Helping Communal Breeding in Birds: Ecology and Evolution [Course Book ed.] 9781400858569

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Helping and Communal Breeding in Birds

MONOGRAPHS IN BEHAVIOR AND ECOLOGY Edited by John R Krebs and Tim Clutton-Brock Five New World Primates A Study in Comparative Ecology, by John Terborgh Reproductive Decisions An Economic Analysis of Gelada Baboon Social Strategies, by R I M Dunbar Honeybee Ecology A Study of Adaptation in Social Life by Thomas D Seeley Foraging Theory, by David W Stephens and John R Krebs Helping and Communal Breeding in Birds Ecology and Evolution, by Jerrarn L Brown

Helping and Communal Breeding in Birds Ecology and Evolution JERRAM L BROWN Princeton University Press Princeton. New Jersey

Copyright © 1987 by Princeton University Press Published by Princeton University Press 41 William Street Princeton New Jersey 08540 In the United Kingdom Princeton University Press Guildford Surrey All Rights Reserved Library of Congress Cataloging in Publication Data will be found on the last printed page of this book

ISBN 0 691 08447 5 0 691 08448 3 (pbk) This book has been composed in Lasercomp Times Roman and Univers Med 689 Clothbound editions of Princeton University Press books are printed on acid free paper and binding materials are chosen for strength and durability Paperbacks although satisfactory for personal collections are not usually suitable for library rebinding Printed in the United States of America by Princeton University Press Princeton New Jersey

T o m y kin a n d their kin

Contents

Preface

xm

Acknowledgments

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1

Why Study Helping Behavior?

3

2.

The Discovery of Helping Behavior and a Classification of Avian Communal Breeding Systems

8

The Pre color banding Era The Advent of Color-banding Communal vs Colonial Social Systems A Classification of Avian Communal Breeding Systems The Number of Communally Breeding Species Multiple Routes to Avian Communal Breeding Nontraditional or Nominal Helping Is Helping A d a p t i v e ' Grades and Contexts of Helping Conclusions

o

4

Climate, Geography, and Taxonomy

9 10 13 15 17 25 26 29 30 33

34

Taxonomy Geographic Distribution of Communal Breeding Correlations w i t h Climate Avian Communal Breeding in Australia Permanent Residency and the Surplus Conclusions

34 36 38 39 40 43

Elements of Inclusive Fitness Theory for Field Studies

45

The Predominance of Individual Selection The Difference between Classical and Inclusive

45

Fitness The Relative Fitness of Strategies Double A c c o u n t i n g Altruism and Mutualism Conclusions

46 51 56 58 61

VIM

0

•

CONTENTS

Delayed Breeding Sets the Stage for Helping Three Basic Questions W h y Delay Breeding? The Skill Hypothesis Territorial Behavior Habitat Saturation The Role of the Environment Insufficient Labor Force Sex Ratio Dangerous Dispersal Altruism and Parental Manipulation Falsifiability Failed Breeders Age of Role Shift from Nonbreeder to Breeder Conclusions

D

Reduced Dispersal Sets the Stage for Helping Population Consequences of Dispersal Strategies Waiting for Alpha General Advantages of Staying Home The Predispersal Period Prolonged Immaturity Dispersal Strategies Conclusions

/

Territorial Inheritance as Parental Facilitation Delayed Dispersal in Group territorial Birds The Trend to Greater Parental Involvement Colonial and Wife-sharing Systems A Model of Parental Facilitation Conclusions

O

Mutualism, Cost-sharing, and Group Size Group Size May Depend upon Individual Energy Budgets A Threshold of Sociality Optimal Unit Size for an Individual in a Cooperative Social Unit Dominants and Subordinates May Differ in Optimal Unit Size Vigilance and Risk Dilution A Key Factor for Group Territoriality is Associated w i t h Reproduction Why Are Some Species Group-territorial and Others Not?

62 62 64 65 70 75 80 81 83 83 86 87 87 89

91 91 93 94 96 101

102 102 106 108 109 115

116 116 118 119 121 122 122 125

CONTENTS

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ix Susceptibility to Resource Depletion Has Been Overlooked Practical Implications of the Model Ecological Conflict between Dominant and Subordinate Group size Decisions in a Game theoretic Context Conclusions

c)

I 0

1 1

129 130 131

Mutualistic Mating Systems Polyandry and Uncertain Paternity

132

Mating Systems of Communal Birds Polyandrous Communal Groups Richness of Food S u p p l y ' Skua Variance in Food Intake Hawks Brotherly Love among Native Hens The Undefendabihty of Female Dunnocks Female Miners Sell Sex for Paternal Care Conclusions

132 135 135 136 138 142 147 152

Mutualistic Mating Systems Joint Nesting and Uncertain Maternity

154

Crossing the Polygynandry Threshold w i t h the Acorn Woodpecker Polygyny in Magpie Geese Semipromiscuous Monogamy in Ostriches Gang Warfare among the Gallmules Joint Nesting w i t h Monogamy in Anis Km Selection in Nest-sharing Systems Conclusions

154 160 161 162 163 166 167

Does Helping Really Benefit the Helped?

169

Effects on Reproductive Success Controversies A Strong inference Experiment Mechanisms of the Helper Effect Parental Facilitation Conclusions

1 Z.

126 127

The Genetic Structure of Social Units Age Structure Relatedness in Singular breeding Species Is It High Enough? Relatedness in Nest sharing Species H o w Low Can It Go? Relatedness under Plural Breeding w i t h Monogamy Is Km Recognition Necessary for Kin Selection? Inbreeding

170 173 178 180 187 188

190 191 196 201 202 204 206

x

1 o

1 4

I D

CONTENTS

Kin Selection as Group Selection Conclusions

209 213

Indirect Selection for Helping

215

Estimates of Indirect Fitness by Age Feeding Preference and Effort A Test of Indirect Selection Conclusions

21 5

Direct Fitness, Mutualism, and Reciprocity

224

A Helping Game between Breeders Direct Benefits of Nonbreeding and Nondispersal Direct Benefits of Alloparental Care Learning Generational Mutualism The Augmentation Hypothesis in the Scrub Jay The Augmentation Hypothesis of Reciprocity in the Green Woodhoopoe "Reciprocity" in Other Species Social Bonding as Mutualism Other Direct Advantages for Nonbreeding Helpers Conclusions

225 234 239 240 242

Parent-Offspring Relationships Donor Recipient Conflict Vehrencamp's Suppression Models Species Differences in Patterns of Fitness Variability Variance Utilization and Variance Enhancement Conclusions

1 D

Infanticide. Dominance, and Destructive Behavior Nest Robbery by Jays Infanticide by Anis and Woodpeckers Behavioral Dominance Conclusions

I /

Diet and Group Territoriality Why Are Nectar Feeders Not Cooperative? Why Are Ommvores More Likely To Have Permissive Food-Cost Functions? Why Is Helping More Common in the Tropics and Australia? Conclusions

1 O

Synthesis Natural-History Correlates The Three Main Questions

220 223

245 246 247 248 249

250 251 255 256 259 263

265 265 266 267 269

270 270 272 274 274

276 276 277

CONTENTS • xi Why Delay Breeding? Two Kinds of Social System and Two Kinds of Km Selection How Important Is Indirect Selection? Conflict within Groups Alloparenting in Nuclear family Systems Reciprocal Alloparenting in Plural breeding Systems Levels and Phases Kin Selection and the Scientific Method

278 279 280 281 282 286 287 287

Appendix

291

Annotated Glossary

297

Literature Cited

309

Author Index

337

Taxonomic Index

343

Subject Index

352

Preface

In the early 1960s biologists began to realize that not only morphological structures but also social relationships and species-typical patterns of sociality were the product of natural selection. This was reflected in the first comparative studies of social organization in relation to environment (e.g., Orians, 1961; Crook, 1963) and in early cost-benefit natural-selection models for social behavior (e.g., Brown, 1964; Hamilton, 1964). The fundamental realization of the adaptiveness of social behavior was an impetus for the subsequent birth and growth of sociobiology and behavioral ecology in the 1970s. In surveying a small but active part of these largely overlapping fields this book reflects their recent history. Acts of apparent altruism or cooperation by animals, such as helping behavior in nesting birds and in insects, have puzzled thoughtful people for ages and have stimulated recent advances in evolutionary theory. Outstanding among these are inclusive fitness theory (Hamilton, 1964) and, to a lesser extent, ESS (evolutionarily stable strategy) theory (Maynard Smith and Price, 1973). As observers of birds and mammals became aware in the early 1970s of the relevance of these theories to helping behavior, more and more of them undertook field studies to test predictions derived from the new theories. The number of persons studying communally breeding birds has increased from perhaps 4 or 5 in the 1960s (Skutch, 1961a; Brown, 1963a; Carrick, 1963; Rowley, 1965a,b) to 50 or more by 1985. Accordingly, there has been an explosion in the number of published studies of helping behavior based on field work in nature. On the theoretical side there has also been a great increase in the number of papers and books on altruism and mutualism (reviewed in Michod, 1982; D. S. Wilson, 1983). It is no longer possible for a textbook account or even a normal review paper to do justice to the literature devoted to these basic questions in evolutionary biology. This book is, therefore, intended as an overview of helping and communal social organizations for persons who require more coverage than can be given in a journal review article but who have not the time or inclination to read the extensive original sources. Although the main goal of this book is to integrate fact and theory from a wide array of sometimes obscure papers already in the literature, considerable new material has been included. Why is such a lengthy overview needed? Firstly, reviews published through 1985 are incomplete or already out of date. Furthermore, there

xiv • PREFACE

has been no thorough and detailed review. Secondly, major advances involving theory and field work which promise to alter the field significantly appeared in 1984 and 1985. Thirdly, where anarchy and uninformed emotion once prevailed, several unifying themes are now solidifying. Fourthly, there has been some misunderstanding of basic concepts and of the implications of particular findings, not to mention semantic confusion. This noise factor has been magnified by unstable terminology, and by the deleterious effects of the "method of advocacy" (explained in E. O. Wilson, 1975). In this book a special effort is made to employ the method of alternative working hypotheses (Chamberlin, 1897, a paper that every graduate student should read) and to avoid one-sided advocacy. Following Popperian methods, hypotheses should be capable of being falsified by empirical test. Controversies will be subjected to this approach. The scientific terms used in this book are based wherever possible on original sources, such as Hamilton (1964) for altruism, Maynard Smith (1964) for kin selection, and Skutch (1935, 1961a) for helping. Since some writers and reviewers have not used these terms in their original sense, the original definitions may be unfamiliar to some readers. Consequently, I have been liberal in quoting sources and have supplied detailed justifications for my choices of controversial terms in the text and glossary. Lastly, it is probably unnecessary for me to say that some of the issues discussed in this book have been controversial for a decade or more, especially that of the importance of what has been too loosely called kin selection and is more accurately termed indirect selection. It is important that both sides of these debates be presented. Since some of the recent literature has emphasized the anti-indirect-selection position, it is especially important that this issue be re-examined more critically and that a fair statement of alternative views be given. A consensus in this field is not yet in sight, but it is my hope that this book will restore a more balanced perspective. The text uses the English names of animals. Scientific names of species with helpers are listed in Table 2.2. For other species, scientific names are provided when the species is first mentioned. The mathematical symbols used are defined in each chapter as they appear. They are consistent and nonoverlapping within a chapter. Some symbols are not consistent between chapters because (1) they have been drawn from many different published works by various authors, (2) where possible I have retained the original symbolism, especially to conform with the original figures reproduced here, (3) some overlap is unavoidable because of the large number of symbols needed and the small number available on standard word processors, and (4) the symbols for a word are easier to remember when the first letter of that word is used. For example,

PREFACE . xv

in Chapter 8 it is convenient to use D for defense costs, since it is not used for donor; and in Chapter 14 it is convenient to employ D to symbolize donor, since defense costs are not mentioned. J.L.B. December 31, 1985

Acknowledgments

In twenty-seven years of studying communally breeding birds I have received aid from many people. One person has stood by me, always ready to help, for this entire period—my wife, Esther R. Brown. She has helped in every imaginable way, in field observations, in processing and analyzing data, in preparation of manuscripts, and in matters of home, family, and university life. In particular, thanks to her energy and efficiency in processing this manuscript, it proved possible to have it printed by computer and sent for private reviews (March 1985) within eleven months of the decision to write the book, April 1984. My own understanding of communal birds has profited greatly from field experience around the world with many of the researchers whose work is featured in this book. For generously showing me their species under natural conditions on their study areas I thank J. Counsilman and D. Dow (Australia), R. Hegner, D. Ligon, S. Ligon, and D. Lewis (Africa), R. Ali (India), H. Bell (New Guinea), S. Yamagishi (Japan), and S. Strahl (Venezuela). For discussion of relevant theoretical constructs I thank W. D. Hamilton, J. Maynard Smith, R. Michod, and D. S. Wilson. I have been fortunate in being able to draw on help from several biologists who have provided mathematical models or helped me with my own; these include T. Caraco, J. Gilliam, S. Pimm, and H. R. Pulliam. For discussion of the biology of communal breeding I am indebted to many, but I am particularly grateful to C. Barkan, J. Craig, S. Strahl, K. Rabenold, U. Reyer, S. Vehrencamp, R. Koford, and B. Bowen. My research on Mexican Jays and Grey-crowned Babblers was made possible by research grants from the National Institute of Mental Health and the National Science Foundation, and by the cooperation of the Southwestern Research Station of the American Museum of Natural History. I am grateful to the following persons for constructive comments covering all or most of this book: S. Austad, D. Siemens, W. Koenig, R. Mumme, K. Rabenold, S. Strahl. I also thank the following for their comments on selected subjects: J. Alcock, C. Barkan, B. Bowen, N. Davies, S. Emlen, A. Grafen, R. Koford, U. Reyer, I. Rowley, P. Stacey, S. Vehrencamp. For help in arranging for the cover illustration I thank S. Yamagishi. All errors are my responsibility.

Helping and Communal Breeding in Birds

1

Why Study Helping Behavior?

A helper is a bird which assists in the nesting of an individual other than its mate or feeds or otherwise attends a bird of whatever age which is neither its mate nor its dependent offspring Helpers may be of almost any age they may be breeding or nonbreeding individuals they may aid other birds of the most diverse relationships to themselves including those of distinct species and they may assist in various ways (Skutch 1961a)

Helping behavior has a special meaning in biology. It is not just any behavior that may appear to be helpful. Conventional usage of the term helping has been somewhat narrower than Skutch's definition above. Helping is parent-like behavior toward young that are not the genetic offspring of the helper. Social organizations in which individuals additional to a single male-female pair typically aid in the care of young at a single nest, not as a result of brood parasitism or brood mixing, are referred to as communal breeding systems (see glossary; the term cooperative breeding is also used). Paradoxically, helping is parental in a behavioral sense but nonparental in a genetic sense. The resolution of this paradox is the subject of this book. How has natural selection produced this exception to the rule that only parents exhibit "parental" behavior? And, in the case of breeding helpers, why do some parents devote much of their parental behavior to the young of other parents? As a technical term, helping is derived from the ornithological term, helpers-at-the-nest, and has been in use for half a century (Skutch, 1935). Alloparental behavior (E. O. Wilson 1975) is a perfect synonym and is more precisely descriptive; however, in practice the term helper is so widely understood and established that it is usually the more useful of the two. Helping behavior, especially as it is performed in the social insects by sterile workers, has been the impetus for one of the greatest revolutions in thinking about natural selection that has occurred in this century. This body of theory was first formally developed and applied by W. D. Hamilton (1963, 1964), and is known as inclusive fitness theory. It will be further elaborated in Chapter 4 and applied throughout the rest of this book. Helping behavior then is the principal test case for the ability of inclusive fitness theory to elucidate the evolution of aid-giving behaviors, some of which when carefully examined might qualify as altruism.

4 . CHAPTER 1

The principal organisms for the testing of predictions based on inclusive fitness theory have rightly been the social insects. The theory was developed by an entomologist (Hamilton, 1964), popularized by an entomologist (E. O. Wilson, 1975), and has been heavily studied by entomologists (e.g., Oster and Wilson, 1978). Yet insects are extremely different from vertebrates in their biology and they have limitations as models for vertebrates. One limitation is that many social insects are haplodiploid while the vertebrate genome is basically diploid. This has focused attention on the difference that haplodiploidy makes in the evolution of helping. For vertebrates this literature provides little insight. This book, therefore, recognizes a need to focus on the vertebrates. In this group helping has been studied for fifty years in birds but has only just begun as a recognized subject for research by mammalogists (Bekoff et al, 1984; Gittleman, 1985; Moehlman, 1979; Riedman, 1982; Rood, 1978; Macdonald, 1983; Owens and Owens, 1984.) Most of this book, consequently, is about birds. Examples from the mammals will be used occasionally. The history of the study of helping behavior has certainly been influenced at least qualitatively by inclusive fitness theory, which appeared in 1963 and 1964; however, the cumulative number of publications on helping behavior shown in Figure 1.1 does not show a dramatic increase in the rate of appearance of new papers on helping in the 5-year period, 1965-70. This may be because papers in the ornithological literature linking helping behavior with inclusive fitness theory did not start coming out until the end of this period (Brown, 1969a, 1970). The connection between helping in birds and inclusive fitness theory was developed more extensively in theoretical papers that appeared in the 5-year period ending in 1975 (Maynard Smith and Ridpath, 1972; Brown, 1974; Ricklefs, 1975). The period following these papers did show an increase in rate of appearance of publications on helping, as shown in Figure 1.1. In fact, the number of publications on helping was only 16 in the interval 1961-65, and 20 in 1966-70, but it doubled in 1971-75 {N = 47), and more than doubled again in 1976-80 (JV = 127). The curves reveal, however, that the literature on helping in birds was growing exponentially before the introduction of inclusive-fitness theory. The causes of this pattern are unclear. The curves might, for example, simply reflect the rate of growth in the number of ornithologists. The main surprise from Figure 1.1 is that the cumulative total of publications on avian helping has been growing exponentially over a 50-year period, with two thirds of the titles appearing in the last fifteen years. Inclusive fitness theory, however, is not sufficient to explain the evolution of helping, nor is it necessary in all cases. Helping behavior exists in a social framework, or social organization; and social organizations

WHY STUDY HELPING BEHAVIOR? . 5 1000 r-

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