of hybrids of the two populations. It turned out that population-specific characteristics such as the two-peaked testis cycle of the African birds and the partial winter molt of the European blackcaps are inherited, whereas the extremely early sexual maturity of African

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blackcaps is under environmental (photoperiodic, i.e., short-day) control (Berthold and Querner, 1993). In some other experiments with European starlings and blackcaps, we found that in the absence of actual spring migration, gonadal development, and breeding occurred earlier than normal and the period of enlarged testes is prolonged. This indicates that migration does indeed have an inhibitory effect on the reproductive cycle (for review see Berthold, 1996).

VI. Quantitative Genetic Analysis A. Mode of Inheritance The first person to devote close attention to the question of whether migratory behavior is inherited was Nice, beginning in 1933. Studying the song sparrow, she constructed genealogies in an attempt to find out whether these partially migratory birds pass migratory activity on to their descendants, as a ‘‘migration instinct.’’ Failing to find any pure strains of migrants or of residents, and instead discovering that parents showing migratory activity can also produce nonmigratory offspring and that nonmigratory parents can also produce migrants, she discarded her original genetic hypothesis for the control of partial migration and concluded that ‘‘the difference between migrating and nonmigrating. . .is not a matter of inheritance’’(Nice, 1937). At that time she had not yet realized that the inheritance of migratory behavior does not conform to simple Mendelian laws but rather those of quantitative genetics. When the genealogies published by Nice were later reanalyzed accordingly (Berthold, 1984), it was clear that migratoriness and sedentariness in the song sparrow are inherited, just as in the blackcap or European robin (Section V.H). In two types of experiments on the blackcap we obtained data about the nature of the inheritance of migratory activity and other parameters of migration. By cross-breeding birds from migratory, partially migratory, and nonmigratory populations (Sections V.B,D,E), we found that the migratory behavior can be genetically transmitted, but in the F1 generation only to a fraction of the offspring. This indicates that migratory activity most likely is a polygenic trait (as would be expected for such a complex behavior), presumably with a threshold (Section VI.C). Migratory behavior is most likely not based on a single-locus system, because then all the F1 hybrids would have been expected to show at least some migratory activity or no activity at all. And migratory activity is also certainly not a simple dominant trait because if it were, all the hybrids descended from migratory individuals should have displayed it.


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Corresponding results were obtained in a second type of experiment— the two-way selection experiment, described in Section V.H. In this experiment we were able to demonstrate that migratoriness (the migratory behavior in the migratory fraction) and sedentariness in an obligate partially migratory blackcap population are inherited and that the partially migratory habit can be converted to exclusive migratoriness or sedentariness just by selection. Because migratory parents also produce nonmigrants before full migratoriness is reached (and nonmigratory parents, migrants), the underlying control mechanism is certainly not a simple genetic dimorphism (polymorphism). It is most likely that migratoriness and sedentariness are threshold characters determined by multiple loci (Section VI.C). In two experiments with blackcaps and in one experiment with redstarts we found that the amount of migratory activity displayed by (migratorily active) hybrids was almost exactly intermediate between the amounts exhibited by the parental populations (Sections V.B, E). It follows that migratory activity is inherited as an additive quantitative, species- or population-specific character. As outlined in Sections V.B and V.D, the population-specific directional preference can be genetically transmitted together with the migratory behavior into the offspring of a nonmigratory population when the parents are cross-bred with individuals of a migratory population. This association between migratory activity and orientation behavior represents a migration syndrome, the genetic integration of which is so far unknown (for more details see Section VI.C). B. Estimation of Heritabilities and Consequences Heritability is a measure of the relative amount of additive genetic variance present in a particular population and is (as so-called narrow sense heritability) one of the central quantitative genetic parameters. The reason for this is that the amount of additive genetic variation is the main determinant of the strength of response to selection, and thus determines the rate of evolutionary change (for details see Falconer and Mackay, 1996; Pulido and Berthold, 2003). In our blackcap studies, we estimated heritabilities of the amount (total for the season), intensity (average amount per night), duration (within a migratory period), time of onset and termination, and incidence of migratory activity. These parameters are represented, together with data from some other studies, in Table I. First, there were no significant differences between heritability estimates derived from offspring-on-mother and offspring-onfather regressions, and therefore it is most likely that resemblances between

TABLE I Heritability Estimates for Migratory Traits* Trait Onset of autumn migratory activity Onset of autumn migratory activity Termination of autumn migratory activity Arrival at wintering site Departure from wintering site Onset of spring migratory activity Arrival at breeding site Arrival at breeding site Amount of autumn migratory activity Amount of autumn migratory activity Amount of autumn migratory activity

Species

Env. Heritability Significance

Method

Source

FSC, POC FSC, POC FSC, POC

Pulido et al. 2001 Pulido and Widmer, unpublished Pulido 1998; Pulido and Berthold, unpublished Rees 1989 Rees 1989 Widmer 1999 Potti 1998 Møller 2001 Biebach 1983 Widmer and Pulido, unpublished Berthold and Pulido 1994, Pulido 1998 Pulido 1998 Nice 1937, Pulido unpublished Berthold et al. 1990; Pulido and Berthold, unpublished Pulido et al. 1996, Pulido and Berthold, unpublished Pulido, unpublished

Sylvia atricapilla Sylvia borin Sylvia atricapilla

l l l

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Cygnus bewickii Cygnus bewickii Sylvia borin Ficedula hypoleuca Hirundo rustica Erithacus rubecula Sylvia borin Sylvia atricapilla

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0.19 0.10 0.67*

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Fig. 4. Results of the prime-probe experiments using eagle shrieks as probe stimuli. (Data from Zuberbu¨hler et al., 1999a; Zuberbu¨hler, 2000a.) Histograms represent the median number of eagle alarm calls (hatched) or leopard alarm calls (solid) given in the first minute after a playback stimulus. Error bars represent the third quartile. The points connected by lines between them represent the median alarm call rate during the five minute period of silence in between two playback stimuli. Using leopard growls as a probe stimulus yielded analogous results.

conspecific Diana monkey male or by a hetero-specific Campbell’s monkey male. Although the alarm calls of the two species differed strongly in their acoustic structure, the priming effects remained the same: The monkeys ceased to respond to a predator if they were previously warned

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of its presence by a semantically corresponding alarm call, regardless of its species’ origin. As outlined earlier, the vocalizations of the two predators are acoustically completely different from the monkey alarm calls, indicating that the monkeys did not simply habituate to a set of acoustic features common to both playback stimuli. These data showed that, although both the acoustic and the semantic properties of the stimuli varied between prime and probe stimuli, only variation in the semantic properties explained the monkeys’ vocal response pattern. Data are consistent with the interpretation that recipients assumed the presence of a particular predator type when hearing conspecific alarm calls and then were not surprised to hear its vocalizations a few minutes later. These primates, in other words, appear to process alarm calls on a conceptualsemantic rather than a perceptual-acoustic level, analogous to earlier findings in vervet monkeys (Cheney and Seyfarth, 1988). B. The Effect of Social and Ecological Knowledge Research by Cheney et al. (1995) showed that free-ranging Chacma baboons (Papio cynocephalus ursinus) took into account social knowledge concerning their group members when responding to other individuals’ vocalizations. In this species, dominance relationships are partially mediated by two kinds of vocalizations, the ‘‘grunts’’ given by a female to lower-ranking group members and the ‘‘fear barks’’ given to higherranking ones. Through the use of a playback experiment, it was possible to show that call sequences that were inconsistent with the social hierarchy— a higher-ranking animal responding with fear barks to a lower-ranking animal’s grunts—elicited stronger responses in recipients than control sequences that were made consistent. A recent experiment with wild Diana monkeys suggested that the ability to respond to vocalizations by taking into account facts about the world and previous events is not limited to the social domain. As mentioned earlier, leopards and chimpanzees prey upon Taı¨ monkeys. These two predators differ in their hunting tactic, and the monkeys use two different anti-predator strategies to defend themselves against them. After detecting a leopard, both male and female Diana monkeys respond by giving loud conspicuous alarm calls that function to warn others and to signal to the predator that it has been detected (Zuberbu¨hler et al., 1997). Forest leopards tend to give up their hiding position and leave the area once they have been discovered by their prey (Zuberbu¨hler et al., 1999b). In contrast, upon detecting a chimpanzee, female Diana monkeys give only a few quiet alarm calls and flee quickly to hide in the canopy, while the adult male of the group does not vocalize at all (Zuberbu¨hler et al., 1997). Taı¨

REFERENTIAL SIGNALLING IN NON-HUMAN PRIMATES

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chimpanzees have sophisticated climbing skills that allow them to hunt cooperatively for monkeys, mainly red colobus (Colobus badius) (Boesch and Boesch, 1989; Boesch, 1994). Chimpanzees capture Diana monkeys less frequently, but individuals are nevertheless exposed to many events of chimpanzee predation because of their high association rates with red colobus monkeys (Wachter et al., 1997). However, the monkeys’ choice of an appropriate anti-predator strategy to chimpanzees is complicated by the fact that chimpanzees themselves occasionally also fall prey to leopards (Boesch, 1991; Zuberbu¨hler and Jenny, 2002). When encountering a leopard, chimpanzees give loud and conspicuous alarm screams. Hearing chimpanzees’ alarm screams therefore not only signals the presence of a group of chimpanzees to Diana monkeys, it additionally signals the presence of a leopard. If the Diana monkeys understand the meaning of the chimpanzee alarm screams, they will be forced to make a decision between two mutually exclusive anti-predator strategies. To investigate whether Diana monkeys understand the meaning of chimpanzee alarm screams, tape recordings of chimpanzees’ social screams, chimpanzee alarm screams, or leopard growls were played back to different monkey groups. Thus, the monkeys were presented with a problem consisting of a cause-effect relation in the biological domain. The monkeys showed consistent differences in their vocal responses to leopards and chimpanzees: both males and females remained silent after hearing chimpanzee social screams but gave loud and conspicuous alarm calls after hearing leopard growls and chimpanzee alarm screams (Fig. 5). Statistical analyses revealed that both adult males and females were significantly more likely to respond with alarm calls to a playback with chimpanzee alarm screams than to chimpanzee social screams (Fisher test, males: p < 0.001; females: p < 0.01, N ¼ 49 groups). Males and females were also significantly more likely to respond with alarm calls to a playback of leopard growls than to chimpanzee alarm screams (Fisher test, males: p < 0.005; females: p < 0.02, N ¼ 47 groups). The latter finding was the result of high variation in responses to playbacks of chimpanzee alarm screams: In the majority of groups of Diana monkeys, both males and females responded by giving their own leopard alarm calls when hearing chimpanzee alarm screams. In some groups, however, individuals adopted a cryptic response after hearing chimpanzees’ alarm screams, thus showing no evidence that they perceived the chimpanzee alarm screams as a sign of leopard presence. A study on territory use of three different chimpanzee communities showed that chimpanzees use a relatively small proportion of their territory as a core area (Herbinger et al., 2001). Diana groups living in the

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Fig. 5. (a) Two types of screams produced by Taı¨ chimpanzees. The left spectrogram depicts a scream given during social interactions (‘‘social scream’’); the right one illustrates a scream given in response to a leopard (‘‘alarm scream’’). (b) Alarm call response of different groups of Diana monkeys to chimpanzee alarm screams compared to chimpanzee social screams and leopard growls. (Data from Zuberbu¨hler, 2000b.)

periphery of a chimpanzee territory were therefore significantly less exposed to encounters with chimpanzees, and because of this, they were significantly less likely to respond with alarm calls than groups living in the core area. A reanalysis of the data yielded a relationship between a group’s likelihood to respond with leopard alarm calls to chimpanzees’ alarm calls and the location of its home range within the large territory of the resident chimpanzee community (Fig. 6).


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100 Male alarm calls Female alarm calls

% Trials

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Location in chimp territory Fig. 6. Relationship between Diana monkey groups’ tendency to respond with leopard alarm calls to chimpanzees’ alarm screams and their location within the resident chimpanzees’ territory. (Data from Zuberbu¨hler 2000b.)

Results so far have suggested that Diana groups living in the periphery of a chimpanzee territory remained silent to chimpanzee alarm screams because they did not understand the calls’ meaning. Recent work concerning harbor seals’ (Phoca vitulina) knowledge of killer whale (Orcinus orca) vocalizations indicates that similar abilities may be common in other mammals (Deecke et al., 2002). To further investigate the predator knowledge hypothesis, a playback experiment was conducted to determine whether Diana monkey groups differed in their tendency to associate chimpanzees’ alarm calls with leopards (Zuberbu¨hler, 2000b). As with the previous one (see Fig. 3), this experiment also included three types of trials: a baseline, a test, and a control condition. In each trial, a Diana monkey group heard two playback stimuli, a prime and a probe, separated by an interval of five minutes of silence. For example, groups first heard chimpanzees’ alarm calls followed after five minutes of silence by the growls of a leopard. Across conditions, prime and probe stimuli varied with respect to their acoustic and referential (semantic) resemblance. In the baseline condition, individuals of different groups were played leopard growls followed after five minutes by playback of the same leopard growls. Male Diana monkeys produced significantly fewer leopard alarm

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calls to the second playback of leopard growls than to the first (Wilcoxon signed-rank, one-tailed; N ¼ 13; z ¼ 3.062; p < 0.003). In the control condition, the monkeys first heard playback of chimpanzee social screams, indicating the presence of chimpanzees, followed by playback of leopard growls, indicating the presence of a leopard. Since both the semantic and the acoustic features differed across the stimuli, individuals did not have the opportunity to predict the presence of a leopard by hearing the chimpanzee screams. As expected, males responded strongly to subsequent leopard growls, suggesting that they were surprised to hear a leopard. Males produced significantly more leopard alarm calls to the probe than to the prime (Wilcoxon signed-rank, one-tailed, N ¼ 15, z ¼ 2.521, p < 0.006). Finally, in the test condition monkeys heard the chimpanzee alarm screams to a leopard, followed by leopard growls. Results suggested that Diana monkeys differed in their understanding of chimpanzee alarm screams: Males who already responded with leopard alarm calls to the prime (‘‘conspicuous males’’) remained largely silent to subsequent leopard growls, resembling the behavior of the animals in the baseline condition. Only one out of the 14 conspicuous males tested (7.1%) responded with alarm calls to this probe stimulus, even though leopard growls are normally highly effective in eliciting male alarm calls. As in the baseline condition, males produced significantly fewer leopard alarm calls to the probe in comparison to the prime (Wilcoxon signed-rank, one-tailed; N ¼ 14; z ¼ 3.219; p < 0.001). When these 14 males’ response to the probe was compared with the 13 males tested in the baseline condition, no statistical difference was found: The number of leopard alarm calls that these males gave in response to leopard growls did not differ from those given by males in the baseline condition (Mann-Whitney U-test, two-tailed; NTEST ¼ 14, NBASELINE ¼ 13; z ¼ 0.578; p > 0.5). These males’ responses to leopard growls did differ, however, from males who have been primed with chimpanzees’ social screams in the control series (Mann-Whitney U-test, two-tailed; NTEST ¼ 14, NCONTROL ¼ 15; z ¼ 2.662; p < 0.008). In contrast, the majority of males (60%; N ¼ 10) who remained silent to the leopard alarm calls (‘‘cryptic males’’), responded with alarm calls to the leopard growls, resembling the males subjected to the control condition in which prime and probe stimuli could not be associated by a semantic link. As in the control condition, males produced significantly more leopard alarm calls to the probe than to the prime (Wilcoxon signedrank, one-tailed, N ¼ 10, z ¼ 2.207, p < 0.02). These males gave significantly more alarm calls in response to leopard growls than males who heard the baseline series (Mann-Whitney U-test, two-tailed; NTEST ¼ 10, NBASELINE ¼ 13; z ¼ 2.407; p < 0.02). Their behavior did

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Alarm call rate

not differ, however, from that of males who were exposed to the control series. In both cases, males responded to the leopard growl probe by giving alarm calls (Mann-Whitney U-test, two-tailed; N T E S T ¼ 10; NCONTROL ¼ 15, z ¼ 0.232; p > 0.8). Figure 7 illustrates these findings. In sum, in some Diana monkey groups, individuals behaved as if they recognized that the chimpanzee alarm screams signaled the presence of a leopard; they responded to chimpanzees’ leopard alarm calls by giving leopard alarm calls themselves, even though chimpanzees normally caused them to behave cryptically. Groups living in the core area of the resident chimpanzee community were more likely to do so than peripheral groups. The prime-probe experiment further showed that these individuals were able to attend to the causal factors underlying the production of chimpanzees’ alarm calls, because priming with both these alarm calls and leopard growls had similar effects on the monkeys’ responses to the probe. 12 10 8 6 4 2 0

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C. The Effect of Causal Information One common feature of the playback experiments discussed so far was the highly specific referential properties of the stimuli used, in which acoustically distinct utterances could be associated with one particular type of predator. Once learned, these relations do not require much flexibility on behalf of the recipient, since the same utterance always refers to the same external event. However, in their natural habitats, monkeys encounter numerous signals that have more vague and ambiguous referents which require them to take into account additional information before being able to respond adaptively (Hauser, 1988; Seyfarth and Cheney, 1990). The predator alarm calls of the ground-dwelling crested guinea fowl (Guttera pulcheri) provide a good example. These birds forage in large groups and, when chased, produce conspicuously loud and rattling sounding alarm calls (Seavy et al., 2001). Chimpanzees do not hunt guinea fowls, but leopards and human poachers may take them. Nevertheless, Diana monkeys respond as if a leopard were present, suggesting that perhaps Diana monkeys give a leopard-type alarm call response to any loud stimulus from the ground. To address this issue, a playback experiment was designed where the monkeys’ responses to recordings of the alarm calls of crested guinea fowls were compared with their responses to alarm calls of the helmeted guinea fowl (Numida meleabris), a closely related species that does not occur in the forest. Results confirmed that Diana monkeys responded to crested guinea fowl alarm calls as if a leopard were present. Recordings of helmeted guinea fowls, however, elicited a response that was fundamentally different and closely resembled the Diana monkeys’ response to human poachers (Fig. 8). As explained before, the histograms illustrate the median vocal response of entire groups, with the exception of the adult male. Leopard alarm calls are typically given by a small number of adult females, while other group members give alert calls. The typical response to humans is to remain silent after giving a small number of contact calls and alert calls following detection. These results are consistent with the idea that Diana monkeys treat guinea fowl alarm calls as indicative of the presence of a leopard, which seems odd given that guinea fowls also give these calls to humans who are chasing them. To test whether Diana monkeys were able to take this fact into account, the following experiment was conducted. Different groups of Diana monkeys were primed either with leopard growls or human speech to simulate the presence of either of these two predators. After a period of five minutes of silence, recordings of guinea fowl alarm calls were played to the monkeys from the same location. If the monkeys were able to link


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Fig. 8. Median vocal responses of Diana monkey groups to recorded predator vocalizations and guinea fowl alarm calls. (Data from Zuberbu¨hler, 2000c.)

the guinea fowl alarm calls to the presence of either of these two predators, the following should be found. First, groups primed with human speech should remain silent to subsequent guinea fowl alarm calls because (a) humans were the likely cause of the birds’ alarm calls and (b) the usual and most adaptive response to humans is to remain silent. Second, groups primed with leopard growls should give alarm calls because (a) the leopard was the likely cause of the birds’ alarm calls and (b) the usual response to leopards is to give alarm calls (Zuberbu¨hler et al., 1999b). Results showed that the priming stimuli affected the way Diana monkeys responded to guinea fowl alarm calls (Fig. 9). When primed with human speech, Diana monkeys remained mostly quiet to subsequent guinea fowl alarm calls, a behavioral pattern that was not found in groups that were primed with leopard growls. This difference did not arise

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Fig. 9. Diana monkey responses to guinea fowl alarm calls and leopard growls after having been primed with either human speech (left) or leopard growls (right). (Data from Zuberbu¨hler, 2000c.)

because human-primed groups behaved cryptically to any subsequent stimulus. When leopard growls were played to human-primed groups, the monkeys responded by giving many alert calls. Monkeys responded with a significantly lower call rate to guinea fowl alarm calls when primed with human speech than after being primed with leopard growls (MannWhitney U-test, two-tailed, NH ¼ 15, NL ¼ 12, z ¼ 2.615, p < 0.009). The number of leopard alarm calls produced, however, did not separate the two groups: In only one out of 15 cases (6.7%) did monkeys (male or females) produce leopard alarm calls to guinea fowl alarm calls after being primed with human speech. Similarly, groups primed with leopard growls produced leopard alarm calls to guinea fowls in only three out of 12 cases (25.0%). No significant differences were found in the number of female leopard alarm calls (z ¼ 1.421, p > 0.1) or male leopard alarm calls (z ¼ 1.584, p > 0.1) to guinea fowl alarm calls between human-primed and leopard-primed groups. This paralleled the behavior of control groups primed and re-tested with leopard growls where females produced leopard alarm calls in only one out of 11 cases (9.1%) to the second leopard playback. In sum, these data suggested that, when responding to guinea fowl alarm calls, the Diana monkeys responded to the most likely cause for why the birds gave the calls, rather than the calls themselves.


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D. The Effect of Syntactic Information Syntax is a crucial and defining feature of language, frequently recruited to distinguish human from non-human communication (e.g., Gleitman et al., 1999, p. 430). Languages consist of a collection of syntactic rules that specify how words and syllables are put together into phrases and sentences. The syntax of a sentence is concerned with its form, as opposed to the semantics, which is concerned with its meaning. Nevertheless, the former affects the later. This fundamental feature of all languages is the source of its creativity, which allows speakers to construct an infinite number of previously unheard messages, or, as it has been put, ‘‘to make infinite use of finite means’’ (von Humboldt, 1836). Animal communication, in contrast, is viewed as event-bound with no comparable evidence for originality or creativity (Ghazanfar and Hauser, 1999). Children learn to extract and apply effortlessly, and without any specific instructions, the syntactic rules of their native language. By simply listening to the speech stream for a period of about two years, they begin to understand and use their native language’s underlying syntactic principles, such as to add the phoneme ‘‘-s’’ to refer to multiple objects. Among the animal studies concerned with combinatorial properties, most have focused on the structural rules that underlie the system, such as the calling system of the chickadees (e.g., Hailman and Ficken, 1987). These authors have argued that the chickadees’ call system qualifies as syntax according to the definition put forward by structural linguists. Although this was an intriguing claim, the analogy is not perfect. For instance, it still remains unclear to what degree call units partaking in call combinations are meaningful to the birds, a crucial feature of human language. Moreover, it remains to be shown whether and how the combinatory rules affect the meaning of an utterance, a crucial function of human syntax. A recent field study suggests that, as recipients, non-human primates possess some of the cognitive capacities required to extract and interpret the meaning from rules present in the natural communication stream (Zuberbu¨hler, 2002b), paralleling recent findings of a captive study (Hauser et al., 2002b). The field study is based on a structural rule present in male Campbell’s monkey alarm calls: In some circumstances male Campbell’s monkeys produce a pair of brief and low-pitched ‘‘boom’’ vocalizations before a series of alarm calls. The boom calls are given in pairs separated by some seconds of silence and typically precede an alarm call series by about 30 seconds. ‘‘Boom’’-introduced alarm call series are given to a number of disturbances, such as a falling tree or large breaking branch, the far-away alarm calls of a neighboring group, or a distant

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predator. Common to these contexts is the lack of immediate danger, unlike when callers are surprised by a close predator. When hearing ‘‘boom’’-introduced Campbell’s alarm calls, Diana monkeys do not respond with their own alarm calls, which contrasts sharply to their vocal response to normal, that is ‘‘boom’’-free, Campbell’s alarm calls (see Fig. 2 and 4). These observations have lead to the hypothesis that the booms selectively affect the meaning of subsequent alarm calls, analogous to a linguistic modifier. To investigate whether this was the case and to determine that monkeys were in fact capable of understanding the semantic changes caused by the presence of ‘‘boom’’ calls, the following playback experiments were conducted. In two baseline conditions, different Diana monkey groups heard a series of five male Campbell’s monkey alarm calls given to a crowned eagle or a leopard. Subjects were expected to respond strongly, such as to give many eagle or leopard alarm calls, as in the previous experiments. In the two test conditions, different Diana monkey groups heard playbacks of the exact same Campbell’s alarm call series, but this time two ‘‘booms’’ were artificially added 25 seconds before the alarm calls. If Diana monkeys understood that the ‘‘booms’’ acted as modifiers to affect the semantic specificity of subsequent alarm calls, then they should give significantly fewer predator-specific alarm calls in the test conditions compared to the baseline conditions. Figure 10 illustrates the experimental design. Results of this experiment replicated the natural observations. Playbacks of Campbell’s eagle alarm calls caused the Diana monkeys to give their own eagle alarm calls, while playbacks of Campbell’s leopard alarm calls caused them to give leopard alarm calls (see Fig. 2). Playback of booms alone did not cause any noticeable change in Diana monkey vocal behavior, but they had a significant effect on how the monkeys responded

Fig. 10. Experimental design of the playback study representing the different playback conditions. (From Zuberbu¨hler, 2002b.)

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to subsequent Campbell’s alarm calls. Figure 11 illustrates the main findings for male Diana monkeys. The response of the females was analogous (Zuberbu¨hler, 2002b). If ‘‘booms’’ preceded playbacks of Campbell’s leopard alarms, subjects no longer responded with leopard alarm calls. There was a significant difference in the number of leopard alarm calls given between cases where ‘‘booms’’ preceded the alarm calls and cases where they did not (males: z ¼ 1.989, p < 0.05; females: z ¼ 2.955, p < 0.004, U-test, two-tailed). An analogous pattern was found if Campbell’s eagle alarm calls were used as playback stimuli. Both the adult male and female Diana monkeys produced their own acoustically distinct eagle alarm calls to this stimulus, but no leopard alarm calls. If ‘‘booms’’ preceded the Campbell’s eagle alarms, however, subjects did not respond with eagle or leopard alarm calls. There was a significant difference between treatments in the number of eagle alarm calls given (males: z ¼ 3.360, p < 0.001; females: z ¼ 2.976, p > 0.003, U-test, two-tailed). If Diana monkey alarm calls were used as playback stimuli instead of Campbell’s alarm calls, then the ‘‘booms’’ of the Campbell’s monkeys no longer had an effect on the Diana monkeys’ alarm call behavior. The booms, in other words, affected the way the Diana monkeys interpreted the meaning of subsequent Campbell’s alarm calls. They seemed to indicate to nearby listeners that whatever message followed about half a minute later did not require any antipredator response. Judging from the Diana monkeys’ response to these

Median Alarm Call Rate

8

12.5 10

6

7.5 4 5 2 2.5 0

0 0 Booms (N=7)

No booms (N=7)

Booms (N=9)

No booms (N=9)

Fig. 11. Median alarm call responses of male Diana monkeys from different groups to the different playback conditions (median call rates þ third quartile during the first minute after beginning of a playback. Black: leopard alarm calls; hatched: eagle alarm calls). (Data from Zuberbu¨hler, 2002b.)

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playback stimuli, therefore, the booms modified the meaning of the subsequent alarm call series and transformed them from highly specific predator labels, requiring immediate anti-predator responses, into more general signals of disturbance that did not require any direct responses. Experimentally adding ‘‘booms’’ before an alarm call series created structurally more complex utterances with different meanings than the alarm calls alone. In sum, recipients were clearly able to adjust to the meaning assigned to a particular call type, and this adjustment was guided by an underlying rule imposed by the booms, which effectively acted as a modifier. But does this qualify as an example of a syntactic rule as psycholinguists would define it? The behavior of the signaler casts doubt on the statement that this syntactic system is really analogous to human syntax: Call production appears to be the product of a rather rigid calling behavior with little flexibility. Syntactic abilities, one might wish to argue at this point, are only present in the heads of the recipients but not in those of the signalers, a point that will be discussed below. Nevertheless, males are able to make accurate judgments of the predatory threat of a situation, and it is this assessment that determines whether or not to initiate an alarm call sequence with a pair of booms. Clearly, more work is required to investigate the acoustic variation and cognitive bases underlying call production in Campbell’s monkeys. How might this communication system have evolved? The previous experiments have clearly shown that male guenon loud calls exhibit all of the properties of classic alarm calls: They advertise perception to predators and warn conspecific recipients about the presence of specific predators (Zuberbu¨hler et al., 1997), suggesting that they have evolved through ordinary natural selection (Maynard-Smith, 1965). However, several lines of evidence (in particular the sexual dimorphism in call structure between adult males and females, the consistent call use in non predatory situations, and some ontogenetic evidence) simultaneously suggest that loud calls have been under additional and significant pressure by sexual selection (Zuberbu¨hler, 2002a). Sexual selection seems to have caused the evolutionary transition from regular monomorphic alarm calls (as they are still to be found in vervet monkeys) to the sexually dimorphic alarm call system of the forest guenons, with males producing structurally distinct ‘‘loud calls.’’ The evolution of this dimorphism may have been driven by sexual selection selectively affecting the calls’ transmission features and by favoring call use to indicate male quality. In the polygynous mating system of the forest guenons, male competition over females is especially fierce. This mating system is notorious for leading to the evolution of conspicuous male traits, such as loud calls. As mentioned before, male Campbell’s


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monkeys utter boom-introduced alarm calls when no immediate antipredator responses are required, apart from increased vigilance. It is conceivable, therefore, that the boom-introduced alarm calls did not primarily evolve as signals to conspecific group members, but that they serve as acoustic long-distance signals to roaming rivals. The male, in other words, might use his highly conspicuous alarm calls to advertise his presence and vigor to other males without causing confusion in conspecific group members. He achieves this by producing booms before producing ordinary alarm calls, allowing eavesdropping recipients to make appropriate semantic decisions, which safeguard them from engaging in unnecessary anti-predator responses.

V. The Mind of the Signaler The previous sections have focused on the cognitive capacities of call recipients and emphasized the many aspects of cognitive flexibility and sophistication involved in call perception. Comparatively less is known about the mechanisms underlying call production, both in terms of call structure and call use. Currently, the available evidence suggests that, as signalers, non-human primates are significantly more limited in their communicative flexibility and creativity than are humans (Tomasello and Zuberbu¨hler, 2002).

A. Call Structure Primates appear to have only limited control over their articulators. A study by Owren et al. (1993) examined the role of environmental effects and acoustic exposure on the ontogeny of call structure. For this purpose, two species of macaques participated in a cross-fostering experiment and it was found that the only measurable effects caused by this manipulation involved some subtle shifts in the acoustic structure and an increase in the frequency of use of calls already in the animals’ repertoires. Related literature suggests that squirrel monkeys produce most call types soon after birth, even if reared in isolation (e.g., Winter et al., 1973; Hammerschmidt et al., 2001). Hybrid gibbons (Hylobates lar x pileatus) produce songs with an intermediate acoustic structure compared to those of the two parent species (e.g., Geissmann, 1984). Finally, only with substantial operant conditioning effort can primates be brought to alter some acoustic features of their vocalizations, such as call duration (Sutton et al., 1973).

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More recent work has suggested, however, that social variables could exert more striking and lasting effects on the acoustic structure of primate calls. For instance, after regrouping, pygmy marmosets (Cebuella pygmaea) have been shown to change the acoustic structure of their ‘‘trill’’ calls (Snowdon and Elowson, 1999) whereas, in cotton-top tamarins, changes in social rank can affect the acoustic structure of food ‘‘chirps’’ (Roush and Snowdon, 1999). Captive chimpanzees have been shown to converge on structurally distinct local pant hoot variants, which has been taken to suggest that they are able to modify the frequency parameters of their calls through learning (Marshall et al., 1999). In natural populations, a number of studies have been able to demonstrate factors that have lasting effects on the acoustic fine structure of vocalizations. For example, rhesus monkeys (Macaca mulatta) can modify the acoustic fine structure of their ‘‘coo’’ calls to some degree because calls within matrilines tend to be more similar than between them (Hauser 1992). Other data suggest populationspecific dialects in saddle-backed tamarins (Saguinus fuscicollis, Hodun et al., 1981) and chimpanzees (e.g., Mitani et al., 1992), although it is difficult to rule out genetic explanations due to assortative mating (Janik and Slater, 1997; 2000). In sum, although much of the early evidence suggested that non-human primates have fixed and immutable calls, more recent studies have shown that a number of aspects of call structure can be modified. The extent of these acoustic changes and the degree of voluntary control that individuals can exert, however, appear to be not nearly as great as described for either bird song or human speech. So where and how do human and non-human primates differ in the control over their vocal tract? Two distinct mechanisms are of interest, the acoustic source and the filter. There is an increasing consensus that the source-filter-theory, originally put forward to explain speech production (Fant, 1960), serves as a useful model for call production in non-human primates (Andrew, 1976; Owren and Bernacki, 1988; Riede and Fitch, 1999). The theory posits that vocalizations are produced in the larynx by the vocal folds (the source) and subsequently shaped by the cavities of the vocal tract (the filter). Air pressure from the lungs drives the vocal folds of the larynx, the glottis, into rapid mechanical oscillations. The oscillating vocal folds modulate the airflow through the glottal opening, the airspace between the vocal folds. The fundamental frequency of the call is a consequence of the periodicity of the vibration, which is determined by the size of the vocal folds, the amount of air pressure produced by the lungs, and the amount of tension exerted on the vocal folds. The sound generated at the glottal source then passes through the supra-laryngeal vocal tract. Like any tube of air, the air column contained in the vocal tract has resonant nodes, which selectively allow certain frequencies of the glottal


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source signal to pass and radiate out through the mouth or nostrils. The vocal tract hence acts as a bank of band-pass filters, each of which allows a narrow range of frequencies to pass. The vocal tract resonances, along with the spectral peaks they produce in the vocal signal, have been termed ‘‘formants.’’ Originally, the term was used to describe speech signals (e.g., Fant, 1960; Titze, 1994) but various researchers have subsequently used it to describe some animal sounds (Lieberman et al., 1969; Nowicki, 1987; Owren and Bernacki, 1988; Riede and Fitch, 1999). It is a common assumption that, in contrast to human speech sounds, acoustic variation in animal calls is mainly created at the level of the glottal source with little subsequent filtering. In vervet monkeys and rhesus macaques, changes in the fundamental frequency seem to delineate bouts of communication rather than determine the acoustic structure of individual call types (Hauser and Fowler, 1991). A recent study has examined the role of the fundamental frequency in conveying referential information in Diana monkey alarm calls (Riede and Zuberbu¨hler, 2003a). Male Diana monkey alarm calls are remarkably low pitched (fundamental frequency 33 to 120 Hz), comparable to the human pulse register (fundamental frequency 10 to 90 Hz; Henton and Bladon, 1988), which is beneath the modal register of normal speech (Blomgren et al., 1998). Acoustic analyses revealed that non-linear phenomena were virtually absent in male Diana monkey vocalizations and pulses were not interrupted by any other vibration modes of the vocal folds. The pulsed phonation in male Diana monkey alarm calls, therefore, appeared to be a special adaptation to deliver a robust source broadband signal for subsequent vocal tract filtering, but the source characteristics themselves were not carriers of referential information. The second mechanism of interest concerns the supra-laryngeal filtering responsible for the formant structures that define speech sounds. Unequivocal identification of vocal tract filtering requires an analysis technique that separates the effect of the glottal source from that of the vocal tract (e.g., Owren and Bernacki, 1998). A common view is that nonhuman primates are quite limited in the number of sounds they can produce due to their relatively short supra-laryngeal vocal tract and unsophisticated articulators, particularly a tongue with restricted motility (Negus, 1949; Lieberman et al., 1969). Nevertheless, limited articulation has been described, at least in some species. In rhesus monkeys, for instance, the tongue, the lips, and the mandibles have been shown to act as articulators of social calls as their various configurations determine the filtering properties of the vocal tract (Hauser et al., 1993). Other studies have similarly suggested that some nonhuman species are capable of vocal tract filtering by controlling the resonance properties independently of the

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glottal source (Hauser and Scho¨n-Ybarra, 1994; Fitch and Reby, 2001; Rendall et al., 1999). Rhesus macaque coo calls and grunts are the effects of vocal tract filtering, but these calls are more likely to be related to individual differences than to external events (Rendall et al., 1998). Vocal tract filtering appears to play a crucial role in labeling external events in primate alarm calls. A recent study has shown that the spectral peaks in Diana monkey leopard and eagle alarm calls can be considered as formants (Riede and Zuberbu¨hler, 2003b). The two alarm call types differed most prominently in the downward modulation of the first formant at the beginning of each syllable, with leopard alarm calls exhibiting a downward modulation that was three-fold stronger than eagle alarm calls. The strength of downward modulation was very consistent and differentiated the two alarm calls unambiguously, providing evidence that non-human primates rely on the formant modulations to convey information about external events. The study corroborated earlier findings by Owren (1990a), which showed that when both the fundamental and the formant frequency of vervet monkey alarm calls were artificially manipulated, only manipulation of the latter disrupted the monkeys’ ability to discriminate between the various calls (Owren, 1990a,b). In sum, these studies suggest that non-human primates are able to utilize vocal tract changes to encode important events in the environment, a defining feature of human speech production. B. Call Use As with call structure, call use seems to be subject to rather limited flexibility. Many primate calls appear to be used in adult-like contexts from early in ontogeny, with a subsequent learning phase in which this is fine-tuned (Seyfarth and Cheney, 1997). For example, infant vervet monkeys give eagle alarm calls to various moving things in the sky or they produce calls that experienced adults only produce when seeing a neighboring group whenever they are distressed (Cheney and Seyfarth, 1990). Only later do they confine call use to the appropriate, adult-like contexts (Hauser, 1989). Similarly, young pigtail macaques (Macaca nemestrina) are less precise when using agonistic screams than are adults (Gouzoules and Gouzoules, 1989). Flexibility of use persists to some degree in adults. For example, in cotton-top tamarins, social and reproductive status affects call use (Roush and Snowdon, 2000), and Japanese macaques show population-level differences in their use of food and contact calls (Green, 1975; Sakura, 1989). It is therefore of relevance what kinds of mental processes underlie call production. The vocal behavior of a number of non-primate species


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suggests that non-categorical labeling of predators may be widespread in animal communication. California ground squirrels, Spermophilus beecheyi, for example, give ‘‘whistles’’ to raptors and ‘‘chatter-chat’’ alarms to terrestrial predators (Owings and Virginia, 1978; Owings and Leger, 1980), but these calls are not labels for raptors and terrestrial predators. Instead, the squirrels give ‘‘whistles’’ whenever a predator arrives suddenly and a response is urgent. Similarly, ‘‘chatter-chat’’ alarms are given to predators spotted at a distance. Typically, such predators are mammalian carnivores but squirrels have been observed to give ‘‘chatter-chat’’ alarms to a distant hawk (Leger et al., 1980). Domestic chickens, Gallus gallus domesticus, provide another interesting example. In this species, males give aerial and ground predator alarm calls (Gyger et al., 1987), but individuals give ground alarm calls to many objects moving on the substrate and aerial alarm calls to many objects moving above in free space, regardless of whether or not they are predators (Gyger et al., 1987), suggesting that chickens do not respond to the predator category but instead to the spatial characteristics of the threat. These examples suggest that monkeys might not denote the ‘‘categorical’’ features of a predator when giving alarm calls. To investigate which aspects the monkeys responded to when giving alarm calls, the presence of a predator was simulated in various ways (Zuberbu¨hler, 2000d). A playback speaker was positioned in the vicinity of Diana monkey groups, such that (a) the distance to the group was either ‘‘close’’ or ‘‘far’’ (about 25 or 75 m), (b) the elevation of the speaker was either ‘‘below’’ or ‘‘above’’ the group (about 2 or 30 m off the ground), (c) the predator was either a ‘‘leopard’’ or an ‘‘eagle’’ (15s playback of leopard growls or eagle shrieks). Results of both male and female alarm call behavior to these variations clearly showed that Diana monkeys consistently responded to predator type, regardless of distance or direction of predator attack (Fig. 12). This experiment was later replicated with Campbell’s monkeys, with comparable results; the predator type was the main determinant of alarm calling behavior rather than the degree of threat (Zuberbu¨hler, 2001). Although results suggest that these primates respond to predator class when giving alarm calls, it could be that this experiment did not examine the crucial range. For instance, the monkeys’ perception of threat by a leopard might differ little between cases whether the predator was 25 or 75 m away. Although this concern is valid, the experiment clearly showed that the variable predator class overwhelmingly affected the acoustic structure of the monkey alarm calls. If the degree of threat had been the main determining variable, it is not clear why the variable predator class exerted such strong effects on the acoustic structure of the monkey alarm calls.

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(a)

(b) 70.0 Median call rate (calls per min)

Median call rate (calls per min)

70.0 60.0 50.0 40.0 30.0 20.0 10.0

60.0 50.0 40.0 30.0 20.0 10.0 0.0

0.0 Leopard close (N=6)

Eagle close (N=6)

Leopard far (N=6)

Leopard below (N=5)

Eagle far (N=5)

Eagle below Leopard (N=5) above (N=7) Playback stimulus

Playback stimulus Eagle alarm

Eagle above (N=7)

Leopard alarm

Alert call

Contact call

Other call

Fig. 12. Diana monkey responses to playbacks of predator vocalizations presented with varying degrees of threat: (a) distance, (b) direction of attack. (Data from Zuberbu¨hler, 2000d.)

C. Audience Effects An especially important type of flexibility in call production concerns audience effects, in which an individual uses its vocal signals differently depending on the social-communicative situation. Positive evidence would suggest that individuals are able to adjust the use of a signal according to a momentary assessment of how it might affect potential recipients. Audience effects can go in either direction (e.g., by honestly advertising the presence of important events to relatives or mates) or by deceptively suppressing calls in the presence of competitors. Although the overall evidence for audience effects is rather weak, a number of studies show that primates can adjust call use to some degree. For example, red-bellied tamarins (Saguinus labiatus) produce specific calls when they discover food, but rates depend on whether or not other group members are present (Caine et al., 1995). Male chimpanzees produce pant hoots more frequently in traveling contexts when their alliance partners are nearby (Mitani and Nishida, 1993). Vervet monkey females adjust the rate of alarm calling depending on whether their own offspring are present, while males call more in the presence of females than males (Cheney and Seyfarth, 1985). However, there is also important negative evidence. Cotton-top tamarins give more food-associated calls when in closer proximity to other group members, but individuals call at an equal rate regardless of whether or not their mates were visible, suggesting that calling is not effected by audience (Roush and Snowdon, 2000). Macaque females do not attempt to alert ignorant offspring more than knowledgeable ones when shown a predator, suggesting that audience effects may not be the result of callers assessing the knowledge of recipients (Cheney and Seyfarth, 1990).


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D. Gestural Communication Primates communicate with gestures in non-urgent everyday social situations, as recently reviewed by Tomasello and Zuberbu¨hler (2002). Unlike vocal signals, however, there is good evidence that primates invent new and idiosyncratic gestural signals (Goodall, 1986; Tomasello et al., 1985; Tanner and Byrne, 1993, 1996). The use of gestural signals is learned via a process called ontogenetic ritualization, in which two organisms shape one another’s behavior over time (Tomasello, 1996). Behaviors that may not have been communicative at first can become gestural signals. Gestures can be used in multiple contexts, sometimes across widely divergent behavioral domains. The current empirical record seems to suggest that gestural signals are an important mode of communication in great apes, showing higher degrees of flexible use than vocal signals. For instance, young chimpanzees only produce gestures to solicit play when the recipient is already oriented appropriately, and produce attention-getting gestures most often when the recipient is socially engaged with others (Tomasello et al., 1994, 1997). Tanner and Byrne (1993) reported that a female gorilla repeatedly used her hands to hide her play face from a potential partner, indicating an understanding of the role of visual attention and flexible control of an otherwise involuntary grimace. However, despite these examples of flexible and sophisticated use, there is no evidence to suggest that primate gestures are referential in the sense that they indicate an external entity. Despite this conspicuous lack, ape gestural communication is frequently cited to support the idea that human language has evolved from a gestural system (e.g., Corballis, 1999).

VI. Communication and Social Intelligence Primate communication involves mental representation. The evidence is strongest in the referential vocalizations used by some monkey species, but similar processes might be at work in ape vocal communication (Crockford and Boesch, 2003). As recipients, primates have revealed a highly sophisticated understanding of the semantic content associated with some of their calls involving appreciation of the referential situation. This may include information on the external event that the caller has just witnessed and the possible causal reasons of calling, rather than a simple working knowledge on how best to respond to a particular call. Primates appear to understand vocal signals as outcomes of specific external events. Despite this remarkable flexibility in call comprehension, the evidence for flexibility during call production is unimpressive. To data there is no

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evidence that primates are able to invent and incorporate new vocalizations into their repertoires or to combine calls creatively to produce novel meanings. Ape gestures may be something of an exception. There are a number of possible hypotheses for the difference in cognitive performance between signalers and recipients. One has to do with lack of neural control over the articulators. Although primates seem to possess sophisticated comprehension capacities, they appear to be limited by a rather unsophisticated neural control of their articulators, which in turn could impede the evolution of more complex cortical circuitry required for flexible signaling. Another hypothesis stresses the limitations in social cognition. Primates have been remarkably resistant to providing evidence of being able to perceive others as mental agents whose behavior is driven by beliefs, desires, and knowledge (Tomasello and Call, 1997, p. 384; Cheney and Seyfarth, 1998). Primates’ ability to take into account other minds might be limited to assessment of each other’s visual perspective during competitive interactions (Hare et al., 2000, 2001, 2003), but this may not be based on assessing each other’s mental states. Primates, in other words, may not interpret each other’s behavior as the outcome of invisible psychological forces, such as ignorance, malignance, or fear. Rather, they possess a good working knowledge of others as animate and separate beings with their own behavior which can be manipulated with communicative signals; however, they do not seem to understand each other as intentional beings (Visalberghi and Tomasello, 1998). If they cannot discern their own intentions from those of a conspecific, primates will be prevented from understanding behavior as the product of intentions and are left to perceive the world at the level of individually learned stimulus-response associations. They will never really be able to come to a sense of intention or psychological causality that so forcefully governs the human mind. Mind-blindness of this sort is likely to have impeded the evolution of more sophisticated communication in situations that go beyond evolutionarily urgent events. This cognitive limitation could have prevented the evolution of mechanisms allowing use of vocalizations in an intentional way in order to affect each other’s knowledge, a hallmark of human communication. A recent review of state-of-the-art research in the neural systems underlying the theory-of-mind in humans is particularly interesting (Siegal and Varley, 2002). The authors review the evidence on whether the brain regions dedicated to language are part of the theory-of-mind core system and they conclude that this is not the case. For example, in an aphasic individual theory-of-mind reasoning was retained despite significant damage to left-hemisphere language centers leading to profound impairments in syntactic abilities (Varley and Siegal, 2000). Although seemingly


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independent, the two systems might still interact with each other. However, linguistic experience does not seem to be essential to triggering the development of theory-of-mind abilities. Children with specific language impairments perform theory-of-mind tasks the same way as normal children (Perner et al., 1989), while syntactic competence does not predict success in theory-of-mind tasks. In sum, linguistic capacities and social cognition appear to be part of separately evolved cognitive systems. According to this scenario, then, the ability to perceive mental states in others evolved first in the primate lineage, as evidenced by the capacity of some apes to solve simplified tasks of assessing other individual’s knowledge (Hare et al., 2001). Once in place, the system might have created selection pressure on individuals to evolve a communicative system to exploit these newly evolved social abilities, leading to an open-ended system capable of inventing novel signs through lawful combinations of a relatively small number of phonemes. If this is how it happened, then the primate evidence suggests that these people would have found it exceedingly easy to comprehend their newly found vocal expressive capacities.

VII. Summary Recent evidence suggests that our hominid ancestors did not have speech until very recently, indicating that many of the cognitive skills required for linguistic competence must have been present in the primate lineage long before the advent of language. These pre-adaptations might have evolved to function in communication as part of a general social or ecological intelligence, or as mere byproducts of other traits, calling for an empirical investigation of the functional significance of these abilities. The natural referential and combinatorial capacities in extant primates in their natural habitats are of particular interest. The empirical evidence reviewed in this chapter suggests that various cognitive capacities required for understanding language, including the ability to take into account semantic, syntactic, and pragmatic cues, are present in non-human primates. As signalers, however, non-human primates are curiously limited, showing little evidence of cognitive flexibility and creativity. These expressive limitations seem to be rooted in at least two deficiencies: a lack of sophisticated control over the articulators in the supra-laryngeal vocal tract and a remarkable shortcoming in social cognition. Non-human primates have consistently failed to show evidence of perceiving others as beings that possess mental states, such as beliefs or desires, suggesting that mind-blindness has impeded the evolution of sophisticated communication in situations that go beyond evolutionarily urgent events.

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Acknowledgments Field research was made possible by grants of the Universities of Pennsylvania and Zurich, the U.S. National Science Foundation, the National Geographic Society, the Swiss National Science Foundation, the European Science Foundation, and the British Academy. Much of the reviewed evidence has been conducted as part of the Taı¨ Monkey Project, which was funded by the University of Zurich, the Max-Planck-Society, and grants of the Leakey foundation and Conservation International. I am thankful to Peter Slater, Tim Roper, Chuck Snowdon, Robert Seyfarth, Julia Fischer, Vincent Janik, and Tobias Riede for their comments.

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Vocal Self-stimulation: From the Ring Dove Story to Emotion-Based Vocal Communication Mei-Fang Cheng biopsychology program department of psychology rutgers university newark, new jersey

I. Introduction The nest coo, a two-note song (Smith, 1991; Baptista, 1996), is a repetitive vocal courtship display of the ring dove (Streptopelia risoria). Although the nest coo is arguably among the simplest songs uttered by birds, the twosyllable notes form a socially communicative message that shares the many attributes for which animal vocal sounds are selected. To me, the female nest coo is warm and seductive. The male ring dove ‘‘understands’’ the message of the nest coo and wastes no time in pursuing copulatory behavior. Can a male safely take the female nest coo as a message of the female’s commitment to mating and reproduction? What is the referent of the female nest coo? No one would dare suggest that the male dove brain has a cognitive representation of the female nest coo because doves have only very modestly differentiated telencephalic structures (the hemispheres that undergo the greatest growth during development). How then can we satisfactorily account for male dove response behavior? These were not among the questions I asked when I began studying the dove’s courtship display. As it turns out, the communicative significance of the female nest coo is embedded in a mechanism which I have designated as a vocal-auditory-endocrine feedback system (vocal self-stimulation, in short). The mechanism begins when female doves vocalize (coo) in response to male courtship. Then the feedback from the female’s own cooing triggers her endocrine changes, culminating in egg-laying. In this chapter, I will chronologically review data that led to the finding of this vocal-auditory-endocrine mechanism and the identification of the neurons in the hypothalamus that recognize the female nest coo and translate the acoustic signal into an endocrine response. The point of the chronological 309 Copyright 2003 Elsevier Inc. All rights reserved. 0065-3454/03 $35.00

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presentation is to convey the serendipitous nature of these findings. Next, I will discuss how the vocal self-stimulation system may contribute to the overall scheme of vocal communication. In this way, I use dove vocalizations as the platform from which to propose a theory on the role of emotions1 in vocal communication. In the field of animal behavior, the 1960’s were marked by a surge in studies on the neural and hormonal bases of reproductive behavior. The Institute of Animal Behavior, founded by the late Daniel S. Lehrman, was a center for the study of the interrelationships between the brain, hormones, and behavior. By the time I joined the Institute, Lehrman and his colleagues had already developed an overarching working hypothesis about brain, hormone, and behavior relationships. One critical finding from this era is that successful reproduction is a culmination of a complex interplay of male-female behaviors mediated and coordinated by hormonal action on the brain. For example, during courtship, a male dove typically initiates nest cooing and is later joined by female nest cooing. This behavioral transition is thought to be mediated by hormones; the combination of the sight of a female and rising testosterone stimulates a male to first exhibit aggressive bow cooing, which repels the female, and then some time later, nest cooing. In response to nest cooing, the female joins the male nest cooing, infrequently at first but then becomes more and more steady. Eventually the male ceases nest cooing and the female bear a performer. In a laboratory setting about three to five days after the female’s first coo utterance, a clutch of two eggs was laid (Fig. 1). According to Lehrman (1961), male courtship is the cause of a female endocrine response that culminates in egg laying. As we will demonstrate, however, the optimal stimuli for female endocrine change are not male signals, but signals by the female herself. This small but crucial twist the highlights the centrality of endocrine changes in vocal communication.

II. Early Fascination with the Female Nest coo: Tinkering with the Neural Substrate Among Lehrman’s colleagues and students, myself included, a preoccupation with neuroendocrine factors may have distracted us from considering the communicative aspects of behavioral interactions. My 1 ‘‘Danger’’ or life-threatening situations evoke the autonomic and endocrine response we experience as emotion. Numerous studies in humans suggest that physiological indices are a more reliable indicator of emotion than subjective reports. Animals in ‘‘danger’’ manifest similar autonomic and endocrine responses. I use the term ‘‘emotion’’ to refer to these —page 2.

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Fig. 1. The male nest coo, the female nest coo, and follicular growth during a breeding cycle. A schematic representation of the rate of follicular growth (the diameter of the largest follicle) in relation to the rate of male and female nest cooing during a normal breeding cycle. Note that (1) the rate of the male nest coo falls as that of the female nest coo rises, and (2) the follicle increases in size gradually until reaching a threshold point after which it grows exponentially. (From Cheng, 1993.)

earlier work with ring doves was systematicly delineating the role of female hormones throughout the normal breeding cycle. The central questions were: What hormones are involved in behavioral change and how do hormonal actions translate into the behavioral changes that take place during the breeding cycle? Since the role of testosterone in male courtship behavior had been widely studied, I gladly took on the task of exploring the role of ovarian hormones in female behavior. In the 1979 issue of Advances, I summarized the work on the roles of testosterone and ovarian hormones (estrogen and progesterone) in the male and female ring dove during the breeding cycle. At that point, we had already identified the causal relationship between gonadal hormones and courtship behavior; we were in a position to determine where in the brain hormones act to yield behavior. We established that the presence of estrogen in the system is necessary for nest coo display in the female as well as the male, in the latter through the conversion of testosterone into estrogen (Cheng, 1979). As a result, we believed there to be an interrelation between the reproductive neuroendocrine system and behavioral changes. Figure 2 shows the hypothalamus-pituitary-ovarian system that mediates the development of the ovarian follicles that culminate in ovulation and egg

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Fig. 2. Male courtship, female nest coo, and female follicular growth. The left panel depicts the relationship between the female nest coo and follicular growth in the original and modified versions. In both cases, the follicular growth is the end product of a cascade effect of the hypothalamus-anterior pituitary-ovarian (H-P-O) system. The mature follicle in turn secrets estrogen and progesterone. The original idea assumes that male courtship triggers the H-P-O system, whereas the modified version proposes that the female’s own nest coo provides feedback to trigger the H-P-O system. GnRH—gonadotrophin releasing-hormone; LH— luteinizing hormone; FSH—follicle-stimulating hormone.

laying. The hypothalamus controls the output of endocrine secretions through several systems, including the hypothalamus-anterior pituitaryovarian system. Also, the hypothalamus receives sensory information from other parts of the brains allowing environmental stimuli to influence its activity, the so-called extra-hypothalamic control of endocrine activity. Therefore it was clear that the hypothalamus plays a critical role in the effect of endocrine changes on behavior as well as in the effect of environmental stimuli on endocrine changes. Thus our task was to illustrate how behavioral and endocrine events interact to engineer behavioral and endocrine changes. With the advent of brain mapping of estrogen binding sites, it was possible to ask where in the brain estrogen acts to induce the female nest coo. While estrogen concentrations are found in many regions of the female brain, the concentration of estrogen in the midbrain, particularly in the medial nucleus intercolliculari (mICo), is most intriguing. We found that a female that sustained bilateral electrolytic lesions in the mICo was unresponsive to male nest coos. That is, the female did not nest coo during a protracted period of courtship (Cohen and Cheng, 1981). Except for the


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lack of the nest coo in her behavioral repertoire, the female was normal in all other respects. Since ICo sends projections to motor neurons regulating sound production (Nottebohm et al., 1976), the results affirmed the role of ICo in the production of the female nest coo. Given that the female nest coo is estrogen dependent, that is, the performance of the female nest coo is contingent on the availability of estrogen in her system, the finding that mICo of the female ring dove contains estrogen binding sites (MartinezVargas et al., 1975) strongly suggests that estrogen acts at the mICo to produce nest coos. Unexpectedly, we also noted that females with mICo lesions failed to lay eggs despite the male’s increased level of nest-cooing, presumably because of the lack of a female response in the form of a nest coo. This suggested a critical role for the female’s own nest coo in her endocrine changes. This observation is not at all incongruent with the concept that male courtship alone is sufficient to bring about a female’s endocrine commitment and breeding success. In Lehrman’s scheme, the female nest coo was thought to serve as a signal for the male to move on to the next phase, nest building, and it was thought that nest coo behavior and endocrine changes are parallel events (Fig. 2). Determining the precise ‘‘message’’ or ‘‘meaning’’ of the female nest coo was not a primary focus of our research. Instead, we spent the next few years determining whether or not the female nest coo was linked to endocrine changes and how the endocrine changes culminated in egg laying. Precisely what are the functions of the female nest coo?

III. Search for Female Vocal-Endocrine Links: Feedback Mechanisms A. Behavioral Studies To address this question, we launched a series of studies to establish first and foremost that the ‘‘no female nest cooing ¼ no egg laying’’ observations were not a fluke. Devocalization of the female by alternative means, such as severing the hypoglossal nerves that control the syrinx, produced essentially the same results (Cohen and Cheng, 1979). Therefore it appeared that there was a causal relationship between the female’s nest coos and her own endocrine changes. This was a major departure from the widely accepted view that male courtship directly activated the female’s reproductive endocrine responses. We proposed that one way in which the female nest coo could impact endocrine responses was through an acoustic feedback system. The

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acoustic output of the female nest coo was presumably processed by the female’s auditory system and then somehow transmitted to the hypothalamus where the acoustic signal was translated into an endocrine response. Using playback studies, we first established the nature of the acoustic feedback using a reversible devocalizing method to impair the female dove’s ability to coo. Female doves were peripherally devocalized by insertion of polyethlene tubing into the interclavicular sac immediately surrounding the syrinx. With the ends of the tubing open, the interclavicular sac was no longer inflated to provide air for vocalization. These female doves were exposed to five consecutive days of playback of one of several prerecorded sound tapes. Females hearing their own coos or other females’ coos showed significant follicular growth, developed in response to luteinizing hormone (LH) and follicle-stimulating hormone (FSH) secreted from the anterior pituitary (see Fig. 2). However, follicular growth in response to the male nest coo was negligible (Cheng, 1986). The difference between the male nest coo and the female nest coo is indistinguishable to the human ear except that the male nest coo is usually louder. Spectral analysis, however, showed that the female coos contained a greater proportion of their total energy in the harmonics than in the fundamental frequency (Durand and Cheng, unpublished). These findings suggested that the female nest coo is an obligatory factor for follicular development. Does this mean that the male courtship nest coo is an evolutionary vestige? In fact, receiving the male nest coo in playback is more potent than the playback of female nest coo in stimulating follicular growth when played to an intact female. Figure 3 shows the results of both playback studies. Although seemingly paradoxical, this finding can be readily explained since an intact female produces her own coos instead of passively receiving the coos played back to her. An intact female coos significantly more to the playback of male nest coos than to the playback of female nest coos; indeed she coos most when courted by an actual male. In the latter situation, the female not only hears male vocalization but also receives visual and tactile stimulation, the full spectrum of courtship stimulation (Cheng et al., 1988). Also, proprioceptive feedback associated with the performance of female nest coos could play a role in activating the female’s endocrine response. Next we found that deafening ‘‘permanently’’ impairs the ability of some females to nest coo and hence their ability to breed normally. In other females, it delays the onset of the female nest coo, thereby delaying breeding efficiency as well (Cheng et al., 1988). These findings suggested that proprioceptive feedback associated with performance of the coo which involves a head-down posture as well as vocalization might play a role in the endocrine response. We hypothesized that convergent input

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Fig. 3. Effects of coo stimulation on follicular growth: playback studies. (Top) Playback of female nest coos to devocalized female in sound isolation chamber in the presence of the male facilitates follicular growth. This is not the case with the male nest coo. (Bottom) Playback of male nest coos facilitates follicular growth more than playback of female nest coos. (From Cheng, 1986; Cheng et al., 1988.)

from the proprioceptive- and audio-feedback may greatly amplify the signal input to the hypothalamus. This could be why a female’s own cooing was more effective than listening to audio playback in rendering an endocrine response (Cheng, 1992). B. Neurophysiological Validation of Behavioral Findings To some critics, however, this was merely an academic exercise. This skepticism was not without scientific grounds. At the time, there were no known pathways that connected coo-producing nuclei in the midbrain with auditory relays in the thalamus or secretory neurons in the hypothalamus. Fortunately, advances in neuroanatomical tracing techniques have made it possible to tackle this problem directly. The neuroanatomical tract tracing method makes use of the fact that a neuron regularly sends material forward to (anterograde) and receives material back from (retrograde) the terminal of its axon. When anterograde tracers are infused into a particular region of the brain, cell bodies in the region will absorb the tracers and transport them to the terminals of the impregnated cells. Through visualization of the path of transport from the cell body to its terminal, one can trace the projection pathway of a particular region.

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Retrograde tracers such as fluorogold are taken up by the terminal of an axon and transported back to the cell body, which becomes filled with fluorogold. A projection from a region A to B is thought to be validated only when an anterograde tracing is confirmed by a retrograde tracing. We infused anterograde tracers (PHAL, dextran) into the midbrain vocal control nucleus, the mICo, and found projections from the mICo to the Ov shell, to the preoptic (POA), and to the anterior medial hypothalamus (AMH) (Cheng and Zuo, 1994). Similar infusions into the thalamic auditory relay, the nucleus ovoidalis (Ov), or its shell region (Ov shell), reveal, with the confirmation of retrograde labels, the existence of projections from the Ov shell to the POA-AMH area and to the ventromedial nucleus (VMN) of the hypothalamus (Durand et al., 1992). The acoustic nature of the connections between the Ov shell and the anterior and ventromedial hypothalamus was subsequently verified using electrophysiological antidromic methods (Cheng and Peng, 1997). We searched for units in the Ov shell that responded to sounds and then stimulated the hypothalamus with electrical pulses. Collisions of action potentials travelling down from the Ov or the Ov shell neurons with those originating from the stimulated hypothalamus suggested that both were travelling along the same pathways. That is, the acoustic stimuli processed in the Ov shell units traveled to the hypothalamus through the Ov shell-hypothalamus pathways. In this way, we identified the neuroanatomical pathways that we believed to be involved with the effects of the coo on the hypothalamus. Still, we were left with the question of whether or not acoustic signals arriving at the hypothalamus had any bearing on the secretion of gonadotrophin releasinghormones (GnRH) which stimulate the pituitary to release luteinizing hormone (LH) and follicle-stimulating hormone (FSH), and activate female endocrine reproductive responses (see Fig. 2). To validate the concept of vocal self-stimulation, rigorous experimentation was essential. We needed to demonstrate that the coo signal is indeed processed in the hypothalamus and that neural activities in these units result in measurable pituitary output. Instead of three separate studies, using playback (birds hearing naturalistic coo), electrophysiological recording (on-going neuronal firing pattern), and an assay endocrine changes (monitoring pituitary hormonal output), we conducted a single study comprising of all these components so that we could witness in real time that when a female hears her nest coo, acoustic units in her hypothalamus show excitation which results in an elevated pituitary hormone output. With the exceptional skills of Dr. Peng who was visiting my lab from China at the time, we conducted the following study. We recorded neuronal activity from the discrete nucleus of the hypothalamus (POA, AMH, and VMN) that receives acoustic inputs


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from the Ov shell region. While sound stimulation and single cell recording were in progress, blood samples were collected from the pituitary veins at 10 to 20 min intervals for a duration of 120 min. This procedure involved exposing the pituitary gland and ventral diencephalons by freeing the bird from the recording position. The blood samples were immediately centrifuged, shipped, and assayed independently by Dr. Johnson at Cornell. We monitored the pituitary level of LH rather than the circulation level of LH because we suspected that the pituitary content was much higher than the systemic level and, as a result, we would be more likely to detect fluctuations. The sound stimulation consisted of female nest coos, reversed female nest coos, male nest coos, reversed male nest coos, and white noise. These sounds were recorded from 16 different individuals using a Marantz stereo cassette tape recorder. Analog recordings of the nest coos were digitized and displayed spectrographically on the computer screen. All vocalizations were standardized to an intercall interval of 2 sec and to a maximum amplitude of 752 dB sound pressure level. Sounds were delivered through a Sony earphone within a cone-shaped box connected to the hollow ear bars. Different sounds were presented in random sequences and repeated 10 to 20 times. Figure 4 outlines the relationship of different components in the experiment. We recorded from a total of 935 units in 36 birds. We found excitatory and inhibitory units in response to coo stimulations. Coo units respond only to coos. Some units are specific to the female nest coo, some specific to the male nest coo, and some respond to both coos but prefer one type of coo. Figure 5 shows a female-nest-coo-specific unit in the preoptic area that responds specifically to the female nest coo in that it shows no response to reversed female nest coo, male nest coo, or white noise. Such female nest coo responsive units are mostly found in POA and AMH and represent only 20 to 24% of units recorded. Recordings from when the female was at rest showed that the female-nest coo-specific neurons were predominantly silent when not stimulated. Most intriguingly, we found that the discharge pattern of the female-nest-coo-specific units often displayed the two-note features of the coo (see Fig. 4b). To our knowledge, this is the first compelling demonstration of acoustic units in the hypothalamus that respond to species-specific vocal signals. As to the LH output in response to various acoustic stimulation, we found that LH concentration in the pituitary vein area was significantly elevated in doves hearing species-typical coos but not in doves exposed to experimentally altered coos (such as reversed nest coos), or to white noise, nor in doves that received no vocal stimulation. Stimulation with female nest coos triggered three times more LH release than stimulation from a

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Demonstrated Endocrine Response to Vocal Self-Stimulation Oscilloscope

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Fig. 4. Demonstrated endocrine response to vocal self-stimulation. A diagram depicting the various parts (auditory stimulation, recording, and blood sampling) of the experimental procedure employed in one on-line experimental setup. Before neural recording, tapes of various coo signals including female nest coos were prepared from breeding pairs. Recording electrodes were placed in the pre-optic hypothalamic regions of female ring doves. Units that burst in response to the nest coo signal were monitored by the oscilloscope, the data stored and analyzed. While recording and auditory stimulation were occurring, blood samples were drawn from the pituitary veins, then stored and shipped to another lab for the RIA of luteinizing hormone (LH) outputs.

playback of male nest coos (Cheng et al., 1998). These data support the behavioral evidence that a female’s own nest coos stimulate her ovarian follicular growth. The unique discharge pattern of female nest coo responsive units in the hypothalamus suggests that the Ov shell-hypothalamus axis is involved in processing coo recognition. Further evidence can be seen from another functional feature of the system: The sum total of excitatory and inhibitory discharges (percentage discharge change) arriving at the preoptic area and the anterior medial hypothalamus was similar whether the nest coos were female or male (Cheng et al., 1998). These observations suggest that the GnRH network, as reflected in the LH response, is governed not by the overall intensity of the stimulus (level of male or female nest coo discharge) but by the recognition of a specific coo feature: An unmistakable cue is provided by the discharge pattern of the female-nest-coo-specific units. That


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Fig. 5. Female-nest-coo-specific units in the preoptic area of the hypothalamus. Response of unit 960108 in the preoptic area of a female ring dove to different acoustic stimuli. (A) The female nest coo as the stimulus; the activity of the unit increases significantly. Top, Dot raster plot showing 10 sweeps of the unit’s response. Each dot represents one spike. Middle, Histogram of the unit’s response. Bottom, Computer amplitude display and spectrogram of the female nest coo. (B) Reversed female nest coo as the stimulus; no change in neuronal activity can be detected in the number of spikes over time or in the histogram representation. (C) White noise as the stimulus: no change in neuronal activity. (D) Male nest coo as the stimulus; no change in neuronal activity. A closed triangle denotes the onset of the stimulus. (From Cheng and Peng, 1998. Copyright 1998 by the Society for Neuroscience.)

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the system does not respond to stimulation in a linear manner is consistent with the pattern of follicular growth described in the next section.

IV. What Does the Female Nest Coo ‘‘Mean’’ to the Male? Given that the female coo stimulates follicular growth, is it designed to provide the ‘‘message’’ or ‘‘meaning’’ of ‘‘commitment’’ to the male? Not exactly, for the relationship between female coo and follicular growth is not linear but incremental up to the threshold level where the follicle then takes on exponential growth culminating in egg-laying (Cheng, 1993; see Fig. 1). The threshold level of exponential follicle growth varies from one female to another. In some cases, a female may nest coo nearly 80 to 200 times (when measured two hours each day until the female lays eggs) before any evidence of measurable follicle change, while others may reach threshold at half that number. Upon further examination, however, we found that the best indication of impending follicular growth is the change in the quality of the coos. The female in the threshold stage squats low in the nest bowl as though incubating and emits gutteral, grunting coos that sound quite distinct even to our human ears. After bouts of joint cooing in which the male and the female nest coo in synchrony, a male typically stops cooing altogether or coos only sporadically once the female is firmly planted on the nest site, and emit gutteral coos while she cooperates with him in the construction of a nest. Thus, the female coo can be considered a reliable signal of intent to a male, although early coos do not reveal what she ultimately will do. Since exponential follicular growth in the female is contingent upon what the male does, in this sense the female nest coo is a manipulative signal. In other words, prior to the threshold level of nest coo (or gutteral coo), female behavior (and hence her endocrine change) is contingent upon the male’s behavior. A female will continue to coo only if a male persists in cooing until a threshold is reached. Interesting, the threshold varies individually. Evidently, females also scrutinize male coo signals in a minute to minute manner. In an ingenious experiment, Friedman (1977) demonstrated that females who saw and heard males courting them showed the greatest ovarian development, whereas females who saw and heard the same males courting, but not courting directly to them, showed only mild development. Females in this case appear to have selected males for the quantity or perseverance of their coo signals. The male response to female nest coo conforms to the notion that the ‘‘meaning’’ of acoustic signals is reflected in the receiver’s response (Smith, 1977, 1998; Slater, 1983). In sum, the female nest coo is a vocal signal which provides the male


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with reliable, though minimal, information about female reproductive readiness that is sufficiently enticing for the male to sustain his courtship. Vocal-endocrine feedback mechanisms may also apply to male coos. Indeed, Brockway made the first observation that volume of the testes in male budgerigars was reduced after devocalization (Brockway, 1965), suggesting that male vocalization may facilitate testicular activity. In the case of male ring doves, the endocrine profile of the male during the breeding cycle is strikingly similar to that of the female, except during the egg-laying period. The release patterns of LH and FSH of the male mirror those of the female up to the point of egg-laying (Cheng and Balthazart, 1982). This shared endocrine profile might serve to ensure the commitment of the male to the female and thus the sharing of the incubation and rearing of young. It appears that the dawn chorus of male songbirds may also involve vocal self-stimulation leading to appropriate hormonal levels for territorial or mating interaction shortly after sunrise (Staicer et al., 1996). In our playback study, we noted that nest coos of other females are also effective in stimulating ovarian follicular growth. This may be the mechanism for female birds to synchronize breeding in colonial birds such as the ring dove. Thus, the Ov shell–hypothalamus pathway involved in vocal self-stimulation may also mediate the endocrine effect of vocal stimulation other than the bird’s own vocal signals.

V. Vocal-Endocrine Links: Cross-Species Comparisons How prevalent is the vocal endocrine pathway? Is vocal self-stimulation unique to doves or more generalized? Projections to the hypothalamus from thalamic regions that receive midbrain auditory input have been reported for amphibians (Allison and Wilczynski, 1991) and rats (LeDoux et al., 1985). In rats, as in doves, the thalamic projection to the VMN of the hypothalamus does not originate from the core auditory thalamus but from nuclei adjacent to the medial geniculate body. And, as in doves, the area of the auditory thalamus that projects to the hypothalamus receives input not from the auditory midbrain (central inferior colliculus) but from its shell region. By contrast, in amphibians on the basis of a study of frogs, it is the core auditory thalamus, the central nucleus, that gives rise to the projections. Single-unit recordings within the ventral hypothalamus identified neurons preferentially responsive to conspecific mating calls (Wilczynski and Allison, 1989). Thus, it appears that the auditory thalamic-hypothalamic tract is a conserved system (Fig. 6). Interestingly, the estrogen-sensitive property of this system makes it particularly suitable for the mediation of vocal communication during the breeding season.

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Auditory Afferents to the Hypothalamus in Three Taxa

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Fig. 6. Auditory afferents to the hypothalamus in three taxa. A diagram showing connections between the midbrain vocal units, the thalamic auditory units, and the hypothalamus in rats, birds, and frogs. AH-anterior hypothalamus; AM-anterior medial hypothalamus; AN-anterior thalamic nucleus; CN-central thalamic nucleus; IC-inferior collicularis; ICo-n. intercollicularis; MGB-medial geniculate body; MLd-n. mesencephalicus lateralis, pars dorsalis; Ov-n. ovoidalis; PMH-n. medial posterior hypothalamus; POAanterior preoptic area; SIN-secondary isthmal nucleus; TS-toris semicircularis; VH-ventral hypothalamus; VMN-ventromedial hypothalamus. (From Cheng, 1993.)

The Ov shell region was subsequently identified in connection with the early gene expression-sensitive caudomedial neostriatum (NCM) in songbirds (Mello and Clayton, 1994). A case may be made that the specialized shell region of the auditory thalamus developed after that of amphibians. A study using a calcitonin-gene-related peptide, an evolutionarily conserved marker, showed that the marginal cell population of the nucleus Ov is distinguishable from the core group in reptiles, birds and rats (Brauth and Reiner, 1991). These marginal cell regions retain the properties of the core cell group but develop distinct functions. In doves, the shell region of Ov and the area surrounding the nucleus mesencephalicus lateralis, the pars dorsalis (MLd), and the midbrain auditory relay (namely the ICo region) are distinguishable from their respective core groups in that both are rich in estrogen receptors and hence are closely


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linked to breeding. By virtue of the shared property of these shell regions and the hypothalamus (also rich in estrogen receptors) they form a pathway uniquely suited to process estrogen-dependent coo vocalizations during the breeding cycle. In the breeding season, the increased levels of estrogen may sensitize the female’s auditory system to pay particular attention to male nest coos; in a preliminary study, we have found that estrogen treatment in females intensifies coo-sensitive firing patterns in Ov shell units. Concurrently, along with visual stimulation, high estrogen levels in the ICo combined with sharply-tuned male nest coo stimulation, set the stage for the female nest coo display. In songbirds, the shell region of Ov, NCM, and HVC shelf (the region surrounding the high vocal control nuclei, i.e., the caudal plane of nucleus hyperstriatum ventrale) form a loop believed to be involved in song recognition (Mello and Clayton, 1994). The field L projections to the HVC shelf are thought to provide audio feedback to the motor system. The Ov shell in ring doves also projects to the NCM, and the telencephalic targets (fields L1, L2, L3) of the Ov projections also receive inputs from the Ov shell. Whether field L of non-vocal learners also serves to influence vocal output, however, has yet to be addressed. Existence of a vocal-auditory-endocrine system in other taxa (see Fig. 6) suggests that this system may be an old evolutionarily pathway from which a more sophisticated system evolves. Since autonomic responses such as heart beats, blood pressure, skin conductance response, and endocrine responses are inseparable signs of emotional state, the finding that vocalization has a built-in control of the endocrine system led me to refocus on the meaning of the affective state in acoustic communication.

VI. Affective States in Acoustic Communication Recent progress in the study of bird song and its development provides much of our current knowledge on the neurobiological basis of animal vocal communication. Marler’s early work in primates and songbirds led him to question the commonly held view that animal vocal signals merely reflect the affective state and to focus instead on symbolic signaling. Similarly, Smith (e.g., 1998) has focused on the cognitive aspects of information sharing in animal communication. Although the affective state plays an important role in other theories of vocal communication (e.g., Owren and Rendall, 1998; Owings and Morton, 1998), sadly it has not become an experimental variable in the field of the behavioral neurobiology of birdsongs. The affective state is notably absent in the vocabulary of much bird song literature, most notably the neurobiology of bird songs. As

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a result, there has been a void of studies on the neural underpinnings of the affective state of vocal signals which has impeded a fruitful synthesis of information-based bird song findings and affective state-based behavioral findings. A. Honest States Selective pressures favor communicative signals that convey the honest affective state. For example, although a smile in a commercial advertisement is a calculated part of the sales pitch, the meaning of the smile remains the same signal for joy and happiness. Why? Because a smile, genuine or artificial, invokes a ‘‘good’’ feeling in the recipient. We are more likely to tip a cab driver or a waitress flashing an ingratiating smile than a disgruntled face. I would suggest that the emotional response to a smile is so entrenched in us that although the meaning of a smile is subject to different interpretations, the emotional response itself is resistant to change. Similarly, as discussed in the preceding section, vocal signals can reflect a particular endocrine state. It is more difficult to fake a physiological state than voluntary muscle movement and also more costly. Some, if not most, vocal signals are constitutionally tied to a physiological state, and therefore reflect an honest reflection of endocrine condition. B. Emotional State as Referent In human speech, the fundamental frequency and the amplitude envelope are related to emotional content (Lieberman and Michaels, 1962). Similarly, vocal signals used by fearful or aggressive animals are distinguishable by frequency and pitch (Morton, 1982). Birds discriminate between acoustic features and respond according to the occasion presumably by ‘‘reading’’ the affective state of the signaler. How do animals ‘‘de-code’’ acoustic signals? We hypothesize that the endocrine responses associated with vocal signals provide the necessary reference for both sender and recipient. C. Vocal Signals as Emotional Expression Vocalization, arguably one of the most conserved forms of emotional expression, may take on a referential quality as cortical connections expand. Recent studies with human infants show, for example, that grunts first occur as vegetative sounds, are then used as expressions of an internal state, and eventually develop into a ‘‘referential ability in language’’


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(McCune et al., 1996). This referential ability in language coincides with the development of mental representation (McCune, 1995). Although according to Ekman (in Darwin, 1998), Darwin never suggested that emotional expression is a means of signal communication. Darwin (1872) was the first to recognize that emotional expression ‘‘serves as the first means of communication between the mother and her infant.’’ We can credit Darwin with documenting the universality of emotional expression as social behavior. Facial expression has been extensively studied in the context of emotional expression (Ekman, 1992, 1994), while vocalization as a form of emotional expression and the mechanism by which a receiver detects the emotional referents of a signaler has not been well studied. To date, the analysis of the vocal signals of animals has focused on the ensuing behavior of the signal receiver. For example, Cheney and Seyfarth (1980, 1992) showed that acoustically-distinct alarm calls of vervet monkeys, in response to distinct predators, result in effective escape strategies by the receivers. These observations have led the authors to attribute a referential quality to primate acoustic communication. Similarly, the audience effects on male chicken food calls and alarm calls again suggest that a vocal signal is used to evoke a desired response from the receiver and is not simply a reflection of the sender’s internal state (Marler et al., 1986; Karakashian et al., 1988). These findings suggest that the response to vocal signals is not fixed and reflexive, but do not necessarily contradict the notion that vocal signals are in essence an emotional expression. Instead, I believe that at its core, the vocal signal is emotional communication. At present, although we do not have critical data to support this idea, this hypothesis can be tested with, for example, a chick’s distress call, which will be discussed later in this chapter. I will also make a case that some, if not all, vocal learning is a case of emotional learning. My goal here is to call attention to considerable anatomical and behavioral evidence that supports the viability of ‘‘emotional sharing’’ as another pillar from which to forge a theory of vocal communication. Smith has compiled impressive data showing how the vocal signals of birds can convey the sex, age, and size of signalers (Smith, 1977). This ‘‘indexical data,’’ as Locke coined it, is the basis for early vocal affect exchange between mother and infant; for example, infants can respond differentially to the sounds of males and females (Locke, 1995). I propose that these indexical data have affective references. Recent neuroimaging studies provide some support for this notion. For example, PET studies of adult subjects show that a more primitive region of the brain (temporal lobe limbic areas including the amygdala) is activated for sex recognition (Andreasen, 2001; plate 6–9B) suggesting that emotional circuitry is used in ‘‘decoding’’ certain communicative signs.

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D. Moto-Mimicry and Emotional Sharing When Smith discusses ‘‘information sharing,’’ he is not referring to emotional sharing (Smith, 1999). In my view, ‘‘emotional sharing’’ is the foundation for pre-representational communication while ‘‘information sharing’’ is a ‘‘spin-off’’ of emotional sharing. What is the mechanism by which emotional sharing can be achieved? Voice mimicry has long been invoked to explain an infant’s tendency to match its mother’s or caretaker’s voice. Studies of an infant’s ability to match pitch, voice quality, and other cues suggests that this kind of vocal accommodation sets the ‘‘path’’ for spoken language (Locke, 1995). Furthermore, Locke characterizes mother-infant vocal accommodation as social (affect) communication. That is, infants use pre-linguistic vocal sounds to convey this affective state just as animals use sounds as a means of emotional expression. Locke argued that this emotional sharing is the basis for the empathy that fosters the development of spoken language. The effect of motor mimicry on emotional states also occurs with other forms of emotional expression. Using electronic sensors, Dimberg (cited by Goleman, 1995) showed that smiling or angry faces elicit subtle muscular changes in the face of the viewer. By including ‘‘the sound production and the feedback to one’s own ears’’ (Locke, 1995, p. 332), Locke extended the idea of Izard (1978, 1992) that a person’s emotion is amplified by way of feedback from facial muscles. The vocal self-stimulation system we have painstakingly documented in the ring dove may be such a mechanism linking the motor program and the emotional state in vocal recognition.

VII. Emotional Referent in Vocal Communication: Role of Vocal Self-Stimulation A. Vocal Recognition and Vocal Self-Stimulation To illustrate how the vocal-endocrine feedback system may be a mechanism involved in emotional sharing that leads to vocal recognition, let us consider a scenario in which a hen reacts to a chick’s distress vocalization. Ample evidence has shown that a hen will predictably respond to a chick’s distress call by a call with a ‘‘cluck’’ call (‘‘Here I am, All is Well’’: Collias, 1987), and then approach and retrieve the chick. However, it is unlikely that a ‘‘distress call’’ means ‘‘distress,’’ in a linguistic sense to the hen. How then does the hen understand the meaning of distress and respond accordingly to the chick’s ‘‘distress’’ signal? One could easily consider reflexive response as an answer. That is, the hen is hard-wired to respond reflexively in a pre-set way to distress vocalization.


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Although this view is plausible, it does not incorporate that important element of vocal communication: emotional communication. In order to insure that the hen recognizes the urgency of the chick’s predicament and responds appropriately, the surest and swiftest mechanism would be to access the hen’s own ‘‘fight or flight’’ mechanism (i.e., for the hen to experience what the chick is experiencing, namely the physiological responses associated with stress). Any vigilant mother can attest to the heartpounding reaction she experiences in response to the slightest indication that her child is in harm’s way. We postulate that when a hen hears a chick’s distress call, that signal is transmitted from the auditory thalamus to the hypothalamus through the avian amygdala which then invokes a rise in corticosterone. Although this pathway has not been experimentally demonstrated in chicks, as we will see later, this scenario is inspired by a well-established fear-conditioning mechanism in rats (LeDoux, 1996) and by recent findings that a similar anatomical pathway exists in birds (Cheng et al., 1999). The significance of the affect state in a hen’s response could be tested by depressing the corticosterone level by injecting the specific compound that blocks the conversion of the precursor of corticosterone (deoxycorticosterone) to corticosterone. It is predicted that such a hen would not look for her distress-calling chick. Such results would suggest that a reflexive response without an emotional component cannot account for the predictability of a hen’s response. In other words, if the hen does not experience distress, as with a rise in corticosterone, the chick’s call does not achieve the desired effect from the hen. We suggest that the postulated elevation of corticosterone in the hen provides the reference or ‘‘meaning’’ to the distress call. A chick in a distressing situation, as when separated from the hen, shows an alarm reaction, including a stress response with a corticosterone rise and distress calls. A hen hearing the chick’s calls will also experience a rise in corticosterone. In this way, the chick and hen ‘‘share’’ an emotional message (Fig. 7). To our knowledge, assessment of the corticosterone level of chicks and hens during distress vocalization has not been attempted. However, the ability of corticotrophin releasing-factor (CRF), the hypothalamic factor that stimulates the release of corticosterones, to intensify vocalization of isolated chicks in a dose-dependent manner (Panksepp et al., 1992) suggests a role for corticosterone in production of distress vocalizations. As in other vertebrates, stress responses of the chick and the hen are likely activated through the amygdala (the nucleus taenia in birds) which is responsive to species-specific ‘‘fight or flight’’ stimuli that require little or no learning to evoke a fixed endocrine response (more on the nucleus taenia in Section E.) The hen, therefore, without experimental manipulation, predictably

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Emotional Sharing in Vocal Communication Endocrine Referent of Distress Call

Distress Situation

Distress Calls

Chick

Corticosterone Rise

Hen

Cluck Cluck Calling

Corticosterone Rise

Fig. 7. Emotional sharing in vocal communication: endocrine referent of distress call. A diagram illustrating how vocal signal recognition may be achieved through emotional sharing. In the case of distress vocalization, a hen’s appropriate response (signifying recognition or understanding of the vocal signal) is postulated to be mediated by a corticosterone rise experienced by both chicks and hens. Activation of corticosterone and distress call in chicks can be explained in terms of a pre-adapted stress response. A hen’s hypothetical corticosterone rise has not yet been tested.

recognizes the distress call and responds appropriately. Although it is unlikely that corticosterone is the only endocrine hormone involved in the stress response, since the corticosterone rise in a stress situation has been consistently demonstrated in mammals and birds (Breuner et al., 1998; Romero et al., 1998, 2000; Sapolsky, 2002), I opt for this simplified scenario for purposes of discussion. It should be noted that the distress call, as far as we know, is a stimulus to which the hen is ‘‘pre-adapted’’ to respond, requiring little or no learning. There are also other vocal signals where recognition is established through emotion-linked motor program. A chick’s own distress call, which is a repetitive vocalization like the nest coo in the ring dove, meanwhile provides feedback (via a vocal-endocrine feedback mechanism) that may increase the level of endorphins in the brain. Endorphins have been shown to inhibit separation-induced distress vocalizations in chicks and dogs (Panksepp et al., 1992). The release of endorphins, which have pain-blunting and -soothing effects during stress has also been demonstrated in various species including humans (Sapolsky, 2002). We suggest that distress vocalizations enhance the brain levels of endorphin, which dampens the distress call and serves as a cap for the duration of vocalization. In a playback study in chicks, we recorded the number of distress vocalizations emitted during a five minute playback

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Mean Number of Distress Vocalizations (dv) During Five Minute Playback Period # of Distress Vocalizations

450 400 350 300 250 200 150 100 50 0

cluck

own dv's

other dv's

control

Fig. 8. Mean number of distress vocalizations during five minute playback period. A histogram showing effectiveness of various vocalizations in reducing the intensity of distress vocalizations emitted by chicks. Each 2–6 day old white leghorn chick (n = 28) was separated from its brood mates for 15 minutes and was subjected to playback in only the middle 5 minutes. Each chick received all four playback conditions and served as its own control. The number of distress vocalizations emitted during all playback conditions was significantly lower than in the control condition (p < 0.001). The number of distress vocalizations emitted during playback of clucking was significantly lower than the number emitted during playback of both the chick’s own distress calls and a brood mate’s distress calls. (Wansaw and Cheng, unpublished data.)

period when one chick was separated from other chicks. We found that the playback of a hen’s cluck-cluck calling reduced the chick’s distress call significantly, as did the chick’s own calls, compared to control chicks who did not receive any playback (Wansaw and Cheng, unpublished data; Fig. 8). Thus, although contrary to common sense, the chick’s own distress call reduced the chick’s rate of calling which is consistent with the idea of vocal self feedback. However, since we did not measure the endorphin levels, it is not yet clear if the alteration of behavior was mediated in this way. Similarly, the hen’s cluck-cluck calling may facilitate the chick’s endorphin release through Ov shell-hypothalamus linkages. The hen’s own endorphin levels may also be elevated through a vocal-self stimulation mechanism. B. Motor Theory of Vocal Signals and Vocal Self-Stimulation System The emotional state is part of an overall internal state. We propose an internal state-based processing view of vocal signal that has much in common with the motor processing view of perception (Lieberman et al.,

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1967; Williams and Nottebohm, 1985) and the idea of posture encoding in the vocal signal (Zahavi, 1987). According to the motor theory of perception and comprehension of language (Lieberman and Mattingly, 1989) and of birdsong (Williams and Nottebohm, 1989), signal perception is mediated by the receiver’s motor reproduction of a signal. The motor theory of signals, however, specifically refers to the motor articulation of sound (Lieberman and Mattingly, 1985) or to the pattern of neural activity in sound production in songbirds (Williams and Nottebohm, 1985). Using recordings from the high vocal center (HVC) and motor neurons (nXIIts), Williams and Nottebohm (1985) showed that a receiver does not recognize a song syllable until it experiences the motor actions that would produce the same sound. This means that neural activation without actual motor output is sufficient for perception. Recent experiments by Dave and Margoliash (2000) further demonstrated that the RA neurons that are active in singing also respond to the playback of birds’ own song in sleep. Thus, song stimulation could engage premotor circuits used in singing (Troyer and Bottjer, 2001). Activation of this vocal-related circuitry may be involved in vocal signal perception. Interestingly, lesions of the HVC of female canaries alter their perception of male songs (Brenowitz, 1991), and disrupt discrimination in a go/no-go task (Brenowitz, personal communication), suggesting that female songbirds ‘‘read’’ or ‘‘share’’ the motor patterns of vocal signals to process them. That the HVC changes seasonally in female red-winged blackbirds, Agelaius phoeniceus (Kirn et al., 1989), is also consistent with the proposed function of the female HVC. Although observations that non-verbal infants, tamarin monkeys (Ramus et al., 2001), Mongolian gerbils (Sinnott and Mosteller, 2001), and quail (Kluender, et al., 1987) can discriminate human speech sounds without being able to produce them, can be construed as evidence against the motor theory of perception, this need not be the case. Firstly, these studies did not obviate the possibility that non-vocal infants and animals may discriminate speech sounds based on the different emotional states that they invoke. For example, the ability of budgerigars (Melopsittacus undulatus) to discriminate among species-specific vocal signals that are highly distorted (Park and Dooling, 1986) suggests that discrimination may not be based entirely on phonetic discrimination. Secondly, we are not proposing that all sound perception is mediated by activation of the motor pathways by vocalization. Instead, consistent with the emotion-based theory of vocal communication, the perception of some sounds may be directly mediated by emotional response. In some cases, such as distress calls, calls are pre-adapted stimuli to which hens respond via the amygdala circuit without involving the motor program. In the case of learned


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vocalizations, we propose that emotional response is mediated by the motor program through vocal-auditory-endocrine pathways. Activation of the motor program becomes essential only in the perception of learned vocalizations. In learned vocalizations, ‘‘emotional sharing’’ is achieved through activation of the motor program for both the vocalizer and the perceiver. Zahavi (1987) proposed that vocal signals are ‘‘analogues’’ to the posture of the body of the signaler at the time of utterance and hence ‘‘encode’’ the honest motivation of the sender. We propose, however, that it is the emotional state associated with the distinct articulation, or neural activity (motor program), and posture in song production, and not the motor action or the posture alone, that is integral to vocal communication. Moreover, vocal-endocrine links ensure that all these elements, including motor programs, endocrine profiles, and sensory feedback, are matched in the vocal signaler and the listener. C. Vocal Learning and Emotional Sharing Experiments on the ontogeny of songs and calls suggest that calls generally develop independently of learning (Thorpe, 1958; but see Zann 1985), with some exceptions as in the case of the male long call in zebra finches (Miller, 1979a). Indeed, deafened young doves develop normal nest coos as adults (Nottebohm and Nottebohm, 1971). Also, interestingly, songs of suboscine species with a relatively small repertoire apparently do not require learning. In contrast, songbirds imitate the songs of adults through auditory feedback (Konishi, 1965a,b; Kroodsma, 1982) or through a process of preferential retention of learned songs as a function of experience (Nelson and Marler, 1994; Marler, 1997). Evidence also suggests that calls associated with specific emotional states often share remarkably common acoustic structures across species. For example, a down sweep of frequency is typical among alarm calls (Owings and Morton, 1998). Using data on avian and mammalian vocalization, Morton (1982) developed a set of motivation-structural (MS) rules to reflect the interplay of motivational state and sound structure. Recently, Hauser (1998) made a between-species comparison of the relationship between motivational state and pitch. Results from the analysis of several hundred vocalizations from 43 nonhuman primates corroborate the MS rule. Similarly, different languages spoken by mothers to achieve a desired behavior from infants share common acoustic patterns; praiseful speech in English (‘‘very clever, darling’’) contains the same distinct acoustic patterns as that spoken in French (‘‘bravo’’), German, or Italian (Fernald, 1992). Acoustic patterns for prohibition,

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comfort and attention are distinct from each other but share common acoustic features across cultures. Given the motivational contribution in the development of sound structure, vocal learning would likely include mimicking the acoustic features as well as the affective state. Bodily structure associated with a specific emotional state appears, at least in part, to shape the quality of sound production. Vocalization thus has its distinct somatic as well as physiological states, viewed collectively as the internal state. The internal state we envision includes Zahavi’s (1987) idea that a vocal signal provides information about the posture of the signaler at the time it produces the signal. Given the direct access of vocal self-stimulation to the endocrine system, we propose that recognition of vocal signals, especially those acquired through learning, is made possible through the association of a vocal motor program and an internal state, mediated by a vocal self-stimulation mechanism. In a typical experiment, vocal learning develops in a social setting involving a tutor and a student. Since this setting is no different from any other communicative interaction involving a sender and a receiver, effective communication would involve emotional sharing. The student achieves emotional sharing with the tutor when the student copies via motor mimicry the distinct patterns uttered by the tutor. Once shared emotion (including bodily posture, endocrine state, and motor pattern) is achieved, the motor pattern associated with a distinct note or phrase becomes the ‘‘template’’ the student can match in rehearsal. In species where young birds learn to produce songs from memory (when there is no tutor to copy from), we need look no further than emotional circuitry for an underlying mechanism. As has been amply shown, learning that involves emotional circuitry characteristically leaves crude but indelible memories (LeDoux et al., 1989, 1996; McGaugh, 1992). Perhaps young birds exposed to their fathers’ songs learn the emotional content of sound or pitch contour rather than specific acoustic notes. When the young birds’ vocal faculties mature, they may then select vocal sounds that match the emotional content of their fathers’ songs. We reason that during the sensory phase of song learning, the template could not possibly contain specific acoustic notes because the motor program has not yet developed. However, it is possible for young birds to encode pre-adapted emotional responses to their fathers’ (or tutors’) song motif and pitch contour, such as temporal coding (rhythm) of the heart beats and respiratory pattern. The observation that auditory responses in the song system are highly selective and emerge not before but during the period of sensorimotor learning (Troyer and Bottjer, 2001) is consistent with this idea. In this context it would be interesting to determine whether the song-matching of birds


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learning from memory is inferior to that of birds learning in the continuous presence of a tutor. The importance of the emotional element in song learning is manifested in many forms but is most tellingly revealed in studies of song-learning preference. The use by Dooling and Searcy’s (1980) study of cardiac measures of responsiveness confirmed that the nestlings preferentially learn conspecific songs. Marler (1997) cited this study as an effective test of avian preferential learning that is independent of imitations. We suggest, however, a different interpretation of Dooling and Searcy’s finding. Evidently, conspecific songs readily evoke emotional responses, manifest as cardiac output, and thus are remembered (copied or encoded) more readily and learned more quickly. A conspecific song derives its premiere status as ‘‘learning friendly’’ from its ability to evoke a pre-adapted emotional response. For birds to acquire species-typical songs, a live tutor is often more effective than a tape-recording (e.g., Chaiken et al., 1993; Baptista and Gaunt, 1996, but see Nelson, 1997), perhaps because a live tutor is more effective for evoking the optimal emotional tone for learning. Evidence that young male finches are more likely to learn songs from adult males with whom they have had close contact (Mann and Slater, 1994; Mann and Slater, 1995; Pearson et al., 1999), even when the interaction was antagonistic in nature (Jones and Slater, 1996), suggests that some aspects of social interaction influence song learning. Although an elevated level of arousal or attention has been suggested as an alternative interpretation of this social effect (Nelson, 1997), we propose instead that social interaction fosters an ‘‘emotional sharing’’ which facilitates song learning. For example, in an antagonistic situation that invokes a fear response in the tutee, the impact on learning may be accounted for by an emotional response involving the release of the stress hormones epinephrine and norepinephrine, and causing an elevation of arousal (Sapolsky, 2002). Emotional circuitry will be discussed further in section VII.E. In conclusion, we suggest that ‘‘sharing’’ of the ‘‘internal state,’’ whether a general emotional state or a specific motor program, is crucial to the learning and recognition of a learned song. In primates such as macaque monkeys (Macaca nemestrina), the motor program, as well as the visual and auditory features associated with performance of a specific action, are neatly packaged in audiovisual mirror neurons in the ventral premotor cortex (Kohler et al., 2002). These neurons are activated whether a monkey performs a specific act (e.g., ripping paper) or hears the sound of the act. Thus, by evoking motor ideas, a monkey can recognize actions performed by others even if they are only heard. It appears that the format for encoding sound through a motor program is preserved in the form of a motor idea and centralized in the cortex.

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D. The Internal State and Vocal Motor Program Damasio’s ‘‘somatic marker’’ is an apt description of the internal state in humans (Damasio, 1999). Somatic-markers, which describe representations in the somatosensory cortex of the body’s changing states, play a pivotal role in the decision-making process. The creation of markers involves other structures such as the prefrontal cortices, dorsal posterior thalamus, and amygdala. Somatic-markers may operate through consciousness or outside of consciousness, which may be what Darwin refers to as the internal state. Similarly, the emotional referent mediating vocal recognition that we hypothesized is the same in concept as Damasio’s somatic markers without the component of consciousness. In species that use vocal signals as the main channel of social communication, the shift from general emotional referent to a motor referent may take on primary import in song recognition. The association of vocal signals with a specific motor program becomes a sufficient reference for sharing by the sender and the receiver. As more sophisticated vocal apparatuses create more varied acoustic sounds, the vocal motor activity associated with a distinct acoustic feature provides sufficient distinction at the neural level to represent the internal state. For example, using recordings from the nXIIts motor nucleus of zebra finches, Williams and Nottebohm (1985) discovered that the neurons responding most strongly to syllables composed of a down swept frequency are inhibited by high-frequency un-modulated syllables. Interestingly, our perception of speech does not depend on hearing alone; rather, visual reading of lip movement assists in identifying syllables accurately (McGurk and MacDonald, 1967). Clearly, accurate motor reproduction is critical in some vocal signal recognition. Although the motor theory of song perception has been developed using male birds as a model, there is no a priori reason for the mechanism to be different for females. Lesions to the forebrain nucleus HVC altered perception of male song by female canaries (Brenowitz, 1991), reduced the ability of female canaries to discriminate between highly and weakly stimulating songs (Del Negro et al., 1998), and significantly attenuated correct recognition of conspecific male songs in female European starlings (Gentner et al., 2000). Similarly, lesions to the lateral portion of the magnocellular nucleus of the anterior neostriatum (IMAN) decreased the female canaries’ ability to discriminate synthetic sound stimuli (Burt et al., 2000). These observations suggest that a motor program is also involved in female birds’ song recognition. The motor theory of song perception, however, does not apply to females of certain species, such as zebra finches. Although female zebra


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finches cannot sing, they do recognize their fathers’ and mates’ songs (Miller, 1979a; Miller, 1979b). The high vocal control nuclei (HVC) in these females are small, area X is lacking (Nottebohm and Arnold, 1976; Simpson and Vicario, 1990), and the projection from HVC to RA is minimal or absent (Konishi and Adutagawa, 1985; Simpson and Vicario, 1990). Clearly, female zebra finches lack a motor program. How then do these females recognize male songs? The emotional state-based process of perception would suggest that female zebra finches use a basic form of learning such as emotional learning. We postulate that in female zebra finches, memory of song is not stored in motor nuclei but rather in the limbic structures. Indeed, female zebra finches retain conspecific song preference following electrolytic lesion to the ‘‘cortical’’ song nuclei, HVC (MacDougall-Shackleton et al., 1998). Brain anatomical connectivity between vocal control nuclei and the limbic system supports this behavioral observation. The limbic structures, such as the hypothalamus, the amygdala, or a somatic marking structure (brain areas such as the dorsal posterior thalamus (see section VIII forebrain pathways in the non-vocal learner), are directly or indirectly connected to the basic brainstem vocal control pathway that originates from the midbrain vocal nucleus, ICo. For example, the ICo receives afferents from the hypothalamus and the nucleus taenia in the ring dove (Cheng et al., 1987), and the preoptic area and the dorsal thalamus in the grey partridge, Perdix perdix (Briganti et al., 1996). Similar vocal-limbic pathways may also exist in female zebra finches. In females that are equipped with motor faculties, motor programs provide the tool for finetuned learning. In this context, it is interesting to note the finding by Simpson and Vicario (1990) that the simple acoustic structure of the female call in zebra finches does not require syringeal innervation, but is instead governed by respiratory patterning. In other words, production and recognition of the female zebra finch call may well involve the limbic system as predicted by the emotional state-based theory of vocal behavior. Based on their observations of the effects of HVC, RA lesions, or tracheosyringeal nerve sections on simple versus complex calls in male and female zebra finches, Simpson and Vicario (1990) suggested that the ICo– ventral parabrachial nucleus (PBv) pathway (Wild and Arends, 1987) is involved in the production of simple calls/songs, whereas the ICo– tracheosyringeal motor nucleus (nXIIts) pathway (Nottebohm et al., 1976; Vicario, 1991), which is more fully developed in male songbirds, is required along with HVC and RA in the production of more complex acoustic songs. This finding was subsequently validated by experiments involving the electrical stimulation of various vocal control nuclei. While the midbrain produced simple vocalizations, vocalizations elicited from the

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forebrain, HVC and RA, were complex with features specific not only to the species, but to the individual bird’s own learned song (Vicario and Simpson, 1995). Given that both pathways, the ICo-PBv and the IConXIIts, are present in male zebra finches, both pathways are most likely involved in the production of complex acoustic structures. The predominant use of a motor pathway, along with the development of telencephalic structures, enables the bird to diversify motor programs to match diversified conditions, such as distinct vocal signals associated with different predators. We propose that female zebra finches with less well-developed IConXIIts learn the emotional content (respiratory patterns) of a call or song and store it without involving the motor program. We therefore infer that the female zebra finch’s ability to discern her father’s and mate’s songs is relatively crude and not as refined as that of females of other species which have developed motor pathways. In fact, although female zebra finches recognized and significantly preferred the songs of their own fathers to the songs of other male zebra finches, when the test involved the father’s song and a similar song (i.e., the uncle’s song), the preference was not statistically significant (Miller, 1979b). The primacy of motor programs in discerning different vocal signals can free the vocal signal from its monolithic relationship with the emotional state. That is, variations in acoustic features may be associated with the general emotional message. For example, qualitatively different alarm calls produced by male chickens (Evans et al., 1993) convey the basic emotional message ‘‘danger.’’2 This is amply shown in the initial startled response to playbacks of alarm calls. Given that hens can select specific anti-predator behavior in response to the playback of male chicken alarm calls, such as in the absence of any visual contextual cues provided by the vocal signaler, Evans et al. (1993) concluded that male chicken alarm calls are ‘‘functionally referential.’’ The distinct alarm call of vervet monkeys (Cheney and Seyfarth, 1980) is another example. As the forebrain region expands to accommodate memory circuits, animals learn to associate distinct acoustic features (and hence distinct 2

According to Porges (1997), the phylogenetic shift in regulation of the heart in vertebrates provides an insight into the evolution of emotional responses. In teleosts, chromaffin tissue that stores catecholamine is located within the heart. Adrenal medulla containing chromaffin tissues are only present in birds, reptiles, and mammals. This shift in location is important because cardiac output is now under neural (spinal) regulation. This, along with migration of the dorsal motor nucleus of the vagus that serves as pacemaker for the heart, provides rapid changes of of cardiac output required for emotional expression such as vocalization. Respiratory output and cardiac output are controlled by the same autonomic system.


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motor programs) with specific objects. One may ask then, what brain circuitry in the chicken supports such memories? We suggest that this is a case of emotional learning, as we will discuss in more detail in the next section. As such, the evolutionarily well-conserved emotional circuitry provides the basic mechanism for such learning to take place. Naturally, the extent of forebrain development may determine the complexity of learning. The chicken’s relatively limited forebrain capacity may explain why a hen’s response to an aerial alarm call, appropriately looking up, also occurs nearly half as often in response to other, non-aerial alarm calls (Evans et al., 1993). Still, the emotional state remains an integral part of highly-developed vocal communicative systems like ours. An abundance of evidence suggests that genuine communication requires that both speaker and listener be attuned to one another (i.e., that they have a matching emotional state). When we talk, it is our bodily expression and not merely the words we speak with which we communicate. Studies of married couples, for example, demonstrate that ‘‘a state of shared physiology’’ is the best indicator of successful communication and conflict resolution between spouses, over and above all other measures including facial expression (Levenson and Ruef, 1992). A couple was videotaped and their physiological responses (heart rate, skin conductance, sweat response) were measured as they discussed troubling issues in their marriage. Each partner was then asked to describe his or her feelings while reviewing the tape. Each partner reviewed the tape a second time and was asked to ‘‘read’’ the feelings of the other partner. The results indicated that the greatest empathic accuracy occurred when one partner’s physiology mirrored that of the spouse. E. The Emotional Circuitry, Repetitive Vocalization and Vocal Endocrine Links I have made a point of emphasizing emotional communication as the essential element of vocal signaling. The story would be incomplete without discussing the specific features and relationships between emotional circuitry and vocal endocrine pathways. LeDoux’s seminal study on fear conditioning in rats identified three structures as the basic circuitry of emotional response: the thalamus, amygdala, and hypothalamus (LeDoux, 1996). The so-called ‘‘short and dirty’’ or ‘‘low road’’ loop of emotional response circuitry is comprised of the input to the thalamus and the output from the hypothalamus, with the amygdala serving as the critical relay (LeDoux, 1996). This pathway is coined ‘‘short loop’’ because sensory

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inputs go directly to the amygdala rather than ascending first to the sensory cortex, to be processed and then projected to the amygdala. Destruction of the amygdala blocks fear conditioning whereas destruction of the cortex does not (LeDoux et al., 1986), suggesting that the amygdala plays the central role in orchestrating a rapid emotional response. Patients with bilateral amygdala lesions have difficulty recognizing a fearful face from a stack of photos (Damasio, 1994, 1999). These patients also have difficulty conjuring up a fearful face. These observations reaffirm the importance of the motor program in recognition of emotional expressions, vocal as well as facial. Given the importance of the amygdala in an emotional response to a pre-adapted stimulus such as a distress call, our hypothesis predicts that a hen with a lesion in the amygdala will not recognize a chick’s distress calls since without the amygdala her corticosterone level will not rise. A negative result may mean that a hen’s response is mediated not by the amygdala but by the vocal-endocrine pathway. Alternatively, other stress hormones such as epinephrine and norepinephrine maybe the basis for ‘‘emotional sharing.’’ This hypothesis is based on the fact that the avian amygdala sends robust projections to the hypothalamus (Zeier and Karten, 1971; Cheng et al., 1999) which controls the release of corticosterone via the hypothalamus-pituitary-adrenal system (Holmes and Cronshaw, 1980). Is there evidence that birds are equipped with a short loop like that of the rat? To our knowledge there has been no equivalent study of birds. However, several findings suggest that the short loop does exist. Using anterograde and retrograde tracing methods in birds, we have shown the existence of projections from the nucleus taenia to the hypothalamus in vocal learners (European starlings) and non-vocal learners (ring doves) (Cheng et al., 1999). Hypothalamic projections are a staple of the mammalian amygdala circuitry. Indeed, by virtue of this projection, first identified in the pigeon, the posterior and medial archistriatum (that includes the nucleus taenia) is thought to be an avian homologue of the amygdala (Karten and Doublebum, 1973). The posterior and medial archistriatum is a vast and loosely defined structure. The nucleus taenia is one discretely defined structure within the posterior and medial archistratum. In addition to the hypothalamic projections, the nucleus taenia receives subcortical sensory inputs as does the mammalian amygdala (Cheng, 1999). It is important to note that the auditory thalamic input to the nucleus taenia is none other than the Ov shell, the substrate involved in the vocal-endocrine pathway in ring doves; the Ov shell thus provides the critical link between amygdala circuitry and vocal endocrine pathway (Fig. 9). Also, when the posterior and medial archistriatum, which includes the nucleus taenia, was lesioned, pigeons failed to exhibit a defense-related, conditioned heart rate change (Cohen, 1976). Lesions in


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Fig. 9. Short and super short loops in vocal communication. A diagram showing connections between the vocal self-stimulation pathway and the amygdala circuitry. The stress or emotional response mediated by the hypothalamus can be initiated by preadapted vocal signals (e.g., distress calls) through the amygdala pathway or through repetitive vocal self-stimulation (such as nest coo, clucking).

the nucleus taenia also reduced fear-related responses in ring doves and European starlings (Cheng et al., 1999). As in the mammalian amygdala (Everitt, 1995), lesions in the nucleus taenia appear to alter sexual behavior in male quails (Thompson et al, 1998). In sum, the nucleus taenia exhibits many important features of the mammalian amygdala in terms of neural connectivity and function. We conclude that the nucleus taenia in birds is a homologue of at least part of the amygdaloid complex in mammals. It is worth noting that the location of the nucleus in starlings has been displaced from the ventral periphery of the anterior hemisphere to the medial periphery of the posterior hemisphere, presumably during the course of forebrain expansion (Cheng et al., 1999). Collectively, these findings suggest that a short loop emotional circuit exists in birds as well as in mammals. We propose that avian amygdala circuitry is involved in distress situations such as when a chick is separated from a hen or when a hen hears a chick’s distress calls or a male’s alarm calls. While the amygdala circuitry may be involved in the initiation of distress calls and a rise in corticosterone, when distress calls are delivered in a repetitive manner, they may invoke an endocrine change via a vocal self-stimulation mechanism. The relationship between the short loop and vocal self-stimulation is depicted in Figure 9. The hypothalamus can be activated via emotional circuitry, the short loop, or by vocal selfstimulation via super short vocal-endocrine links. We propose that the

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initiation of fear-based vocal signals, such as distress calls of chicks, is mediated by the short loop in chicks and that in hens call recognition is similarly mediated by the short loop, that is response mediated by amygdala without first processed by the ‘‘cortex.’’ In the case of vocal signals that require vocal learning, both signal learning and recognition involve vocal-endocrine pathways. Given that both the short loop and vocal-endocrine pathways involve the amygdala, it is conceivable that both pathways may be involved, to different degrees, in endocrine responses to vocal signal mediated stress situations. In this scheme, the perception of vocal signals involves sub-cortical systems as opposed to higher ‘‘cortical’’ structures such as the HVC, the high vocal center implicated in song perception in oscine birds (Brenowitz, 1991). We have advanced the notion that vocal signals may be elicited as part of a pre-adapted emotional response and that, moreover, the signaler’s endocrine state may change as the result of vocalization via the vocal selfstimulation mechanism. For example, in the case of repetitive alarm calls, the caller may benefit from self-stimulation by boosting endocrine preparation for ‘‘fight or flight,’’ while the receiver’s short loop is activated in the form of fear or stress responses without the endocrine benefit of a vocal self-stimulation mechanism (Fig. 10). In sum, the amygdala short loop is likely to be activated in response to pre-adapted stimuli such as predator-related vocal signals, whereas the vocal self-stimulation Endocrine States Associated with Alarm Calling Alarm Call

Auditory Thalamus Vocal Self-Stimulation

Auditory Thalamus

Short Loop

Endocrine Preparation for Flight or Fight

Fear Response

Signaler

Receiver

Fig. 10. Endocrine states associated with alarm calling. A hypothetical diagram showing how the involvement of the amygdala mediated circuitry (short loop) and vocal selfstimulation (super short loop) during an alarm call may result in a more advantageous endocrine state for the signaler than for the receiver.


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mechanism is likely to be involved in the vocal learning and recognition of learned vocal signals or in the singing of a song by an individual. It should be emphasized that, although there is a built-in endocrine response in hearing and vocalizing, glucocorticoid may not be the sole output. An emotional response invokes a range of endocrine changes. Changes in emotional state may involve one given hormonal change or there may be a change in the profile of endocrine states. Given the projections from the amygdala to the auditory thalamus (Cheng et al., 1999), the emotional state may in turn affect or modulate hearing and singing. It is worth noting that the proposed endocrine effect of vocalization is similar to the facial feedback theory of emotion (Tomkins, 1962; Izard, 1992). In one study, subjects were asked voluntarily to move certain facial muscles without the knowledge that they were mimicking the facial expressions of different emotions. The subjects were then asked to describe their moods. The results showed that the subjects’ feelings corresponded to the different expressions they had been asked to assume. Subjects wearing a positive facial expression were likely to report feeling happy, while subjects with a negative expression were likely to feel sad or angry (Ekman et al., 1983). This basic finding has been replicated in different cultures (Ekman, 1992, 1994). Similarly, in another study, subjects were instructed to make either happy or angry facial expressions while viewing a series of happy-inducing and anger-inducing slides. The subjects reported better than chance feeling happy when making happy faces while viewing anger-inducing slides and angry when making angry expressions while viewing happy-inducing slides (Rutledge and Hupka, 1985). In our hypothesis, vocal self-stimulation is the vocalization equivalent of the facial feedback mechanism with the motor program of vocalization functioning like the contraction or relaxation of a particular set of facial muscles. In our case, however, we have documented how the vocalauditory-endocrine pathway provides the mechanism for vocal selfstimulation effect whereas the mechanism mediating facial feedback has yet to be demonstrated. Since the hypothalamus receives inputs from multiple sensory modalities, a similar pathway may be involved in facial feedback.

VIII. The Forebrain Pathways in the Non-Vocal Learner A widely held view is that the specialized forebrain nuclei of songbirds are developed for vocal learning (Bottjer et al., 1989, Sohrabji, et al., 1990; Doupe, 1993; Brainard and Doupe, 2000). The neural circuitry connecting

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these specialized nuclei form an anterior forebrain pathway (AFP) (Okuhata and Saito, 1987; Doupe and Konishi, 1991; Nottebohm, 1991; Brainard and Doupe, 2000). The AFP is connected to the motor pathway for song production. The motor pathway of songbirds overlaps that of nonvocal learners such as ring doves. The common motor pathway is the connection from the midbrain dorsomedial (DM) nucleus of the ICo complex to the nXIIth motor nuclei (Nottebohm et al., 1976; Cohen, 1983). Recent evidence from ring dove studies suggests, however, that there is also involvement of auditory and forebrain nuclei in vocal communication, implicating AFP-like circuitry in the non-vocal learner. For example, in recordings from the dorsal posterior thalamus (DP), a dorsal thalamic zone (DTZ) nucleus (Ferries, 2001), and a component of AFP within the oscine songbird vocal system, neurons responded selectively to acoustic features of coo songs in the ring dove (Durand and Cheng, unpublished data). Evidence from rock doves further suggests that the DP neurons are polysensory (auditory, visual, and somatosensory) in nature (Korzeniewska and Gunturkun, 1990). This nucleus may be uniquely suited for providing a minute by minute ‘‘summation’’ of somatic information in animals. Therefore, the DP may be involved in providing an internal state to be associated with specific acoustic features in song learning. In this context, it is interesting to note that DP is one of the nuclei Damasio has identified as being involved with ‘‘somatic markers.’’ DP, therefore, is a good candidate for a subcortical structure involved in vocal signal recognition. DP provides information pertaining to the internal states that may be critical in identifying the quality of the singer from the singing. Evidently, female black-capped chickadees (Poecile atricapilla) eavesdrop on males to decide with which male they will copulate (Mennill et al., 2002). High-ranking males lose significant levels of paternity after just six minutes of playback trials of a simulated intruder. It seems presumptuous of the female to switch partners based solely on acoustic information. In truth, according to our model, the female has all the information she needs to make her choice. Emotion-based song recognition would involve a DP-like structure that provides information regarding the internal states (endocrine profile, posture, vocal motor program) of the signaler at the time it produces the signal. As such, females can make a sound assessment of the physical fitness of two competing males. Future study on the effects of DP lesions on vocal communication will be the first step in elucidating the precise role of DP in vocal signals recognition in vocal learners as well as non-vocal learners. The anterior forebrain pathway that is thought to be involved exclusively in the vocal learning of oscine songbirds includes the DP suggesting that emotional state can have access to the song learning


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system. A projection from the midbrain auditory region, the caudomedial nucleus of the torus semicircularis (CM, overlap with mICo) to the DP was confirmed by a tract tracing study in the ring dove (Durand et al., unpublished data) and projections from components of the DP to the anterior neostriatum have been shown in pigeons (Wild, 1987). In male European starlings, Sturnus vulgaris, lesions to the medial preoptic area (POM) of the hypothalamus disrupt some aspects of songs (Riters and Gall, 1999) and seasonal variations in the volume of the POM correlate with seasonal changes in singing (Riters, et al., 2000). Since the POM is likely to be involved in the aromatization (a biochemical process involving the enzyme aromatase) of testosterone (Riters et al., 2001), which is critical for male courtship arousal, these findings also suggest the importance of the emotional state in the song system. Although the precise role of the DP-anterior forebrain pathways in nonvocal learners is not clear, interestingly, the shell region of the auditory thalamus, the Ov shell that sends a projection to the hypothalamus, also projects to the DP. The DP-anterior forebrain pathway is thus connected to the vocal endocrine pathways. Studies of three distantly related groups of birds, oscine songbirds, parrots and hummingbirds show that these birds possess different forebrain specialization but contain a similarly positioned thalamic component. These are the three groups of birds on which vocal learning has been established. Evidently, the DP is the conserved component of vocal learning pathways (Durand et al., unpublished data). In humans, the DP has been implicated in lexical selection (Nadeau and Crosson, 1997). Since the Ov shell-hypothalamus link is involved in repetitive vocal self-feedback, the Ov shell’s connection to the DP suggests that the DP-anterior forebrain pathway may be involved in vocal communication in non-vocal learners as well. Given that non-vocal learners do not learn songs, what function might the DP-anterior forebrain pathways serve in these species? We speculate that they may provide the ‘‘cortical’’ control of vocal production as in the case of audience effects or context dependent vocal responses. Conceptually speaking, this rudimentary form of ‘‘cortical’’ influence on vocal signals may be a special case of a more general cortical influence on basic emotional responses which LeDoux (1996) designated as the ‘‘long loop’’ or ‘‘high road’’ in fear-conditioned response. In contrast to ‘‘short loop’’ mentioned earlier, the ‘‘long loop’’ is long compared to the short loop because the thalamic input is first processed in the sensory cortex before being forwarded to the amygdala for a response. In rats, while a long loop is not required to learn fear conditioning, a long loop is involved in the extinction of an acquired fear response. That is, the cortex is required for rats to learn not to respond to a tone (conditioned stimulus)

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with a freezing response after having experienced tones without being shocked (LeDoux et al., 1986; LeDoux, 1996). The cortex is also involved in learning a fear conditioning task that requires fine-tuned discrimination between conditioning stimuli. For example, rabbits without an auditory cortical area fail to learn fear conditioning that requires distinguishing between two closely related tones, one followed by shock, the other not (Jarrel et al., 1987). Thus, disruption of perceptual responsiveness can affect emotional responding; in this way, cortical structures are involved in emotional learning. Vocal learning, as we have hypothesized, involves an emotional component and as such may be subject to some of the same mechanisms as emotional learning. Vocal signals that involve a ‘‘functionally referential’’ or a context-dependent response may recruit the higher forebrain structures. It would be interesting to determine if lesioning one of the anterior forebrain substrates or severing the DP-anterior forebrain pathway in chickens would abolish their ability to exhibit ‘‘audience effects.’’ In songbirds, the connection of the Ov shell to the AFP through DP provides all the necessary circuitry for learning required for audiovocal communication. Viewed in this way, the difference between vocal and non-vocal learners represents an evolutionary continuum. As more sophisticated vocal instruments evolved, selective pressure may have favored refinement of the rudimentary anterior forebrain pathways that build on pre-existing emotional circuitry. Figure 11 summarizes the neural connections that have been documented in non-vocal learners. Two points can be made about these circuitries. Firstly, it is clear that the system mediating vocalization is connected to the neuroendocrine system. There are several structures serving as an interface between these two systems with the hypothalamus, the amygdala and the dorsal posterior thalamus as likely candidates. Secondly, the neural pathway mediating vocalization does not differ in kind from that of the songbird system. The anterior forebrain pathway once thought to be exclusive to the vocal learner is found in a lessspecialized form in the non-vocal learner. The structures that bridge these two vocal systems are the dorsal posterior thalamus and other nuclei yet to be documented.

IX. Summary As Darwin stated, the vocal signal is emotional expression in a social context. As such, a study of the vocal system outside its social context is not complete. We believe ‘‘emotional sharing’’ provides the means for social context. We hypothesize that emotional sharing is central to the


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Central Pathways for Vocal Communication

Cb

DP Ov Shell PBv nXIIts

ICo Hypo

Av Tn

Fig. 11. Central pathways for vocal communication in a non-vocal learner. A summary diagram of neural pathways implicated in vocal communication of the non vocal-learner. It consists of (1) motor output: ICo to n. XIIts (Nottebohm, et al., 1976; Cohen, 1983); ICo to PBv (Wild and Arends, 1987). (2) endocrine output: The hypothalamus receives inputs from the amygdala pathway (Cheng, et al., 1999) and the vocal self-stimulation pathway (Durand, et al., 1992; Cheng and Zuo, 1994) and (3) vocal signal perception: the hypothalamus (such as specific female-nest-coo-units), the thalamus (Ov shell) that receives both motor inputs (Cheng and Zuo, 1994) and sensory feedback of coo units (Durand et al., 1992), or the dorsal posterior thalamus (DP) that receives Ov shell projections (Durand et al., unpublished data) bodily information including vocal motor program (Damacio, 1999). The connection to the anterior forebrain structures may foretell cortical control of vocalization such as audience effects. Av ventral archistriatum; Cb-cerebellum; DP-dorsal posterior thalamus; Hypohypothalamus; ICo-nucleus intercollicularis; nXIIts-tracheosyringeal motor nucleus.

non-vocal learning system. As a sample experiment, we propose to test this idea with a chick distress call. Furthermore, we espouse the view that the vocal learning system builds upon the non-vocal learning system. We hypothesize that emotional sharing in vocal learning systems is mediated by a motor program through the vocal-auditory-endocrine system. We define this emotion as the endocrine state, posture, and motor program associated with vocalization. Although the concept of an affective state has been explicitly and implicitly accepted, it has yet to be incorporated as a critical variable in experimentation, thus validating or disavowing its role in the song system. Meanwhile, behavioral studies addressing the affective state have yet to make a link to the neurobiology of the song system. We developed the concept of ‘‘emotional sharing’’ primarily on the strength of our anatomical and physiological findings. Our lengthy investigations of the nest coo of

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female doves has led us to discover a vocal self-stimulation mechanism and its underlying neuroanatomical pathways. These findings, together with the structural bridge between the avian amygdala and the vocal-auditoryendocrine pathway, provide the foundation for an emotion-based theory of vocal communication. We postulate a hierarchy of vocalization, vocal learning, and recognition involving three interrelated levels of emotional circuity: (i) amygdala-hypothalamus circuitry at the base, (ii) ‘‘cortical’’ connections at the top, and (iii) dorsal posterior thalamus connections in between. Future studies must define the electrophysiological properties of, and the effects of lesion on, these structures. What are the effects of lesion on the amygdala, the dorsal posterior thalamus, or both, on the affective state, song learning, and song recognition? Are neurons in these structures activated in the form of excitation or inhibition during song learning and song recognition? What is the functional relationship between these structures and song circuitry? Does a vocal-auditory-endocrine system exist in the song bird system? What roles do hormones, particularly steroid hormones, play in the relationship between the affective state and song systems? Comparisons of vocal versus non-vocal learners, and simple versus complex calls, may reveal the nature of emotional involvement in different forms of vocal communication. Acknowledgments I would like to thank my colleagues Drs. Peter Marler, Jay S. Rosenblatt, and Cheryl Harding for their thoughtful contributions to this manuscript. The section on song perception in female birds was inspired by and benefited immensely from Harding’s probing questions and her generosity in sharing information. I alone, however, bear the responsibility for any errors or oversights in the manuscript. I would also like to take this opportunity to thank my daughter, Julie, for her graphics. This work was supported by NIMH NS36924 and a Rutgers Busch Biomedical Research Grant.

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Index

A Ability, lack, 24 Acquisition, 50 Activity coordination, 26 Adult learning, songs, 71 Affective states, 323–326 Agents, 2 Alarm call behavior, 269 Ancestral sedentary population, 177 Animal teams, 17–21 birds, 17–18 carnivores, 19–20 cetaceans, 18–19 primates, 20–21 Annual periodicity, 193 Anthropocentric approach, 271 Aphaenogaster, teams, 16 Apis, teams, 13–14 Audience effects, 296

B Behavioral-constitutional hypothesis, 178, 196–197 Behavioral jump, 177 Behavioral tactics, 108 Biological clocks, 179 Bird estimation of heritabilities and consequences, 201–206, 202t juvenile development, 193–194 molt, 193–194f migration continental drift theory, 177

genetic basis and evolutionary aspect of, 175–229 ice age theory, 177 threshold model, 177 origin of, 177 quantitative genetic analysis, 200–209 reproductive period, 199–200 species, search for and selection of, suitable for testing, 180–183 teams, 17–18 Blackcaps, 180–222 directional choice, 189f European, 188, 199 lifestyles and migration routes of, 183f migratory restlessness, 208f traits, 203–206 nocturnal phases of migratory restlessness, 184f patterns of migratory activity (restlessness), 192f partially migratory, 197f, 217 wintering grounds, 216f

C Calendar reaction, photoperiodically controlled, 183 Calls, 63 alarm, 273f, 274f acoustically distinct, 272 aerial, 271 behavior, 269 male, 283f, 289f 355

356 Calls (continued ) perception, 274 predator-specific, 270 terrestrial, 270 alert, 274 comprehension, 271–291, 297 contact, 274 distress, 326, 329f learning, 70t, 71–72 production, 269, 294, 297 repertoire, 71 structure, 291–294 types, 269 use, 294–296 Canary, domestic, 182 Captivity-raised primates, 267–268 Carnivores, teams, 19–20 Castes, 7 Causal information, 284–286 Cetaceans, teams, 18–19 Circannual rhythmicity, 210–211 rhythms discovery of – the challenge to genetic studies, 179–180, 180f Class, 36 Communication, 297–299 acoustic, 323–236 emotional expression, 324–325 emotional sharing, 326 emotional state as referent, 324 honest states, 324 moto-mimicry, 326 vocal signals, 324–325 direct, 37–38 gestural, 297 primate, 297 system, 272 vocal, 345f Competitive scenarios, 99–101 Continental drift theory, 177 Control mechanisms and evolution, the broad palette of theories on, 176–178 Coo, 309, 315f, 317–320, 318f female nest, 312f, 319f

INDEX

male nest, 311f recognition, 318 Copulatory behavior, 109–111 Copulatory imperative, 96–118 basic considerations, 98–99 competitive scenarios, 99–101 ground rules, 98–99 males, 116–118 mate choice, 116–117 mechanisms of intra-sexual selection, 101–115 paternal care, 115–116 sexual strategies, 118 Cost, 25

D Deer barking, 231; see also, muntjac and territoriality, 234 barks chase, 246 longer loud, 247 call costs of, 259–260 indirect, 260 physiological, 259–260 effects on females, 237–238 production, the source-filter theory of, 241–242 rate and male-male contests, 236–237 long-term, 235 short-term, 235 studies of, 235–238 roars common, 244, 245f deterministic chaos, 2458 lazy bout of red deer, 257f subharmonics, 258 frequencies, formant and fundamental, 257f grunt, 247 harsh, 247

357

INDEX

non-linear phenomena in red deer, 258–259f quantitative studies of filter characteristics in red deer, 252–256 acoustical analyses, 253–254 anatomical analyses, 252–253 descended and mobile larynges in other mammal species, 254–255 evolutionary paths toward laryngeal descent, 254 spectogram of, 255f vocal tract length versus vocal tract shape modulations, 255–256 quantitative studies of source characteristics in red deer, 249–252 acoustic analyses, 250–251 anatomical analyses, 249–250 heritability of FO characteristics in red deer stags, 251–252 interspecific variation in fundamental frequency, 251 research in progress and future directions, 256–260 formant modulation as potential indicator of motivational state, 256–258 rutting, 234–235 acoustic characteristics of, 244–249 fallow deer, 248f-249 red deer, 244–248, 245–246f variation in, 239–240f studies on the acoustic structure of, 238–256 Cervidae, schematic phylogenetic tree for the family, 232f gregarious species, reproductive calls in, 234–256

males anatomy of the vocal apparatus in a fallow, 243f functional anatomy of the vocal apparatus in red and fallow, 242–244 mating calls, 233–234 polygynous, 231, 233 solitary, 232–233 reproductive calls in, 233–234 vocal communication and reproduction in, 231–264 Deterioration of weather in the temperate zone, 177 Directional preference, populationspecific, 185 Direct benefits, 130 Displays, 102–103 Dominance, 105–108 Dominance relationships, 278 Dorylus, teams, 12–13 Duetting species, songbirds, 69–71

E Eciton, teams, 12–13 Ecological knowledge, 278–283 Efficiency, 24 Egalitarianism, 105–108 Emotional circuitry, 337–341 Emotional expression, 324–325 Emotional referent in vocal communication, 326–341 Emotional sharing, 326, 328f, 331–333 Emotional state, 324 Endocrine states, 340f Endogenous annual cycles, 179 periodicity, 180f circannual rhythms, 210 control mechanisms, 178–179 factors, 184 program, 178, 190 time, 183

358

INDEX

Endogenous-genetic control of migration, 210 Evolution and control mechanisms, the broad palette of theories on, 176–178 Exogenous factors, 184, 210 control mechanisms, 178

F Father’s song, 59–60 Fault tolerance, 24–25 Female advertisement, 124–128 auditory signals, 127–128 olfactory signals, 128 proceptive behavior, 126 visual signals, 126–127 Female choice, 49, 128–134 constraints, 119–121 cryptic, 134–136 direct benefits, 130 humans, 132–133 indirect benefits, 130–132 questions for the future, 133–134 Female competition, 136–138 Female counter-strategies, 91 Female follicular growth, 312f Female nest coo, 310–313, 312f, 319f, 320–321 Female perspective, 118–140 Female receptivity, 121–122 Fight of flight mechanism, 327 Follicular growth, 311f, 312f, 314, 315f Forebrain pathways in the non-vocal learner, 341–344 Formants, 241

hypothesis, 178 Genetically integrated syndromes, 206 Geographic song variation, 56–58 Gestural communication, 297 Global warming, 221 Glottal wave, 241–242f; see also, source signal Group tasks, 3, 3t, 4 why use? 24–25 Groupwork, 31–32, 36 Goals, 39 Goal orientation, mechanisms of, 192

H Habituation-dishabituation technique, 275 Harem, 120 Heritability definition of, 201 estimates for migratory traits, 202t Home range, 99 Honest states, 324 Human female choice, 123–133 language areas, 266 teams, 25–28, 28t coordination, 26 comparison to insect teams, 28t definitions, 27t self-organizing, 27–28 what constitutes? 26–27 Hypothalamus, 311, 322f endocrine secretions, 312

I G Genetic control, 183–200 approach, 183–184

Ice age theory, 177 Indirect benefits, 130–132 Individual tasks, 3t, 4 Individual recognition, 36–37 Inherited spatiotemporal program, 191

359

INDEX

Insect teams, 5–17, 28t Instinct migrants, 184 Instinctive behavior, 184 Interdependence, 26 Interindividual differences, 36 Internal state, 334–337 Intermediate orientation, 188–189f Internal calendars, 179 Inter-sexual selection, 88 Intra-sexual selection, 88, 101–115 alternative tactics, 108–109 copulatory behavior, 109–111 displays, 102–104 dominance, 105–108 egalitarianism, 105–108 mate detection, 101–102 other postcopulatory mechanisms, 114–115 physical superiority, 104–105 physiological suppression, 108 signals, 102–104 sperm competition, 111–114

L Language evolution, 265–266 neutral basis, 266–267 specific acoustic regularities, 268 Leader, 38–39 Learning, sex differences, 73–77 Leptothorax slave-making ants, teams, 14–15 Lifetime reproductive success, 145–146 Linguistic capacities in non-human primates, 267–271 captivity-raised primates, 267–268 common critique, 260–271 natural populations, 268–269

M Male courtship, 312f Male-male competition, 49 Male nest coo, 311f Male perspective, 96–118 Mate choice, 116–117 Mate detection, 101–102 Management, 41 Mate choice, 59–60 Menstrual cycle, 132 Mental processes underlying call comprehension, 271–291 ecological knowledge, 278–283 mental representations, 271–278 social knowledge, 278–283 Migrants instinct, 184 intercontinental, 219 interaction with other annual cycles, 198–200 long-distance, 219 nocturnal, 182, 186 phenotypic, 207 selective breeding of, 197f weather, 184 Migration date of departure, 185–186 dispersal, 177 distance, 190 endogenous-genetic control of, 210 new theory of the evolution, control and adaptability of avian, 211–213 obligate, 177–178 partial, 196, 198, 201 outlook, 221–223 partial, 196–198 distribution and key role of, 209–211 rapid changes due to selection and microevolution, 213–221 experimental studies, 214–218 observations so far, 213–214 predictions, 218–221 syndrome, 185, 188, 201, 223

360

INDEX

Migration (continued ) genetic correlations among, 206–209 summary, 223–224 termination of and goal finding, the vector-navigation hypothesis, 189–192 Migrating while seated, 183 Migratoriness, 201, 207 conversion from to more sedentariness, 219, 222 decreasing, 213–214 increasing, 214 Migratory activity, 183, 185, 190–192f, 201 temporal distribution of, 191 behavior, 183–185, 188 mode of inheritance, 200–201 direction, 186–189 disposition and prerequisites, 194–195 drive, 183 restlessness, 183–184f, 189–190, 192f, 205f, 208f caged birds vs. wild conspecifics, 186 traits, genetic correlations among, 206–209 Molt juvenile, 193–194f processes of, 198–199 Monandry, 119 Monomorphic society, 7 Moose, mating calls of, 233–234 Morphological tactics, 108 Moto-mimicry, 326 Motor theory of vocal signals, 329–331 Muntjac, 231; see also, barking deer Indian, 233 Mutations, 177 Myrmicaria, teams, 10–12

N Navigation genuine, 192 star–pattern, 190

Neuroendocrinological sex differences, 73–744 Nocturnal migrants, 182, 186 restlessness, 183–184f Non-migrants phenotypic, 207 selective breeding of, 197f Non-oscine birds, 72–73

O Objective, common, 26 Oecophylla, teams, 8–10, 9f Offspring investment, 138–140 Ontogenetic ritualization, 297 Orientation behavior, 201 intermediate, 188–189f Ornithology, 176 Oscine songbirds, 72 Ovulation, unpredictable, 122–124

P Partitioning, 30–31 Partitioned task, 3t, 4 Paternal care, 115–116 Paternal lines, 52 Paternity, 118–140 Perceptual fine tuning, song, 60–61 Perceptual processing, 272 Permanent association, 100 Pheidole, teams, 15 Pheidologeton, teams, 15–16 Phenotypic migrants, 207 non-migrants, 207 plasticity, 178, 217 variation, 221 Physical superiority, 104–105 Physiological suppression, 108 Playback study, 276f, 288f

361

INDEX

Polyandry, 119 Polygenic trait, 185 Polymorphic society, 7 Population variation in song, 58–59 Post-copulatory mechanisms, 114–115 Predator vocalization, 274f Preference, song, 52, 56–60 early exposure, 53t–55t Primates captivity raised, 267–268 cognition, 268 mating systems, 97t non-human, 265–307 linguistic capacities, 267–271 selection in relation to sex, 87–172 causes, mechanisms, and consequences, 88–923 introduction, 87–88 teams, 20–21 Prime-probe procedure, 275, 277f Proceptive behavior, 126 Production learning, song, 61 Protomognathus, teams, 14–15

R Receptive periods, 122 Recognition, song, 52–56 Redstarts, 182, 201 common and black, 182, 186, 187f, 193–195 body mass development, 195f Redundancy, 24–25 Repetitive vocalization, 337–341 Reproductive strategies, conflict, 140–142 Reproductive success, 97t, 145–146 Ring dove story, 309 introduction, 309–310 Robins, American or European, 178 Robot teams, 21–25 cooperative system, 23 examples, 22–23 why use? 24–25

Robotics, 41 Rosefinch, scarlet, 182

S Scientia amabilis, 176 Screams, 280f chimpanzees, 281f, 282–283 leopard, 281f Sedentariness, 201, 207 conversion from migratoriness to, 219, 222 Sex differences, 73–77 learning abilities, 74–76 neuroendocrinological, 73–74 sensitive phases, 74–76 sex-specific lineages, 76–77 Sex ratio manipulation, 138–140 Sexual activity, timing, 121–124 female receptivity, 121–122 lengthened receptive periods, 122 seasonality, 121–122 synchrony, 121–122 unpredictable ovulation, 122–124 Sexual selection, 87–172, 97t causes, 88–92 consequences, 89, 93t–94t future directions, 143–144 broader species representation, 146–147 experimental approaches, 145 interdisciplinary studies, 144–145 lifetime reproductive success, 145 overlaying strategies, 144 mechanisms, 89, 93t–94t non-primates, 143 primates, 143 outcomes, 92 relevance of primates, 92–96 Sexual strategies female primates, 140 male primates, 118 Short loops, 339f Signal, 102–103 acoustic, 103

362

INDEX

Signal (continued ) auditory, 127–128 culturally transmitted mating, 50 function, 63 mate attracting, 49 olfactory, 128 physical characteristics, 63 referential, 265–307, 269 territorial, 49 visual, 126–127 vocal, 329–331 Signaler, 291 Skills, 36 Social intelligence, 297–299 knowledge, 278–283 monogamy, 119 Sociobiology, 41 Song, 63 acquisition, 50 impoverished, 64–66 learning, 64–71 adult, 71 developmental and experimental evidence, 67t–68t neuroendocrinological sex differences, 73–74 mate attracting signal, 49 models, 64–66 perception, 61–63 perceptual fine tuning, 60–61 preference, 52 production, 61–63 recognition, 52–56 sexual selection, 49 sharing, male and female, 64 territorial signal, 49 tutoring experiments, 66–69 Songbirds duetting species, 69–71 female, 29–86 introduction, 49–51 sex differences is learning, 73–77 vocal learning in non-oscine birds, 72–73 vocal perception learning, 51–63

vocal production learning, 63–72 summary, 77–78 granivorous, 182 Source-filter theory of call production, 241–242f Source signal, 241; see also, glottal wave Sperm competition, 111–114 Star-pattern navigation, 190 Structural homologues, 266, 267 Subtasks, 3, 10t–11t group, 40 individual, 40 Superefficiency, 13, 32 Super short loops, 339f Syntactic information, 287–291

T Tasks, 37 complex, 8 group, 3t, 4 individual, 3t, 4 partitioned, 3t, 4 structure, 5, 10t–11t subtasks, 10t–11t team, 3t, 4, 16, 37 types, 2–5 Team, 1 attributes, 28t redefine, 5–8 size, 28–29 social insect, 5–17 tasks, 3t, 4 why use? 24–25 Teamwork 1–48 boundaries, 30–32 conclusions, 39–41 definition, 2 efficient, 37–38 human 25–28 introduction, 1–5 misconceptions, 35–39 other animal, 17–21 robots, 21–25

363

INDEX

social insect, 5–17 summary, 41 team size, 28–35 testing, 30–35 borderline cases, 30–32 case study, 34–35 experiments, 32–34 Thermoregulation, 193 Threshold model of bird migration, 177 Tutoring experiments, songs, 66–69

V Vector-navigation hypothesis, termination of migration and goal finding, 189–192 Vocal auditory-endocrine feedback system, 309 communication and reproduction in deer, 231–264 courtship display, 309 learning, 331–333

motor program, 334–337 production and perception learning in female songbirds, 49–86 recognition, 326 responses of female Diana monkeys, 274f, 285f, 286f self-stimulation, 309–353, 326–241, 329–331 Vocal-endocrine links, 337–341 cross species comparisons, 321–323 female, 313–320 behavior studies, 313–315 neurophysiological validation, 315–320

W Warbler program, 180 Weather migrants, 184 Wing whirring, 190


Contents of Previous Volumes

The Evolution of Courtship Behavior in Newts and Salamanders T. R. HALLIDAY

Volume 18 Song Learning in Zebra Finches (Taeniopygia guttata): Progress and Prospects PETER J. B. SLATER, LUCY A. EALES, AND N. S. CLAYTON

Ethopharmacology: A Biological Approach to the Study of Drug-Induced Changes in Behavior A. K. DIXON, H. U. FISCH, AND K. H. MCALLISTER

Behavioral Aspects of Sperm Competition in Birds T. R. BIRKHEAD

Additive and Interactive Effects of Genotype and Maternal Environment PIERRE L. ROUBERTOUX, MARIKA NOSTEN-BERTRAND, AND MICHELE CARLIER

Neural Mechanisms of Perception and Motor Control in a Weakly Electric Fish WALTER HEILIGENBERG

Mode Selection and Mode Switching in Foraging Animals GENE S. HELFMAN

Behavioral Adaptations of Aquatic Life in Insects: An Example ANN CLOAREC

Cricket Neuroethology: Neuronal Basis of Intraspecific Acoustic Communication FRANZ HUBER

The Cicadian Organization of Behavior: Timekeeping in the Tsetse Fly, A Model System JOHN BRADY

Some Cognitive Capacities of an African Grey Parrot (Psittacus erithacus) IRENE MAXINE PEPPERBERG

Volume 19 Volume 20 Polyterritorial Polygyny in the Pied Flycatcher P. V. ALATALO AND A. LUNDBERG

Social Behavior and Organization in the Macropodoidea PETER J. JARMAN

Kin Recognition: Problems, Prospects, and the Evolution of Discrimination Systems C. J. BARNARD Maternal Responsiveness in Humans: Emotional, Cognitive, and Biological Factors CARL M. CORTER AND ALISON S. FLEMING 365

The t Complex: A Story of Genes, Behavior, and Population SARAH LENINGTON The Ergonomics of Worker Behavior in Social Hymenoptera PAUL SCHMID-HEMPEL

366

CONTENTS OF PREVIOUS VOLUMES

‘‘Microsmatic Humans’’ Revisited: The Generation and Perception of Chemical Signals BENOIST SCHAAL AND RICHARD H. PORTER

Parasites and the Evolution of Host Social Behavior ANDERS PAPE MØLLER, REIJA DUFVA, AND KLAS ALLANDER

Lekking in Birds and Mammals: Behavioral and Evolutionary Issues R. HAVEN WILEY

The Evolution of Behavioral Phenotypes: Lessons Learned from Divergent Spider Populations SUSAN E. RIECHERT

Volume 21

Proximate and Developmental Aspects of Antipredator Behavior E. CURIO

Primate Social Relationships: Their Determinants and Consequences ERIC B. KEVERNE The Role of Parasites in Sexual Selection: Current Evidence and Future Directions MARLENE ZUK Conceptual Issues in Cognitive Ethology COLIN BEER Response in Warning Coloration in Avian Predators W. SCHULER AND T. J. ROPER Analysis and Interpretation of Orb Spider Exploration and Web-Building Behavior FRITZ VOLLRATH Motor Aspects of Masculine Sexual Behavior in Rats and Rabbits GABRIELA MORALI AND CARLOS BEYER On the Nature and Evolution of Imitation in the Animal Kingdom: Reappraisal of a Century of Research A. WHITEN AND R. HAM

Volume 22 Male Aggression and Sexual Coercion of Females in Nonhuman Primates and Other Mammals: Evidence and Theoretical Implications BARBARA B. SMUTS AND ROBERT W. SMUTS

Newborn Lambs and Their Dams: The Interaction That Leads to Sucking MARGARET A. VINCE The Ontogeny of Social Displays: Form Development, Form Fixation, and Change in Context T. G. GROOTHUIS

Volume 23 Sneakers, Satellites, and Helpers: Parasitic and Cooperative Behavior in Fish Reproduction MICHAEL TABORSKY Behavioral Ecology and Levels of Selection: Dissolving the Group Selection Controversy LEE ALAN DUGATKIN AND HUDSON KERN REEVE Genetic Correlations and the Control of Behavior, Exemplified by Aggressiveness in Sticklebacks THEO C. M. BAKKER Territorial Behavior: Testing the Assumptions JUDY STAMPS Communication Behavior and Sensory Mechanisms in Weakly Electric Fishes BERND KRAMER


Volume 24 Is the Information Center Hypothesis a Flop? HEINZ RICHNER AND PHILIPP HEEB Maternal Contributions to Mammalian Reproductive Development and the Divergence of Males and Females CELIA L. MOORE

367

An Overview of Parental Care among the Reptilia CARL GANS Neural and Hormonal Control of Parental Behavior in Birds JOHN D. BUNTIN Biochemical Basis of Parental Behavior in the Rat ROBERT S. BRIDGES

Cultural Transmission in the Black Rat: Pine Cone Feeding JOSEPH TERKEL

Somatosensation and Maternal Care in Norway Rats JUDITH M. STERN

The Behavioral Diversity and Evolution of Guppy, Poecilia reticulata, Populations in Trinidad A. E. MAGURRAN, B. H. SEGHERS, P. W. SHAW, AND G. R. CARVALHO

Experiential Factors in Postpartum Regulation of Maternal Care ALISON S. FLEMING, HYWEL D. MORGAN, AND CAROLYN WALSH

Sociality, Group Size, and Reproductive Suppression among Carnivores SCOTT CREEL AND DAVID MACDONALD Development and Relationships: A Dynamic Model of Communication ALAN FOGEL Why Do Females Mate with Multiple Males? The Sexually Selected Sperm Hypothesis LAURENT KELLER AND HUDSON K. REEVE

Maternal Behavior in Rabbits: A Historical and Multidisciplinary Perspective ´ LEZ-MARISCAL GABRIELA GONZA AND JAY S. ROSENBLATT Parental Behavior in Voles ZUOXIN WANG AND THOMAS R. INSEL Physiological, Sensory, and Experiential Factors of Parental Care in Sheep ´ VY, K. M. KENDRICK F. LE E. B. KEVERNE, R. H. PORTER, AND A. ROMEYER

Cognition in Cephalopods JENNIFER A. MATHER

Socialization, Hormones, and the Regulation of Maternal Behavior in Nonhuman Simian Primates CHRISTOPHER R. PRYCE

Volume 25

Field Studies of Parental Care in Birds: New Data Focus Questions on Variation among Females PATRICIA ADAIR GOWATY

Parental Care in Invertebrates STEPHEN T. TRUMBO Cause and Effect of Parental Care in Fishes: An Epigenetic Perspective STEPHEN S. CRAWFORD AND EUGENE K. BALON Parental Care among the Amphibia MARTHA L. CRUMP

Parental Investment in Pinnipeds FRITZ TRILLMICHx Individual Differences in Maternal Style: Causes and Consequences of Mothers and Offspring LYNN A. FAIRBANKS

368


Mother–Infant Communication in Primates DARIO MAESTRIPIERI AND JOSEP CALL Infant Care in Cooperatively Breeding Species CHARLES T. SNOWDON Volume 26 Sexual Selection in Seawood Flies THOMAS H. DAY AND ´ S. GILBURN ANDRE Vocal Learning in Mammals VINCENT M. JANIK AND PETER J. B. SLATER

Volume 27 The Concept of Stress and Its Relevance for Animal Behavior DIETRICH VON HOLST Stress and Immune Response VICTOR APANIUS Behavioral Variability and Limits to Evolutionary Adaptation P. A. PARSONS Developmental Instability as a General Measure of Stress ANDERS PAPE MØLLER

Behavioral Ecology and Conservation Biology of Primates and Other Animals KAREN B. STRIER

Stress and Decision-Making under the Risk of Predation: Recent Developments from Behavioral, Reproductive, and Ecological Perspectives STEVEN L. LIMA

How to Avoid Seven Deadly Sins in the Study of Behavior MANFRED MILINSKI

Parasitic Stress and Self-Medication in Wild Animals G. A. LOZANO

Sexually Dimorphic Dispersal in Mammals: Patterns, Causes, and Consequences LAURA SMALE, SCOTT NUNES, AND KAY E. HOLEKAMP

Stress and Human Behavior: Attractiveness, Women’s Sexual Development, Postpartum Depression, and Baby’s Cry RANDY THORNHILL AND F. BRYANT FURLOW

Infantile Amnesia: Using Animal Models to Understand Forgetting MOORE H. ARNOLD AND NORMAN E. SPEAR Regulation of Age Polyethism in Bees and Wasps by Juvenile Hormone SUSAN E. FAHRBACH Acoustic Signals and Speciation: The Roles of Natural and Sexual Selection in the Evolution of Cryptic Species GARETH JONES

Welfare, Stress, and the Evolution of Feelings DONALD M. BROOM Biological Conservation and Stress HERIBERT HOFER AND MARION L. EAST

Volume 28

Understanding the Complex Song of the European Starling: An Integrated Ethiological Approach MARCEL EENS

Sexual Imprinting and Evolutionary Processes in Birds: A Reassessment CAREL TEN CATE AND DAVE R. VOS

Representation of Quantities by Apes SARAH T. BOYSEN

Techniques for Analyzing Vertebrate Social Structure Using Identified


Individuals: Review and Recommendations HAL WHITEHEAD AND SUSAN DUFAULT Socially Induced Infertility, Incest Avoidance, and the Monopoly of Reproduction in Cooperatively Breeding African Mole-Rats, Family Bathyergidae NIGEL C. BENNETT, CHRIS G. FAULKES, AND JENNIFER U. M. JARVIS Memory in Avian Food Caching and Song Learning: A General Mechanism or Different Processes? NICOLA S. CLAYTON AND JILL A. SOHA Long-Term Memory in Human Infants: Lessons in Psychobiology CAROLYN ROVEE-COLLIER AND KRISTIN HARTSHORN Olfaction in Birds TIMOTHY J. ROPER Intraspecific Variation in Ungulate Mating Strategies: The Case of the Flexible Fallow Deer SIMON THIRGOOD, JOCHEN LANGBEIN, AND RORY J. PUTMAN

Volume 29 The Hungry Locust STEPHEN J. SIMPSON AND DAVID RAUBENHEIMER Sexual Selection and the Evolution of Song and Brain Structure in Acrocephalus Warblers CLIVE K. CATCHPOLE Primate Socialization Revisited: Theoretical and Practical Issues in Social Ontogeny BERTRAND L. DEPUTTE

369

Ultraviolet Vision in Birds INNES C. CUTHILL, JULIAN C. PARTRIDGE, ANDREW T. D. BENNETT, STUART C. CHURCH, NATHAN S. HART, AND SARAH HUNT What Is the Significance of Imitation in Animals? CECILIA M. HEYES AND ELIZABETH D. RAY Vocal Interactions in Birds: The Use of Song as a Model in Communication DIETMAR TODT AND MARC NAGUIB

Volume 30 The Evolution of Alternative Strategies and Tactics H. JANE BROCKMANN Information Gathering and Communication during Agonistic Encounters: A Case Study of Hermit Crabs ROBERT W. ELWOOD AND MARK BRIFFA Acoustic Communication in Two Groups of Closely Related Treefrogs H. CARL GERHARDT Scent-Marking by Male Mammals: Cheat-Proof Signals to Competitors and Mates L. M. GOSLING AND S. C. ROBERTS Male Facial Attractiveness: Perceived Personality and Shifting Female Preferences for Male Traits across the Menstrual Cycle IAN S. PENTON-VOAK AND DAVID I. PERRETT The Control and Function of Agonism in Avian Broodmates HUGH DRUMMOND

370


Volume 31

Volume 32

Conflict and Cooperation in a Female-Dominated Society: A Reassessment of the ‘‘Hyperaggressive’’ Image of Spotted Hyenas MARION L. EAST AND HERIBERT HOFER

Self-Organization and Collective Behavior in Vertebrates IAIN D. COUZIN AND JENS KRAUSE

Birdsong and Male–Male Competition: Causes and Consequences of Vocal Variability in the Collared Dove (Streptopelia decaocto) CAREL TEN CATE, HANS SLABBEKOORN, AND MECHTELD R. BALLINTIJN Imitation of Novel Complex Actions: What Does the Evidence from Animals Mean? RICHARD W. BYRNE Lateralization in Vertebrates: Its Early Evolution, General Pattern, and Development LESLEY J. ROGERS Auditory Scene Analysis in Animal Communication STEWART H. HULSE Electric Signals: Predation, Sex, and Environmental Constraints PHILIP K. STODDARD How to Vocally Identify Kin in a Crowd: The Penguin Model THIERRY AUBIN AND PIERRE JOUVENTIN

Odor-Genes Covariance and Genetic Relatedness Assessments: Rethinking Odor-Based Recognition Mechanisms in Rodents JOSEPHINE TODRANK AND GIORA HETH Sex Role Reversal in Pipefish ANDERS BERGLUND AND GUNILLA ROSENQVIST Fluctuating Asymmetry, Animal Behavior, and Evolution JOHN P. SWADDLE From Dwarf Hamster to Daddy: The Intersection of Ecology, Evolution, and Physiology That Produces Paternal Behavior KATHERINE E. WYNNE-EDWARDS Paternal Behavior and Aggression: Endocrine Mechanisms and Nongenomic Transmission of Behavior CATHERINE A. MARLER, JANET K. BESTER-MEREDITH, AND BRIAN C. TRAINOR Cognitive Ecology: Foraging in Hummingbirds as a Model System SUSAN D. HEALY AND T. ANDREW HURLY

Advances in the Study of Behavior, Volume 33 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 34 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 27 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 38 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 30 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 35 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 36 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 32 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 29 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 37 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 23 (Advances in the Study of Behavior)

Advances in the Study of Behavior, Volume 25: Parental Care

Advances in the Study of Behavior, Volume 43

Advances in The Study of Behavior, Volume 18

Advances in the Study of Behavior, Volume 14

Advances in the Study of Behavior, Volume 6

Advances in the Study of Behavior, Volume 17

Advances in the Study of Behavior, Volume 24

Advances in The Study of Behavior, Volume 15

Advances in the Study of Behavior, Volume 21