Helping Communal Breeding in Birds: Ecology and Evolution

by J. L. Brown

Overview

An overview of the extensive and frequently controversial literature on communally breeding birds developed since the early 1960s, when students of evolution began to examine sociality as a product of natural selection. Jerram Brown provides original data from his own theoretical and empirical studies and summarizes the wide array of results and interpretations made by others.

Originally published in 1987.

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Product Details

ISBN-13:	9780691609645
Publisher:	Princeton University Press
Publication date:	07/14/2014
Series:	Monographs in Behavior and Ecology , #504
Pages:	374
Product dimensions:	6.90(w) x 10.00(h) x 0.90(d)

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Helping and Communal Breeding in Birds

Ecology and Evolution

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By Jerram L. Brown

PRINCETON UNIVERSITY PRESS

Copyright © 1987 Princeton University Press
All rights reserved.
ISBN: 978-0-691-08448-0

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CHAPTER 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 non-breeding 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.

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 (N = 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 differ greatly among species. To understand helping, we must understand the ecological determinants of the social organization within which it occurs. These are outlined in Chapter 2.

To learn why species differ in their social organizations and why helping is found in some species but not others, it is necessary to examine their ecologies. We begin by describing the eco-geographic distributions of helping in Chapter 3. Of particular interest is the demographic context of helping (Brown, 1969a, 1974; and many recent authors). This phrase refers to such phenomena from population ecology as survival rate, age structure, age-specific reproductive success, age at first breeding, fluctuations in population density, and dispersal. The demographic context "sets the stage" for selection to act on helping behavior and is the subject of Chapters 5 and 6. Studies on natural populations of species with helpers have made important contributions to our knowledge of the population ecology of birds and mammals. This constitutes an additional reason for studying helping.

Helping behavior, like all social behavior, involves at least two parties. Since the participants are typically not genetically identical, the possibility of conflict of genetic interest occurs. Donor and recipient may differ on how much help is to be given, on the cost to the donor and what is expected of the recipient as compensation. In many cases parent-offspring conflict (Trivers, 1974) might arise. Do parents "manipulate" their offspring to the parent's advantage (Alexander, 1974), or is it vice versa (Trivers and Hare, 1976). Or is this too simple a view? Perhaps a broader view expressed in the concepts of variance utilization and variance enhancement provides more insight. These problems are discussed in Chapter 15 along with a discussion of the role of dominance in cooperative social systems.

Behavioral conflict inevitably involves decisions by two or more participants. For such situations models that incorporate two or more decision makers are needed. Selection acting in such situations is best modeled using evolutionary game theory as embodied in the literature on evolutionary stable strategies, ESS (Maynard Smith and Price, 1973; Maynard Smith, 1982) and exemplified by the adaptation of the prisoner's dilemma game to the study of animal mutualisms by Axelrod and Hamilton (1981). These approaches are developed and the relevant data on "reciprocity" evaluated in Chapter 14.

Because of the interest in helping and genetic relatedness stimulated by inclusive fitness theory, new ways of conceptualizing the genetic structure of populations have developed. It is now recognized that there is significant "structure" at levels below the deme. The concept of a structured deme (D. S. Wilson, 1975,1977,1980) has led to a modernization of "group selection" (Wade, 1978; D. S. Wilson, 1983), which I prefer to call either trait-group selection, using D. S. Wilson's term to distinguish it from interdemic group selection, or kin-group selection (Brown, 1974). The study of helping has led to new empirical approaches to the study of population genetic structure and processes, and these will be reviewed in Chapter 12. Kin recognition provides a behavioral genetic structure, especially when kin-group structure is diffuse rather then discrete; kin in a large group of non-kin may associate preferentially with other kin.

Lastly, the study of helping is in some ways a microcosm of the present state of naturalistic evolutionary biology with respect to the formulation and testing of selection models. This area of sociobiology is in a rapidly developing phase of its history. It has its full share of controversies over real and supposed issues It is a fascinating exercise to examine how various workers have used (or not used)

(1) the method of alternative working hypotheses (Chamberlin, 1897),

(2) the method of weak inference or "natural experiment" and correlation,

(3) the method of strong inference by controlled experiment (Piatt, 1964),

(4) the idea of parsimony, and, unfortunately,

(5) the method of advocacy (explained by E O Wilson, 1975)

Throughout this survey of helping behavior we shall keep in view the scientific method of resolving differences between theories As explained in Chapter 18, the method of alternative working hypotheses has not always been used in strict Poppenan manner

CHAPTER 2

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

In the great majority of bird species whose nesting has been carefully studied each pair build their nest and rear their offspring without help from others of their kind This indeed is almost a corollary of the theory of Territory which teaches that each breeding pair occupy a definite nesting area from which they vigorously expel other individuals of their own species While the concept of territory in bird life has done much to stimu late and give definite direction to bird study as so often happens in the first enthusiasm of working out the details suggested by a fertile scientific theory it has resulted in a tendency to neglect the opposite side of the story There are many species in which the mated pair are not so exclusive in their territory and as a result of this coupled with other peculiar circumstances receive more or less assistance in the duties of the nest The number of recorded cases of helpers at the nest which have come to my notice is relatively small but this appears to be at least in part because their discovery requires a more concentrated attention than is commonly devoted to studies of nesting birds (Skutch 1935)

In 1935 Alexander Skutch wrote a brief paper titled "Helpers at the nest." In it he described the feeding of young Brown Jays, Bushtits, and Banded Cactus Wrens by more than two unhanded birds of their own species. Some of the birds must have been feeding young that were not their own; hence some were helpers. For decades this paper was known to a few ornithologists, but it stimulated almost no further work except by Skutch himself. In the 1930s, '40s and '50s few ornithologists were interested in field studies of social relationships and few of them could visit the tropics where most of Skutch's helper species were found. There were a few exceptions. A bird-loving Japanese army officer took advantage of the Japanese occupation of the island of Taiwan (Formosa) to study "A sociable breeding habit among Timaliine birds" (Yamashina, 1938). David E. Davis carried out an extensive comparative study of the Crotophaginae (Davis, 1942).

A quarter-century later Skutch (1961a) reviewed the literature on helping that had accumulated. This review established the generality of helping by documenting its widespread taxonomic occurrence. Still ornithologists paid little attention — probably because helping had little relevance to the theoretical issues and controversies of those years, such as speciation, the subspecies concept, ecological niches, the motivation of displays, imprinting, and the phylogeny of behavior.

This chapter outlines the early history of the study of helping, then describes some studies of helping based upon color-banding, and closes with a survey of the types of social organizations in which helping is found. Some evolutionary hypotheses based on the comparative method are entertained briefly.

The Pre-color-banding Era

As pointed out by Skutch (1935) and Rowley (1968) the mind-set of temperate-zone naturalists assumed that parents exclude all others from their territory and take care of their own young exclusively. This had been observed so often that to many observers it seemed futile to look for exceptions. Since birds are usually not easily recognized as individuals, exceptions to the rule were rarely noticed and were apparently rare and confined for the most part to the tropics and Australia. Furthermore, there was virtually no incentive to employ techniques that might have revealed the presence of extra birds at a nest.

Nevertheless, studies on unbanded birds did allow some progress. Three patterns of group living were identified. In north temperate regions it is common for birds of many species to form flocks during the winter and to disband into pairs on large territories to breed. Sparrows, warblers, waterfowl, and many other taxa form such nonbreeding groups. Another common pattern is for birds to congregate in colonies to breed in groups, with each pair defending only the nest or a small space around it. In neither case do the groups stay together for the entire year. Birds in their first spring (at the age of one year) either attempt breeding or not, but they are not expected to be with their parents. Studies on unbanded birds by Skutch (1935,1953,1954,1959,1960) showed that some Central American species, such as the Brown Jay, departed from the temperate-zone pattern by the association of young with adults even during the breeding season and probably for a few years at least. These 1- and 2-year olds (Skutch's "innubiles") even helped in care of the nestlings. The resultant groups existed all year.

Davis (1940a,b, 1941) and Skutch (1959) showed that in tropical America anis live all year in social groups. Anis belong to a group of New World cuckoos known as the Crotophaginae. Davis showed by comparative studies on the four species of this group that they could be arranged in a loose series ranging from simple to complex in social organization. In the simpler forms, pairs tended to live by themselves, while in the more complex forms pairs tended to live together and share the same nest, which Skutch called joint nesting.

In California, Leach (1925) described communal nesting by groups of Acorn Woodpeckers; and Ritter (1938), in a rambling, philosophical work, provided more details.

In Australia, Robinson (1956) carried out detailed studies of the Australian "Magpie," a black and white, crow-sized bird of the endemic Australian family Cracticidae which is not taxonomically close to the Holarctic magpies. He also showed that groups of more than two birds persisted all year.

In Arizona, Gross (1949) showed that Mexican Jays breed in groups in which more than two birds frequent a nest.

(Continues...)

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Table of Contents

• FrontMatter, pg. i
• Contents, pg. vii
• Preface, pg. xiii
• Acknowledgments, pg. xvii
• 1. Why Study Helping Behavior?, pg. 1
• 2. The Discovery of Helping Behavior and a Classification of Avian Communal Breeding Systems, pg. 8
• 3. Climate, Geography, and Taxonomy, pg. 34
• 4. Elements of Inclusive Fitness Theory for Field Studies, pg. 45
• 5. Delayed Breeding Sets the Stage for Helping, pg. 62
• 6. Reduced Dispersal Sets the Stage for Helping, pg. 91
• 7. Territorial Inheritance as Parental Facilitation, pg. 102
• 8. Mutualism, Cost-sharing, and Group Size, pg. 116
• 9. Mutualistic Mating Systems Polyandry and Uncertain Paternity, pg. 132
• 10. Mutualistic Mating Systems Joint Nesting and Uncertain Maternity, pg. 154
• 11. Does Helping Really Benefit the Helped?, pg. 169
• 12. The Genetic Structure of Social Units215, pg. 190
• 13. Indirect Selection for Helping, pg. 215
• 14. Direct Fitness, Mutualism, and Reciprocity, pg. 224
• 15. Parent-Offspring Relationships, pg. 250
• 16. Infanticide. Dominance, and Destructive Behavior, pg. 265
• 17. Diet and Group Territoriality, pg. 270
• 18. Synthesis, pg. 276
• Appendix, pg. 291
• Annotated Glossary, pg. 297
• Author Index, pg. 337
• Taxonomic Index, pg. 343
• Subject Index, pg. 352