Advances in
THE STUDY OF BEHAVIOR VOLUME 22
This Page Intentionally Left Blank
Advances in THE STUDY OF BEHAVIOR Edited by PETERJ. B. SLATER School of Biological und Medical Sciences University of St. Andrews F$e9 Scotland
JAYS. ROSENBLATT Institute of Animal Behavior Rutgers University Newark, New Jersey
CHARLES T. SNOWDON Department of Psychology University of Wisconsin-Madison Madison, Wisconsin
MANFRED MILINSKI Zoologisches Institut Universitat Bern Hinterkappelen Switzerland
VOLUME 22
ACADEMIC PRESS, INC. Harcourt Brace Jovanovich, Publishers San Diego New York Boston London Sydney Tokyo Toronto
This book is printed on acid-free paper. @
Copyright 0 1993 by ACADEMIC PRESS, 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.
Academic Press, Inc. 1250 Sixth Avenue, San Diego. California92101 United Kingdom Edifionpublished by
Academic Press Limited 24-28 Oval Road, London NW I 7DX Library of Congress Catalog Number: 64-8031 International Standard Book Number: 0- 12-004522-2 PRINTED IN T H E UNITED STATES OF AMERICA 93 94 95 96 91 98 QW 9 8 1 6 5 . 4 3 2
1
Contents Contributors .............................................. Preface ..................................................
ix xi
Male Aggression and Sexual Coercion of Females in Nonhuman Primates and Other Mammals: Evidence and Theoretical Implications
BARBARA B. SMUTS AND ROBERT W. SMUTS I. Introduction ....................................... 11. Male Aggression and Sexual Coercion in Nonhuman Primates .......................................... 111. Costs to Female Primates of Male Aggression .......... IV. Primate Female Counterstrategies to Male Aggression . . V. Male Aggression against Females in Chimpanzees ...... VI. Male Aggression against Females in Other Mammals . . . . VII. Variation in Male Aggression against Females .......... VIII. Evaluating the Sexual Coercion Hypothesis ............ IX. Implications of Male Sexual Coercion for Sexual Selection Theory ................................... X. Conclusions ....................................... XI. Summary .......................................... References ........................................
1
3 9
II 19
24 31 37 43 49 49 50
Parasites and the Evolution of Host Social Behavior ANDERS PAPE MOLLER, REIJA DUFVA, AND KLAS ALLANDER
I. Introduction ....................................... 11. Group Living and Parasites .......................... 111. Parasites, Reproduction, and Sexual Selection . . . . . . . . . IV. Social Behavior and Parasite-Host Coevolution . . . . . . . . V. Summary .......................................... References ........................................
V
65
73 83 91 93 94
vi
CONTENTS
The Evolution of Behavioral Phenotypes: Lessons Learned from Divergent Spider Populations SUSAN E. RIECHERT I. Introduction
.......................................
11. The Spider System ................................. 111. Fitness-Linked Behavioral Traits .....................
IV. Arizona Riparian Population Deviation from Adaptive Equilibrium ........................................ V. Factors That May Have Limited Adaptation . . . . . . . . . . . VI. Experimental Manipulation of Gene Flow versus Selection .......................................... VII. Discussion and Conclusions ......................... VIII. Summary ........................................... References ........................................
103 I04 I12 119 I23 I28 I30 132 133
Proximate and Developmental Aspects of Antipredator Behavior E. CURIO
I. Introduction ....................................... 11. Causal Aspects of Enemy Recognition . . . . . . . . . . . . . . . . 111. Developmental Aspects of Enemy Recognition . . . . . . . . . IV. Conclusions ....................................... V. Summary .......................................... References ........................................
135 I39 I87 221 225 227
Newborn Lambs and Their Dams: The Interaction That Leads to Sucking MARGARET A. VINCE
I. Introduction ....................................... 11. Pre- and Perinatal Factors That Play a Part in the Ewe and Lamb Relationship after Birth .................... 111. Sensory and Behavioral Factors Involved in the Postnatal Relationship between Ewe and Lamb . . . . . . . . IV. Discussion ........................................ V. Summary .......................................... References ........................................
239 240 244 262 263 264
CONTENTS
vii
The Ontogeny of Social Displays: Form Development. Form Fixation. and Change in Context T . G . G . GROOTHUIS I . General Introduction ................................ I1 . Mechanisms of Form Development . . . . . . . . . . . . . . . . . . . 111. Form Fixation of Display ............................ IV . Change in Context of Display ........................ V . Functional Aspects of Display Development ........... V1 . A Summarizing Scheme ............................. VII . Summary .......................................... References ........................................
lndex
..............................................
Contents of Previous Volumes ...........................
269 273 302 306 310 315 318 319 323 328
This Page Intentionally Left Blank
Contributors
Numbers in parentheses indicate the pages on which the authors’ contributions begin.
KLAS ALLANDER (65). Department of Zoology, Uppsala University, S-75122 Uppsala, Sweden E. CURIO ( 1351, Arbeitsgruppe fur Verhaltensforschung, Fakultat fur Biologie, Rithr-Universitat Bochum, 0 4 6 3 0 Bochum 1, Germany REIJA DUFVA (65), Department of Zoology, Uppsala University, S-751 22 Uppsala, Sweden T. G . G . GROOTHUIS (2691, Zoological Laboratory, University of Groningen, 9750 A A Haren, The Netherlands ANDERS PAPE MOLLER (651, The Galton Laboratory, Department of Genetics and Biometry, University College of London, London, England SUSAN E. RIECHERT (103). Department of Zoology, The University of Tennessee, Knoxville, Tennessee 37996 BARBARA B. SMUTS ( I ) , Departments of Psychology and Anthropology, und Center for Human Growth and Development, University of Michigan, Ann Arbor, Michigan 48109 ROBERT W. SMUTS ( I ) , Ann Arbor, Michigan 48104 MARGARET A. VINCE (239), AFRC Institute of Animal Physiology und Genetics Research, Babraham, Cambridge CB2 4AT,England
ix
This Page Intentionally Left Blank
Preface The aim of Advances remains as it has been since the series began: to serve the increasing number of scientists 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. While the recent rise of behavioral ecology and sociobiology has tended to overshadow other areas, scientists studying behavior today range more widely than ever before: from ecologists and evolutionary biologists to geneticists, endocrinologists, pharmacologists, neurobiologists. and developmental psychobiologists, not forgetting the ethologists and comparative psychologists whose prime domain is this subject. It is not our intention to focus narrowly on one or a few of these fields, but rather 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 the publisher of Advances in rhe Srudy 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 especially penetrating research that introduces important new concepts. The realization of these aims is well illustrated by the spectrum of topics presented in the present volume. With this volume we welcome Dr. Charles T. Snowdon, of the University of Wisconsin at Madison, as an editor. A primatologist with wideranging interests, his expertise will make a valuable contribution to the breadth of our editorial team, and his contribution will do much to maintain the vigor of the series.
xi
This Page Intentionally Left Blank
ADVANCES
IN THE STUDY OF B E H A V I O R . VOL. ?.
Male Aggression and Sexual Coercion of Females in Nonhuman Primates and Other Mammals: Evidence and Theoretical Implications BARBARAB. SMUTS DEPARTMENTS OF PSYCHOLOGY AND ANTHROPOLOGY AND CENTER FOR HUMAN GROWTH AND DEVELOPMENT UNIVERSITY OF MICHIGAN ANN ARBOR, MICHIGAN 48109
ROBERTW. SMUTS ANN ARBOR. MICHIGAN 48104
I.
INTRODUCTION
The single most important difference between the sexes is the difference in their investment in offspring. The general rule is this: females do all of the investing: males do none of it. (Trivers. 1985, p. 207)
Although Trivers' general rule has many exceptions, it accurately identifies the primary source of conflict between the sexes: in most sexual organisms most of the energy and time invested in offspring comes from females. From this basic fact it follows that, for males more than females, reproductive success is limited by the number of matings with fertile partners. For females more than males, on the other hand, reproductive success is limited by the time and effort required to garner and transfer energy to offspring and to protect and care for them (Bateman, 1948; Trivers, 1972). Males therefore are usually more eager than females to mate at any time with any partner who may be fertile, while females are usually more careful than males to choose mates who seem likely to provide good genes, protection, parental care, or resources in addition to gametes (Trivers, 1972; Alexander and Borgia, 1979). Combined with female interest in mate quality, male interest in mate quantity creates a widespread conflict of interest between the sexes (Borgia, 1979; Parker, 1979; Hammerstein and Parker, 1987). The conflict is I Copyright 0 1993 by Academic Press. Inc. All rights of reproduction in any form reserved.
2
BARBARA B. S M U T S A N D ROBERT W . SMUTS
mitigated when males court females by offering them the benefits females want from males, such as food, protection, or help in rearing young. These benefits are typically costly in terms of male time and energy, however, and males may often be able to overcome female reluctance at lower cost to themselves by using force or the threat of force, behavior that we call “sexual coercion.” Theoretical treatments (e.g., Hammerstein and Parker, 1987) indicate that sexual coercion can function as an important selective force influencing the evolution of both male and female behaviors. However, male aggression toward females, including sexual coercion, has rarely been a focus of study, and for the vast majority of animals, including most mammals, quantitative information is unavailable. These limitations severely constrain our ability to determine the evolutionary significance of sexual coercion. This article aims to stimulate research and theorizing about sexual coercion by reviewing the relevant evidence for nonhuman primates and some other mammals in which sexual coercion is especially well documented. Two contrasting goals guide this review. On the one hand, we hope to persuade the reader that sexual coercion is an important phenomenon worthy of further study. On the other, we wish to highlight important gaps in our knowledge of sexual coercion. We have tried to balance these two goals by using limited evidence from a small number of species to generate hypotheses, while emphasizing that, to test these hypotheses, we need much better information from a larger number of species. We begin by describing aggressive male behaviors that appear to function as sexual coercion, the costs that this male aggression imposes on females and young, and the counterstrategies that females employ to reduce these costs. The data that we review for primates and other mammals reveal extensive variation in the form and frequency of male aggression against females, and we propose several hypotheses to help account for this variation. We also consider the kinds of evidence needed to determine whether particular cases of male aggression against females function as sexual coercion. In the final section, we argue that sexual coercion has been underestimated as a significant force in social evolution, and indicate how more attention to intersexual coercion as a form of sexual selection can enhance our understanding of animal societies. OF SEXUAL COERCION THECONCEPT
We define sexual coercion as use by a male of force, or threat of force, that functions to increase the chances that a female will mate with him at a time when she is likely to be fertile, and to decrease the chances that
MALE AGGRESSION AND SEXUAL COERCION
3
she will mate with other males, at some cost to the female. The functional consequences of male sexual coercion distinguish it from other instances of male aggression against females (e.g., in the context of feeding competition) that do not appear to involve manipulation of sexual opportunities. Our definition of sexual coercion as a subset of aggressive male behaviors toward females that is delineated by their function means that sexual coercion is not a purely behavioral concept, but involves a combination of behavioral description and functional explanation. Sexual coercion cannot be identified by observing only the immediate behavior of the aggressor; it is also necessary to observe the subsequent behavior of the aggressor, the target, and even of other individuals. It is not an easy concept to work with, but we believe it is nevertheless useful because it accurately reflects the complexity of agonistic sexual behavior in animals. Toward the end of this article, we consider in some detail how one can test the hypothesis that particular acts of male aggression against females fit the functional definition of sexual coercion given here. We delay this discussion until later because it requires a basic understanding of the wide variety of male aggression toward females that is observed in nature. Thus, we will proceed for the moment on the assumption that sexual coercion does indeed exist, while keeping in mind the need to examine functional consequences before accepting the hypothesis that a particular aggressive act (or set of acts) actually functions as sexual coercion. Our definition also limits sexual coercion to behavior that involves the use or the threat of force. Although males can (and do) manipulate female mating behavior to their own advantage by inflicting other kinds of costs or by withholding benefits, such a broad definition of sexual coercion would encompass so large a part of all interactions between males and females that it would prove useless. 11. MALEAGGRESSION A N D SEXUAL COERCION IN NONHUMAN PRIMATES In what follows, we concentrate on polygynous primates living in groups in which a single male monopolizes matings with two or more females, or multiple males compete for mating opportunities with multiple females. Because polygyny is typically associated with much more intense male-male competition for mates (Clutton-Brock and Harvey, 1976, 1978), these species are expected to show more male sexual coercion than species living in monogamous or polyandrous groups. Reduced sexual coercion is especially likely in monogamous and polyandrous primates, because these species invariably establish long-lasting pair bonds and defend territories
4
BARBARA B. SMUTS AND ROBERT W. SMUTS
against other groups (Goldizen, 1987; Robinson et al., 1987; Robbins Leighton, 1987), minimizing opportunities for contact between oppositesex individuals other than mates. This is in contrast to the situation in many monogamous birds and in most human groups, in which, because of high mobility and/or communal living, mated individuals may frequently encounter opposite-sex individuals other than their mates (Westneat et al., 1990; Rodseth ef al., 1991). Although, on theoretical grounds, sexual coercion is expected to be considerably less common in monogamous and polyandrous nonhuman primates, we do not imply that it is entirely absent in these species, and, indeed, the possible significance of sexual coercion of females by mates (e.g., Goldizen, 1989) or male neighbors during encounters between family groups, or by strange males when they encounter lone females, or by mates when females approach territory boundaries, deserves further attention. We focus on information from wild primates, when it is available, because wild groups are more likely to reflect socioecological conditions that obtained during the species’ evolutionary history, but we also include relevant evidence from provisioned and captive animals. Caution is necessary when such information is used to support an argument related to selection pressures in the wild. However, evidence from captive or provisioned animals can provide useful indications of behavioral potentials not typically shown in the wild, which may nevertheless reflect a species’ evolved capacity to respond adaptively to novel circumstances (R. W. Smuts, 1993). Finally, we conclude our discussion of primates with a special section on chimpanzees. We discuss chimpanzees as a separate “case study” because much more information is available on male aggression against females in this species than in any other primate, and we wish to present this information as a coherent whole. A.
FREQUENCY OF MALEAGGRESSION AGAINST FEMALES AND CONTEXTS OF OCCURRENCE
Male aggression against females is frequently mentioned in passing or briefly described in the literature on wild nonhuman primates, which suggests its widespread occurrence through the Primate order (Tracy and Crawford, 1992). However, few quantitative data are available on male aggression against female nonhuman primates. Smuts (1985) determined rates of male aggression toward anestrous (i.e., pregnant and lactating) females in a troop of wild olive baboons. During daylight hours, the average anestrous adult female was a victim of male aggression five times per week. One-quarter of these episodes involved physical attack, and
MALE AGGRESSION A N D SEXUAL COERCION
5
roughly 1 of every 50 attacks resulted in a serious wound. Put another way, each adult pregnant or lactating female baboon in the troop could expect to receive at least one serious wound from a male every year (Smuts, 1985). The rate at which female mountain gorillas receive aggression from the silverback male is even higher (ranging from 1 to 4.3 times per female per 12-hour day, depending on the group and time period), but, in contrast to baboons, this aggression very rarely leads to injury (Watts, 1992).In some other species, male aggression toward females occurs much less often. Among red howlers, for example, Sekulic (1983a) observed male aggression toward females at a rate of less than 0.04 times per female per day. The contexts in which males show aggression toward females also vary widely, both within and between species. In many species, a significant proportion of male-female agonism occurs during feeding competition (e.g., olive baboons: 20% [Smuts, 19851; mountain gorillas: 5-20% [Watts, 19921; wedge-capped capuchins: 63% [O’Brien, 19911; chimpanzees: about 18% [Goodall, 1986, fig. 12.31). Smuts (1985) found that males were also aggressive toward anestrous females in a wide variety of social situations, including defense of other females and young who were affiliated with the aggressor. Mountain gorilla males and macaque males also frequently direct aggression toward females in order to break up fights between females (Kaplan, 1977; Harcourt, 1979; Bernstein and Ehardt, 1986; Oi, 1990; Watts, 1992). Smuts (1985) also observed young, high-ranking males attacking the close female associates of older, lower ranking rivals, apparently in order to provoke the older males into aggressive confrontations that they were likely to lose. Similarly, de Waal (1982) described how, during a power struggle between captive chimpanzee male allies Nikki and Luit on the one hand, and alpha male Yeroen on the other, Luit and Nikki often attacked one of Yeroen’s female supporters near Yeroen, apparently to test his willingness to protect females against the rivals. These examples indicate that bonds with particular males sometimes make females vulnerable to manipulative aggression by rival males. The examples just given highlight the fact that not all male aggression toward females functions as sexual coercion. However, quantitative data from several species show that male aggression toward females is more likely when the females are in estrus (macaques: Tokuda, 1961; Kurland, 1977; Enomoto, 1981; Fedigan, 1982; Eaton, 1984; Teas, 1984 [but see Ruehlmann et al., 1988, for an exception]; savanna baboons: Hausfater, 1975;chimpanzees: Goodall, 1986; mountain gorillas: Nadler, 1989b).This widespread tendency for males to show more aggression toward potentially fertile females is consistent with the hypothesis that male aggression often functions to increase access to mates.
6
BARBARA B. SMUTS A N D ROBERT W . SMUTS
B. POSSIBLE EXAMPLES OF MALE SEXUAL COERCION The primate literature contains numerous descriptions of behaviors that appear to satisfy our definition of sexual coercion. For example, male rhesus monkeys attack females caught mating or consorting with lower ranking rivals and sometimes injure them severely (Carpenter, 1942; Lindburg, 1983; Manson, 1991). Manson (l991), studying free-ranging, provisioned rhesus monkeys on Cay0 Santiago, reported a significant positive relationship between the frequency with which estrous females associated with lower ranking males and the rate at which they received aggression from high-rdnking males, who were apparently intent on disrupting these mating relationships. Chimpanzees, like male macaques, also tend to attack the female, rather than the lower ranking rival, if the two are caught courting (de Waal, 1982; Goodall, 1986; Hauser, 1990). Male chimpanzees (Goodall, 1986; see also Section V,A), rhesus monkeys (Carpenter, 1942; Lindburg, 1983), Japanese macaques (Enomoto, 1981), and savanna baboons (Hausfater, 1975) also use aggression to try to initiate or maintain consortships with uncooperative females. The most dramatic examples of apparent sexual coercion come from wild orangutans, in which most copulations by subadult males (MacKinnon, 1971; Rodman, 1973; Rijksen, 1978; Galdikas, 1985; Mitani, 1985) and nearly half of all copulations by adult males (Mitani, 1985) occur after the female’s fierce resistance has been overcome through violent restraint. Similar forced copulations have occasionally been observed among wild chimpanzees; in most cases these involved incestuous matings (Goodall, 1986;Nishida, 1990). In a series of studies ofcaptive chimpanzees, lowland gorillas, and orangutans, Nadler (1982, 1988; Nadler and Miller, 1982) found that, when heterosexual pairs were housed alone together, males in all three species used aggression to force females to copulate throughout the estrous cycle. When females were given control over proximity to the male, however, copulations occurred only with female cooperation and only at mid-cycle. These observations indicate that males in all three of these species of apes will employ sexual coercion when the opportunity for females to escape is minimized. Even when a female is not sexually receptive, male aggression may be designed to increase, or maintain, future mating access. A well-known example involves the male hamadryas baboon, who uses coercion to keep the females he gathers around him away from other males at all times. Should one of “his” females stray toward another male, the hamadryas male will instantly threaten the female with an eyebrow flash; if she fails to approach him immediately he will attack her with a neckbite (Kummer, 1968). Male use of aggression to herd mates away from strange males
MALE AGGRESSION A N D SEXUAL COERCION
7
during encounters with other groups has been reported for species in all major primate taxa, including prosimians (M. E. Pereira, personal communication), cercopithecines (Cheney and Seyfarth, 1977; van Noordwijk and van Schaik, 1985; Byrne et ul., 19871, colobines (Stanford, 19911, New World monkeys (Goldizen, 19891, and apes (Nishida and HiraiwaHasegawa, 1987; Sicotte, 1989; Watts, 1991). Our definition of sexual coercion in functional as well as behavioral terms means that it may sometimes be difficult to determine whether a particular behavior qualifies as sexual coercion. For example, in several primates, male ritualized courtship displays incorporate aggressive behaviors that are typically directed against other males (e.g., stalking in rhesus macaques: Manson, 1991; hair erection and bipedal swagger in chimpanzees: Goodall, 1986; charging in gorillas: Nadler, 1989b). The functional significance of “ritualized” aggression during courtship is not well understood; such displays could possibly function to demonstrate a male’s health and vigor and might thereby facilitate female mate choice. Thus, the fact that a male directs aggression toward an estrous female does not in and of itself constitute evidence for sexual coercion (see Section VlII for further discussion of this issue). On the other hand, male aggression that has no obvious sexual significance may nevertheless function to increase female sexual cooperation in the future and thus qualify as aform of sexual coercion. Goodall (l986),for example, notes that 83% of severe male attacks on females that occurred in no obvious context involved cycling females whose sexual swellings had not yet reached the stage of full tumescence associated with ovulation. She suggests that these attacks intimidate the female so that, when she is close to ovulation, she will respond positively to the male’s mating initiatives. Another possible example of sexual coercion involves the frequent cooperative aggression against single females by allied male spider monkeys (black-handed spider monkeys: Fedigan and Baxter, 1984; black spider monkeys: McFarland Symington, 1987). This aggression has not been observed to injure females, but it can be intense; McFarland Symington (1987, p. 153) describes “frenzied chases involving three males and lasting up to 15 minutes.” The functional significance of this aggression remains obscure; although it is directed only at cycling females (McFarland Symington, 1987), it has not been observed as a prelude to copulation (Fedigan and Baxter, 1984; McFarland Symington, 1987). Spider monkeys are among a handful of primates in which males remain in their natal groups and form lifelong bonds with one another, while females transfer to other groups. They are also one of the few polygynous anthropoid primates that show little sexual dimorphism, but females are nevertheless consistently
8
BARBARA B. SMUTS AND ROBERT W. SMUTS
subordinate to males and relations between the sexes are “generally tense” (McFarland Symington, 1987, p. 161). Given the slight sexual dimorphism in these species, it seems reasonable to hypothesize that male dominance over females is a product of aggression by male coalitions and that, by increasing their power over females, cooperating males also increase their ability to gain sexual access to them. Since courtship and copulation have rarely been observed in wild spider monkeys (Fedigan and Baxter, 1984; McFarland Symington, 1987), further evidence is needed to evaluate this hypothesis. Male primates’ use of force to increase sexual access to females can also involve considerably longer-term strategies such as infanticide (Hrdy , 1979). Males from a wide variety of nonhuman primates, including Old and New World monkeys, apes, and prosimians, kill infants sired by other males (Hausfater and Hrdy, 1984; Crockett and Sekulic, 1984; Struhsaker and Leland, 1987; Pereira and Weiss, 1991). Male infanticide occurs most often in species that live in groups with a single breeding male after a strange male aggressively usurps the breeding position and attempts to kill the immature offspring of the previous male (grey langurs: Hrdy, 1977; red howlers: Sekulic, 1983a; Crockett and Sekulic, 1984; mantled howlers: Clarke, 1983; red-tail monkeys: Struhsaker, 1977; blue monkeys: Butynski, 1982). Male infanticide can also occur when immigrant males enter groups with multiple breeding males (baboons: Collins er id., 1984), in association with a change in male status relationships within multimale groups (red colobus: Struhsaker and Leland, 1985), or after a breeding male dies, leaving vulnerable mothers and infants without protection (gorillas: Watts, 1989). Because a return to sexual cycling is inhibited by lactation, death of the infant typically brings the mother into estrus sooner than would occur otherwise. In many instances, the infanticidal male subsequently mates with the female (reviewed by Struhsaker and Leland, 1987). Although the aggression involved in infanticide targets the infant rather than the mother, it is appropriate to view infanticide as a form of sexual coercion for two reasons. First, like other forms of sexual coercion, it involves the use of force to manipulate the female’s sexual state and mating behavior to the male’s advantage; killing the infant is simply a means to this end. Second, like other forms of sexual coercion, it imposes a cost on the female.
C. A NOTE ON TERMINOLOGY In the following section, we discuss the costs to females of male aggression that we hypothesize functions as sexual coercion. However, below and in later sections, we refer to specific behaviors as “male aggression”
MALE AGGRESSION AND SEXUAL COERCION
9
rather than “sexual coercion” because, in most cases, the functional consequences of these behaviors have yet to be demonstrated conclusively. 111. COSTSTO PRIMATE FEMALES OF MALEAGGRESSION
Although the reproductive costs to females of male aggression have seldom been measured, they may often be considerable. Lindburg (1983) saw a top-ranking rhesus male fatally injure his consort partner after she repeatedly approached another male, and B. B. Smuts (personal observation) saw an adult male olive baboon kill an adolescent, estrous female. Rajpurohit and Sommer (1991) reported the death of a grey langur female as a result of wounds inflicted by a male, but the context of the attack was not described. Enomoto (1981) and Manson (1991) reported frequent male aggression toward estrous female macaques (Enomoto: 0.86 times per day per female; Manson: 0.26-0.44 times per day per female). These two studies and Teas’ (1984), study of wild rhesus “temple monkeys” in India agree that male aggression against estrous females often resulted in serious wounds. These results should be regarded with caution, however, because they are from provisioned troops living in crowded conditions, which may increase rates of male aggression and wounding. At Gombe, observers have witnessed numerous brutal attacks by male chimpanzees on females from other communities, and some of these females died from their wounds (Goodall, 1986). Finally, even when females themselves are not severely injured by male attacks, male violence can lead to abortion (baboons: Pereira, 1983), disruption of estrous cycles (chimpanzees: Goodall, 1986; rhesus macaques: J. Manson and s. Perry, personal communication), and perhaps other deleterious, stress-related effects. The reproductive costs of male infanticide are easier to ascertain. Among grey langur troops near Jodhpur, when the previous resident male was replaced by a new male, 40% of infants present at the time of replacement (n = 81 in 12 different troops) and 35% of the infants born shortly thereafter (n = 34) were victims of infanticide (Sommer, 1992). Since male takeovers occurred on average every 26.5 months (Sommer and Rajpurohit, 1989), infanticide is clearly an important source of infant mortality. Among mountain gorillas, at least 37% of infant mortality is due to male infanticide (Watts, 1989). Crockett and Rudran (1987) and Clarke and Glander (1984) give similar estimates (44 and 40%) for red howler monkeys and mantled howlers, respectively. Male infanticide may also be responsible for a significant proportion of infant mortality in chimpanzees
10
BARBARA B. SMUTS AND ROBERT W. SMUTS
(Goodall, 1986; Nishida, 1990; Nishida er al., 19901, baboons (Collins er ul., 1984), and probably a number of other species. Potential costs of infanticide for females are probably even higher, since rates of infanticide are undoubtedly reduced, sometimes substantially, by female counterstrategies (see below). In addition to the obvious costs due to severe injuries or death, male aggression can inflict subtle but perhaps significant costs by constraining female behavior in many ways. For example, male herding in hamadryas baboons sometimes prevents a female from joining her female kin in a different group, thus depriving her of potential allies (Abegglen, 1984). In mountain gorillas, male infanticide constrains female movements between groups. Mothers with young infants must remain in their current group until the infant is older, abandon the infant and transfer without it (as sometimes occurs), or transfer with the infant, which nearly always leads to infanticide (Watts, 1989). When males employ aggression to exact female sexual cooperation, the benefits females derive from free mate choice will be reduced (for discussion of possible benefits of mate choice. see Smuts, 1987a; Small, 1989; Manson, 1991). Manson (1991), for example, found that among rhesus macaques on Cay0 Santiago, estrous females preferentially maintained proximity to lower ranking males, and such proximity-maintaining behavior correlated with higher copulation rates. However, after higher ranking males chased or attacked females in consort with lower ranking males, the females often failed to restore proximity to their previous partners. This suggested to Manson that male aggression disrupted females’ attempts to express their mating preferences. The time and energy involved in maintaining vigilance toward potentially aggressive males may sometimes be costly, although such costs are difficult to measure. Female baboons with young infants consistently avoid proximity to recent male immigrants (the males most likely to commit infanticide; Collins er a / . , 1984; Busse, 1984), female vervets restrain their infants significantly more often in the presence of new males (Fairbanks and McGuire, 1987), and female ring-tailed lemurs carefully monitor the movements of recently immigrated males who are likely to commit infanticide (Pereira and Weiss, 1991). Finally, it is important to note that the costs discussed here occur in spite of whatever female counterstrategies exist to resist or reduce male aggression. In the absence of such counterstrategies, the costs to females of male aggression presumably would often be considerably higher. These “original,” higher costs are the selective forces that promote the evolution of female counterstrategies. In addition, the counterstrategies that females
MALE AGGRESSION A N D SEXUAL COERCION
11
employ to resist or reduce male aggression themselves often involve costs, as indicated below. IV. A.
PRIMATE FEMALE COUNTERSTRATEGIES TO MALE AGGRESSION
FIGHTING BACK
The most obvious first line of defense against male aggression is to fight back. In extreme cases, particularly when protecting vulnerable infants. this is just what female primates tend to do. Mountain gorilla females, for example, usually fight back against male attacks on their infants. However. because male gorillas are twice as large as females, female resistance is usually futile, and resistant females risk severe injury (Watts, 1989). Red howler and grey langur females also attempt to physically thwart infanticidal males, and occasionally wound them, but they are rarely able to prevent infanticide (Hrdy. 1977; Sekulic, 1983a; Crockett and Sekulic, 1984). Similarly, orangutan females struggle free only rarely during forced copulations (Mitani, 1985). In most nonhuman primates in which male aggression toward females has been reported, males are larger than females and dominate them in one-on-one encounters (reviewed by Smuts, 1987b), which limits the effectiveness of retaliatory aggression by single females. A few striking exceptions exist, however. In ring-tailed, crowned, and ruffed lemurs, females consistently win dyadic agonistic encounters with males (Kappeler, 1990; Pereira et a l . , 1990; Kaufman, 1991). Among patas monkeys, individual females often defeat males in one-on-one fights, and males “appear extremely reluctant to use force against females in almost all contexts, presumably because of the threat of female retaliation’’ (Loy, 1989, p. 39). Similarly, in macaques, vervet monkeys, brown capuchins, wedge-capped capuchins, and several other species, individual females sometimes win agonistic encounters against males (e.g., stumptail macaques: Bernstein, 1980; Japanese macaques: Johnson et d., 1982; vervets: Bramblett et al., 1982; brown capuchins: Janson, 1984; wedgecapped capuchins: Robinson 1981; O’Brien, 1991; see Smuts, 1987b. for further details). Since, with the exception of lemurs, males are larger than females in all of these species (and much larger than females in patas monkeys), these observations are puzzling; they are discussed further below. Because of the limited effectiveness in most primates of individual retaliation by females, evolution has favored a variety of other female counterstrategies. These are not trivial, but involve critical aspects of
12
BARBARA B . S M U T S A N D ROBERT W . S M U T S
female life histories, including timing of sex and reproduction, mate choice, choice of group, and the development of social relationships and alliances. Below we give some examples of each.
B. TIMINGOF S E X U A L
ACTIVITY A N D
REPRODUCTION
In grey langurs (Agoramoorthy et d.,1988). gelada baboons (Mori and Dunbar. 1985). and captive hamadryas baboons (Colmenares and Gomendio, 1988),takeover of the unit by a new male induces spontaneous abortions in pregnant females, which has been interpreted as female termination of investment in infants who are likely to be victims of infanticide (Mori and Dunbar, 1985; Sommer, 1987). In addition. in all three species. lactating females confronted with anew male may rapidly return to cycling, shortening lactational amenorrhea (Sigg et d.,1982; Mori and Dunbar. 1985; Colmenares and Gomendio, 1988; Winkler. 1988). In the captive hamadryas group, all six lactating females quickly resumed cycles, regardless of the age of their infants, and one grey langur female resumed cycling only 7 days after giving birth (Winkler. 1988).Thus, the presence of a new male overrode the role that infant suckling normally plays in the control of female reproduction (Colmenares and Gomendio, 1988). Whether rapid return to cycling by lactating females has evolved to prevent infanticide, however, remains an open question. In several wild gelada females (Mori and Dunbar, 1985) and in the single case reported for wild langurs (Winkler, 1988), the infants of the nursing mothers who resumed cycles early were not killed, but in the captive hamadryas group, some were. which led the observers to reject the infanticide hypothesis (Colmenares and Gomendio, 1988). However, the hamadryas data are ambiguous because all four victims of infanticide were killed by a single male described as so aggressive in temperament that he was removed from the colony (Colmenares and Gomendio, 19881, and because of abnormal crowding in captivity. In many primates, pregnant females may solicit copulations when confronted with an unfamiliar male (red colobus: Struhsaker and Leland, 1985; grey langurs: Hrdy, 1977; captive patas: Loy. 1985; gelada baboons: Mori, 1979;redtail monkeys: Cords, 1984; mountain gorillas: Watts, 1989). Hrdy (1977, 1979)first argued that such situation-dependent sexual receptivity may reduce the likelihood of infanticide by confusing paternity. Sommer (1987, 1992) rejects this hypothesis for grey langurs, because the pattern of postconception estrus observed over many years at Jodhpur was virtually the same whether the sire was still resident in the troop or a new male had taken over (in other words, it was not “situationdependent”), and because the presence or absence of copulations with a
MALE AGGRESSION A N D SEXUAL COERCION
13
new male did not affect whether or not the female’s infant was subsequently killed by that male. In contrast, female red colobus monkeys who were pregnant when a male attacked infants in their group mated more frequently and later into their pregnancy than did pregnant females either before or after these attacks. A large fraction of these copulations was with the infanticidal male, who did not attack infants of the pregnant females after they were born (Struhsaker and Leland, 1987, p. 96). Thus postconception estrus may serve different functions in different species. Other species in which infants are vulnerable to infanticide, such as red howlers, fail to show postconception estrus in response to invading males (Sekulic, 1983~). When some infants are killed by infanticidal males, others in the same group often escape harm. At Jodhpur, for example, a substantial proportion of vulnerable langur infants (44%) were not attacked by new males, even though other infants in the troop were killed (Sommer, 1992). The fact that some infants go unharmed raises intriguing questions about the factors that may be responsible for their survival, including, perhaps, presently unidentified female counterstrategies. After red howler females experience invasion and infanticide from immigrant males, they rapidly return to cycling but do not conceive immediately. Crockett and Sekulic (1984) hypothesize that the rapid return to cycling incites male-male competition, hastening resolution of the identity of the new alpha male; similarly, delayed conception may benefit females because it increases the probability that their next infant will be sired by the new alpha male. C. MATE CHOICE In primates that live in multimale troops, females often show preferences for mating with dominant males; these preferences have usually been interpreted in terms of the proven genetic quality of the males (reviewed by Small, 1989). The alternative hypothesis that females choose dominant males in order to reduce harassment of themselves or their infants by other males (Wrangham, 1979; Trivers, 1985) has received little attention and deserves further scrutiny. Manson (1991), for example, showed that when rhesus monkey females consort with high-ranking males, they are attacked significantly less often by rival males than when they consort with lowranking males. Since, as noted above, such attacks can lead to severe injury or even death, mate choice could significantly reduce the costs to females of male aggression. Pereira and Weiss (1991) hypothesize that female ring-tailed lemurs choose to mate with males that indicate superior ability to maintain high rank throughout the subsequent birth season,
14
BARBARA B. S M U T S A N D ROBERT W . S M U T S
because such males will be more effective in protecting infants from infanticide by rival males. Similarly, Pope (1990)and O’Brien (1991)suggest that, among red howlers and wedge-capped capuchins, respectively, females benefit from mating with the alpha male, because he provides the most effective protection against infanticide by other males. Janson (1984,1986) suggests that female brown capuchins benefit from mating with dominant males because the protection they provide enables females and their infants to forage undisturbed at rich food sources. In many Old World primates, female mate choice appears designed to facilitate copulation with a number of different males (reviewed by Smuts, 1987a; Small, 1989). Hrdy (1979) and Wrangham (1980a) suggested that, by mating with many males, a female can confuse paternity and thus reduce the probability of infanticide. This hypothesis predicts that females will be particularly interested in mating with males who are most likely to commit infanticide, namely, males that have recently entered a group, or extragroup males who might later transfer into the group (Hrdy, 1979). Indeed, in a number of primate species, females are sexually attracted to such males (reviewed by Smuts, 1987a; Small, 1989). This has been documented both for species living in multimale troops (e.g., Japanese macaques: Wolfe, 1981; rhesus macaques: Brereton, 1981; Manson, 1991; vervet monkeys: Henzi and Lucas, 1980; savanna baboons: Packer, 1979) and species living in one-male troops (grey langurs: Hrdy, 1977; Mohnot, 1984; Sommer, 1988; blue monkeys: Tsingalia and Rowell. 1984; patas monkeys: Olson, 1985). Sommer (1988) has suggested, in addition, that female grey langurs solicit copulations from male invaders in order to incite male-male competition and induce takeover by the strongest possible male. Sommer’s hypothesis could apply to many other species living in one-male troops in which females copulate enthusiastically with invading males (e.g., redtail monkeys: Cords, 1984; blue monkeys: Tsingalia and Rowell, 1984; patas monkeys: Harding and Olson, 1986). Alternatively, females may induce takeover by the strongest male not by mating, but by inciting male-male competition through other means, such as howling (Sekulic, 1983~). Despite promiscuous tendencies, females in many species living in multimale groups show marked mating preferences for particular male partners (reviewed by Smuts, 1987a). For example, in savanna baboons, females often prefer to mate with males with whom they have developed a long-term, affiliative relationship (Seyfarth, 1978; Smuts, 1983a,b, 1985). Smuts (1985) argued that females form such friendships with males, and prefer them as mates, in exchange for protection by these males against aggression from other males toward themselves and their infants. Indeed, when a male defended a female or her immature offspring against other
MALE AGGRESSION A N D SEXUAL COERCION
15
baboons, in 91% of the cases he was the female’s friend (Smuts. 1985). Females form friendships with both high- and low-ranking males. This reflects the fact that, in olive baboons (unlike macaques; see below), even low-ranking males are useful allies, because they are willing to challenge higher ranking males, especially when they receive agonistic support from other males (Packer, 1977; Strum, 1982; Smuts, 1985; No&, 1990). M. E. Pereira (personal communication) has documented similar special relationships among captive redfronted brown lemurs, which are also characterized by male protection of the female against other males in exchange for enhanced mating opportunities. The significance of such special relationships was highlighted when, after a male transferred from one enclosure to another, he killed the infants of one female and “bonded” with the other, leaving her infants alone (M. E. Pereira. personal communication).
D. CHOICE OF GROUP A female’s choice of which group to live in may be strongly influenced by potential male aggression, particularly in those species in which females commonly transfer. In red colobus monkeys (Marsh, 1979) and grey langurs (Sugiyama, 1967), females sometimes emigrate in response to the presence of a potentially infanticidal male immigrant. In howler monkeys, in contrast, patterns of female emigration seem to be more related to female-female competition than to attempts to avoid infanticide ( Jones, 1980; Crockett and Sekulic, 1984). Since mountain gorilla infants are vulnerable to infanticide by extra group males, mothers will clearly benefit from association with a male who can protect their infants effectively. In two of three cases in which an infant was killed despite the resident male’s presence, the female subsequently deserted the male for another (in the third case, it is not known whether or not she transferred)(Fossey, 1984). Even for females who have not experienced infanticide, evaluation of a potential mate’s ability to protect her infants may be the most important criterion for mate choice (Wrangham, 1979, 1982; Watts, 1983, 1989; Stewart and Harcourt, 1987). In chimpanzees, both females and their infants are vulnerable to severe aggression from males from neighboring communities, particularly when their own community range is shrinking due to intercommunity male-male competition (Goodall, 1986; see below). Consistent with this danger, at Mahale Mountains, when all but one of the adult males of K-group disappeared, K-group females transferred en masse to the neighboring M-group, which contained many adult males (Nishida et al., 1985). However, for the first few years after transfer, most male infants of transferred females were killed by M-group males, even though they were often the infants’
16
BARBARA B. SMUTS AND ROBERT W. SMUTS
likely fathers (Kawanaka, 1981; Nishida and Kawanaka, 1985; Nishida, 1990; Nishida et al., 1990). Observers speculate that the M-group males may have regarded these infants as offspring of K-group males, because the ranging habits of females that had transferred from K-group made their community identity ambiguous (Nishida and Kawanaga, 1985. Nishida, 1990).
E. DEVELOPMENT OF SOCIAL RELATIONSHIPS AND ALLIANCES As indicated above, in savanna baboons, gorillas, and chimpanzees, females choose to associate and mate with males who, in turn, help protect females and infants from aggression by other males. In several species, females who have recently given birth increase the time they spend near male “friends” (savanna baboons: Altmann, 1980; Smuts, 1985; Japanese macaques: Takahata, 1982) or near the probable fathers of their infants (gorillas: Harcourt, 1979; red howlers: Sekulic, 1983b; black spider monkeys: McFarland Symington, 1987;long-tailed macaques: Van Noordwijk and van Schaik, 1988; blue monkeys; Tsingalia and Rowell, 1984). Through these close associations with males, females probably gain protection from potential infanticide. Male-female relationsips in macaques appear to involve mutual protection against males who threaten the established social order-maturing males and male immigrants. Like female savanna baboons, female macaques form long-term, affiliative bonds with particular males who selectively protect their female affiliates and the infants of those females from aggression by other males (Kaufman, 1967; Takahata, 1982; Chapais, 1983b,c). In macaques, however, unlike baboons, females consistently prefer high-rankingmales as associates (Takahata, 1982;Chapais, 1983a,c; Hill, 1990; Manson, 1991). This is consistent with the fact that, in macaques, in contrast to baboons, only high-ranking males can effectively protect females from other males, since aggression directed up the male hierarchy is extremely rare. High-ranking males, in turn, prefer highranking females as associates (Takahata, 1982; Chapais, 1983a,c; Hill, 1990; Manson, 1991),and these females support the males during aggressive competition with other males (Koyama, 1970; Fedigan, 1976; Gouzoules, 1980; Chapais, 1983a,c; de Waal, 1989). This mutual support provides the females with protection against aggression from male immigrants and young natal males (Chapais, 1983a,c; Bernstein and Ehardt. 1986; Oi, 1990), and it helps the resident males to achieve and maintain high rank (Koyama, 1970; Bernstein, 1969; Gouzoules, 1980; Chapais, 1983a,c; de Waal, 1980). Studies of naturalistic, captive groups of vervet monkeys indicate the existence of similar, mutually supportive relationships be-
MALE AGGRESSION A N D SEXUAL COERCION
17
tween high-ranking females and dominant males (Raleigh and McGuire, 1989; Keddy Hector and Raleigh, 1992). In wild brown and wedge-capped capuchins, as well, females preferentially associate and groom with the dominant male, and both females and the dominant male direct aggression toward all subordinate males (Robinson, 1981, 1988; Janson, 1984; O’Brien, 1991). Since infanticide has been observed in capuchins (Valderrama et al., 1990), O’Brien (1991) speculates that a strong association with the dominant male may help females to obtain protection for their infants. Bonds with other females can also prove critical in reducing male aggression toward females and young (Smuts, 1987b; Nadler, 1989a; Strier, 1990). Females form coalitions against males in a wide variety of nonhuman primates, including lemurs; New World monkeys, such as howlers and capuchins; and Old World monkeys, such as macaques, baboons, vervets, patas monkeys, and several colobines (reviewed in Smuts, 1987b; see also Robinson, 1981, 1988; Sekulic, 1983a; Pope, 1990; O’Brien, 1991, for New World monkeys). Female coalitions are especially likely in response to male harassment of females or infants. In many species, females gang up on males when they attack, herd, or frighten other females (rhesus macaques: Bernstein and Ehardt, 1985; Japanese macaques: Watanabe, 1979; pig-tailed macaques: Oi, 1990; olive baboons: B. B. Smuts, personal observation; chacma baboons: Hall, 1962; silver-leaf monkeys: Bernstein, 1968; captive chimpanzees: de Waal, 1982). In common squirrel monkeys (Baldwin, 1968), patas monkeys (Hall, 1967; Loy, 1989), vervets (Andelman, 1985), and captive chimpanzees (de Waal, 1982), several females may turn on a male who solicits sex from an unwilling female. The most frequent context in which females form aggressive coalitions against males involves potential, or actual, threat to an infant (grey langurs: Boggess, 1979; Hrdy, 1977; Jay, 1963; blue monkeys: Butynski, 1982; redtail monkeys: Struhsaker, 1977; vervet monkeys; Lancaster, 1972; patas monkeys: Hall, 1968; rhesus monkeys; Bernstein and Ehardt, 1985; Lindburg, 1971; Japanese macaques; Kurland, 1977; Watanabe, 1979; long-tailed macaques: Chance et ul., 1977; olive baboons: Ransom, 1981; Smuts, 1985; common squirrel monkeys: Baldwin, 1968; red-backed squirrel monkeys: Baldwin and Baldwin, 1972; wedge-capped capuchin monkeys: Valderrama et al., 1990; red howlers: Sekulic, 1983c; Pope, 1990; ring-tailed lemurs: Pereira and Weiss, 1991). In species in which females normally remain in their natal groups, female-female coalitions typically involve close kin and are usually directed against females and juveniles from other matrilines (reviewed by Walters and Seyfarth, 1987). In striking contrast, when the target is an adult male, females often form coalitions with females to whom they are not closely related (rhesus monkeys: Bernstein and Ehardt, 1985; red-
18
BARBARA B. SMUTS A N D ROBERT W. SMUTS
backed squirrel monkeys; Baldwin and Baldwin, 1972;grey langurs: Hrdy , 1977;olive baboons: B. B. Smuts, personal observation; vervets: Cheney, 1983b;bonobos: Kano, 1987; Furuichi, 1989).Such coalitions can mobilize very quickly in response to male aggression, since any females nearby can be recruited (B. B. Smuts, personal observation). This may help to explain why, as noted above, females can sometimes individually dominate males in spite of the females’ smaller size: Males may sometimes defer to individual females because of the ever-present possibility that one female opponent may suddenly become many (cf. Robinson, 1981, 1988, for wedgecapped capuchins). Thus, female cooperation against males may benefit females both in the short-term, by halting male aggression, and in the longterm, by making males more hesitant to harass females or young because of the risks of counterattack by a female mob. How effective are female coalitions in reducing male aggression? In Japanese macaques (Packer and Pusey, 1979), vervet monkeys (Cheney, 1983a,b), and patas monkeys (Hall, 1967), female coalitions can drive males from the troop or prevent them from entering in the first place. Among capuchins, female coalitions probably help to keep non-alpha males peripheral, both socially and spatially (Robinson, I98 1 ; O’Brien, 1991). In wild red colobus monkeys, female-female coalitions have been observed to kill immigrant males (Starin, 1981), and among captive talapoin monkeys, female-female coalitions have also resulted in killing of males (Rowell, 1974). In grey langurs and red howlers, however, female coalitions are not very effective against infanticidal males (Hrdy, 1977; Crockett and Sekulic, 1984). Few data are available to evaluate the effectiveness of female coalitions against males. For instance, no published data indicate whether female coalitionary aggression toward a male reduces the likelihood that he, or male witnesses, will show subsequent aggression toward females or young. Clearly, this topic deserves further attention.
F. FORMOF THE SOCIAL SYSTEM Until this point, we have considered how, given particular features of the social system (e.g., presence of related females; one-male vs. multimale groups), females may develop counter strategies to resist male aggression. Here, we briefly consider how sexual coercion and female strategies to resist it may influence the form of the social system itself. Mountain gorillas provide the clearest evidence that male sexual coercion and female counterstrategies can determine the form the social system takes. In these apes, almost all infants who lose the protection of a mature silverback male (in most cases, because he has recently died) are soon
MALE AGGRESSION AND SEXUAL COERCION
19
killed by other males (Watts, 1989). In contrast, contrary to Fossey's earlier (1984) suggestion, recent data indicate that infants living in a group with a mature silverback are rarely killed (Watts, 1989). These observations provide strong support for Wrangham's hypothesis that infanticide is the selective force responsible for group-living in gorillas ( Wrangham, 1979, 1982, 1987a; Watts, 1983). Because females rely for protection primarily on the silverback male, rather than on other females (Watts, 1989), the gorilla social system is based not on bonds between related females, but on bonds between (usually unrelated) females and the adult male(s) in the group (some gorilla groups have more than one mature male: Harcourt, 1979; Stewart and Harcourt, 1987). Male sexual coercion may also help to explain the distribution of onemale versus multimale polygamous primate groups-a problem that remains unresolved despite numerous attempts to explain it in terms of male competitive strategies (Glutton-Brock et al., 1977; Ridley, 1986). Several people have argued that we also need to consider the effect of female strategies on the number of males in the group (Wrangham, 1980a; van Schaik and van Noordwijk, 1989; Altmann, 1990). Altmann (1990) proposes that the threat of male infanticide may result in the evolution of synchronized female ovulation, which in turn will make it more difficult for one male to control all of the fertile females in his group. This will result in a transformation from one-male to multimale groups (see Section VII for a discussion of why infanticide is generally reduced in multimale groups). V.
MALE AGGRESSION AGAINST FEMALES I N CHIMPANZEES
Chimpanzees have been studied continuously and intensively for more than 25 years at two study sites in Tanzania, Gombe National Park (Goodall, 1986) and Mahale Mountains National Park (Nishida, 1990). Although they have also been studied at other sites in East, Central, and West Africa (Heltne and Marquardt, 19891, these studies have not yet produced detailed information on male aggression against females. Thus, it remains to be seen whether the patterns observed at Gombe and Mahale characterize all chimpanzees or are limited to populations living in particular areas. Chimpanzee males show two main kinds of aggression against females: aggression against potential mates from the same community and aggression against nonestrous females from neighboring communities. Each kind is reviewed in turn.
20 A.
BARBARA B. SMUTS AND ROBERT W. SMUTS
MALE AGGRESSIONTOWARD POTENTIAL MATES
Goodall succinctly summarizes the role of male aggression in chimpanzee sex as follows: “Almost always, unless he is crippled or very old, an adult male can coerce an unwilling female into copulating with him” (1986, p. 481). In chimpanzees, males copulate under three different circumstances (Tutin, 1979; Hasegawa and Hiraiwa-Hasegawa, 1983, 1990):promiscuous, opportunistic mating, which involves frequent copulations with many different males in the group setting; possessive mating, which involves a single male’s attempts to monopolize copulations in spite of the presence of other males; and consortships, in which mating takes place between one male and one female who travel apart from the rest of the community for several days or weeks. Promiscuous, opportunistic mating typically occurs early in the female’s cycle before her swelling reaches maximum tumescence, and is unlikely to result in fertilization. As she nears ovulation, she will typically either participate in a possessive mating relationship (most likely involving the alpha male), or form a consortship. Male aggression against females occurs in all three contexts but especially during consort formation (Goodall, 1986). Among chimpanzees at Gombe, Tanzania, consortships are probably responsible for at least one-third of all conceptions, and they greatly improve a lower ranking male’s chances of fathering offspring (Goodall, 1986). It is thus not surprising that males appear highly motivated to form consortships. In order to do so, they must convince a female to follow them away from other males and to remain with them for at least several days (sometimes as long as 5-6 weeks) until her sexual swelling begins to subside, which indicates that ovulation has occurred. In order to accomplish this end, males employ what Goodall terms “a fair amount of brutality” (1986, p. 453). Males often try to initiate consortships with a female long before her sexual swelling reaches the full size associated with ovulation. The male’s apparent goal is to escape the rest of the group early, before competition for the female becomes too intense, and then to sequester the female through the period of ovulation. Aggression is most common during the early stages of consortship, when the male is trying to lead the female away from other males by traveling away from the core area of the community range (Tutin, 1979; Goodall, 1986). During this time, the female often refuses to follow the male, and she may scream, which sometimes attracts other males. If she is approaching ovulation, a higher ranking male may disrupt the consortship and she can escape her suitor. However, if she is not fully swollen, other males show little interest and she has a harder time escaping.
MALE AGGRESSION AND SEXUAL COERCION
21
Goodall (1986) reports that if the female refuses to accompany the consorting male, he will often use violence to force her to follow him. For example, Evered spent 5 hr leading Winkle north across a valley, away from other males. During these 5 hr, he repeatedly displayed at her aggressively and attacked her six times, twice severely (Tutin [ 1975, 19791 and Goodall [ 19861provide numerous additional vivid examples of male aggression in this context). Once the pair has moved far from the core of the community range, the female becomes more cooperative (probably because she is in an unfamiliar area and relies on the male for protection) and the male becomes more relaxed and tolerant (probably because he has left his mating competition far behind)(Goodall, 1986). Male aggression appears to be quite effective in convincing females to go on consort. This is well illustrated by the case of Jomeo, an adult male who showed the lowest rates of punitive aggression toward consort partners. He was also least successful in forming consortships and was the only adult male who is thought not to have sired any offspring. The significance of male aggression during consort formation may help to explain why males frequently conduct severe, apparently unprovoked attacks on cycling females whose sexual swellings have not reached full tumescence. Goodall (1986) hypothesizes that these attacks function as intimidation designed to increase the chances that the female will submit to the male’s advances in the future. Similarly, she argues that when a female appears to follow a male on consort voluntarily, her lack of resistance does not necessarily indicate willing participation; rather, it may simply reflect previous experiences with male aggression. Along the same lines, the low frequency with which females ignored adult male invitations to copulate (4.1%) may also reflect previous experience with male aggression. When a female did ignore a male’s invitation to copulate, on one out of every five occasions he responded with aggressive displays or chases and she gave in. These hypotheses linking female acquiescence to previous aggression, or to the expectation of future aggression, seem intuitively reasonable but are difficult to test (see Section VIII,B for further discussion).
B. MALEAGGRESSION AGAINST FEMALES FROM OTHERCOMMUNITIES At Gombe (Pusey, 1979; Goodall, 1986) and Mahale Mountains (Nishida, 1979; Nishida and Hiraiwa-Hasegawa, 1985), young, sexually cycling, nulliparous females typically transfer, either temporarily or permanently, to neighboring communities; while there, they mate with community males. Males welcome such females and sometimes even pro-
22
BARBARA B. SMUTS A N D ROBERT W. SMUTS
tect them from hostility by resident females. In dramatic contrast, when chimpanzee males encounter mature, anestrous females from another community, they typically respond with intense, sometimes lethal aggression, as illustrated by the killing of the old female, Madam Bee, at Gombe. The attacked females are not immigrants but are encountered in areas of overlap between the ranges of the two communities or in their own community range during invasions by neighboring males (Bygott, 1972; Goodall et ul., 1979; Goodall, 1986; Nishidaand Hiraiwa-Hasegawa, 1985). From 1975 until 1982, observers at Gombe witnessed 25 encounters between adult males from the habituated community and strange, anestrous mothers from neighboring communities (Goodall, 1986). Nineteen of these encounters were aggressive, involving chases or attacks. Fifteen attacks were observed, and, with one exception, they were extremely severe. Three attacks resulted in the death of the female’s infant. In 10 cases, observers were able to see the victim after the attack. Each time she was bleeding heavily from wounds on the limbs and/or back and, in at least 8 cases, on the face or head; some females may have died of their wounds. Males showed a marked degree of cooperation in this context. All of the attacks involved aggression by more than one male; some involved as many as six males. The males often embraced one another before attacking the female. In one case the males persistently “hunted” (Goodall’s term) a strange female before attacking her, and, in another case the males cooperated to surround the female as they sometimes do when hunting baboons (Goodall, 1986, p. 494). Several similar attacks have also been observed at Mahale Mountains (Nishida and Hiraiwa-Hasegawa, 1985). In two instances involving the same female, observers intervened because they were certain she would be killed (Nishida and Hiraiwa-Hasegawa, 1985). At both Gombe and Mahale, although infants may be killed and even cannibalized during these attacks, observers gained the impression that the males’ aggression was directed primarily at the mother (Goodall, 1986; Nishida and HiraiwaHasegawa, 1985). Several explanations have been proposed to account for aggression toward anestrous females from other communities. Wolf and Schulman (1984) argued that males attack older females because they have low reproductive value, and, if killed, additional habitat becomes available for younger females of higher reproductive value who may eventually mate with the killers. Many of the females attacked by males from other communities were not, however, especially old (Goodall, 1986; Nishida and Hiraiwa-Hasegawa, 19851, so this explanation cannot account for all of the cases. Nishida and Hiraiwa-Hasegawa (1985, p.12) speculated that, by attacking neighboring females who may compete with resident females for
MALE AGGRESSION A N D SEXUAL COERCION
23
food and other resources, the males may “court the favor” of resident females. However, resident females will rarely witness such attacks, since they are relatively uncommon, and typically only one or two resident females are likely to be present (at Gombe, on average, only I .25 resident females were present during attacks on strange females, based on data in Goodall, 1986, Table 17.2). Goodall (1986) provides a third hypothesis, suggesting that repeated brutal attacks on mothers may facilitate recruitment of their daughters to the attacker’s group. In support of this idea, she notes that, at least at Gombe, many daughters retain close bonds with their mothers and remain as residents in their natal groups. If the mother-daughter bond is weakened due to repeated attacks, or destroyed because the mother is killed, the daughters may be more likely to transfer permanently to the neighboring group. Consistent with this explanation, all but one of the (at least) five attacks on the old female, Madam Bee, occurred when the attacking males were recruiting her daughter, Little Bee; during this period, Little Bee transferred to their community. After Madam Bee’s death, her other daughter, Honey Bee, associated with the attackers’ community off and on for 3 years. If Goodall’s explanation is correct, then male aggression toward females from other communities would qualify as a form of sexual coercion (although in this instance the individual who directly suffers the cost of the coercion is not the males’ potential mate, but her mother). Whatever the explanation for the brutal attacks on strange females, they clearly occur regularly at Gombe and Mahale, and thus constitute an important selection pressure influencing the behavior of female chimpanzees. Female chimpanzees forage, often on their own with dependent young, in dispersed, but overlapping, home ranges. Males range more widely and cooperate in defending a community range that encompasses that of several females. As adults, and often after transferring from their natal communities, female chimpanzees become clearly identified with a particular community, i.e., with a particular group of males (Goodall, 1986; Nishida and Hiraiwa-Hasegawa, 1987). Although female dispersion is probably a product of feeding competition (Wrangham, 1975, 1979), the fact that females “belong” to a particular male community, rather than ranging and associating freely regardless of community boundaries, is probably a response to violence by males from neighboring communities. This conclusion is supported by observations from Mahale Mountains indicating that infants of lactating females with ambiguous community identity are especially vulnerable to infanticide by males (Kawanaka, 1981; Nishida and Kawanaka, 1985; Nishida, 1990; Nishida et af., 1990). Thus, among chimpanzees, as among gorillas (see above), male aggression against females appears to have influenced the form the social system takes.
24
BARBARA B. SMUTS AND ROBERT W. SMUTS
VI. MALEAGGRESSIONAGAINST FEMALES IN OTHERMAMMALS Table I summarizes information on male aggression against females in selected mammals. It is not exhaustive, and it is biased toward large, diurnal mammals whose behavior has been studied in the wild. We present the information in Table I to illustrate (a) the fact that male aggression against females and infants occurs in a variety of mammals, (b) the varied contexts and forms of this aggression, (c) the potential costs to females, and (d) the different kinds of counterstrategies that females exhibit. Most of the instances of male aggression toward females were interpreted by the authors as sexual coercion, as defined in this article. In surveying the literature on nonprimate mammals, we encountered few instances of male aggression toward females in nonsexual contexts. A. TYPESOF MALE AGGRESSION
Females in many mammalian species experience both sexual aggression and infanticide by males. Male sexual aggression appears to be most common in gregarious species in which females do not form long-term bonds with a single male (or, as in lions, with a group of allied males), so that females are exposed to a number of males competing for sexual access to them (e.g., fallow deer, bighorn sheep, African elephants, several pinnipeds, bottlenose dolphins). In contrast, females that do form longterm bonds with particular males (wild horses, lions) are usually protected from routine sexual harassment by other males and do not experience sexual aggression from their long-term male associates. These females, however, are vulnerable to infanticide (in lions) or induced abortion (in horses) during male takeovers. Female rodents and farm cats also experience infanticide when they encounter strange males. In species in which estrous females are exposed to several competing males, they are typically chased and herded, and sometimes kicked, pushed, or bitten by males attempting to mount. In some species (such as fallow deer or African elephants), males apparently do not frequently injure females, and the main costs to females of sexual aggression are probably loss of feeding time and energy expended in escape. In other species, sexually aggressive males sometimes severely injure and even kill females (e.g., several pinnipeds). In addition, in their aggressive attempts to gain access to estrous females, males sometimes cause death of infants (e.g., crabeater seals, sea lions, elephant seals). Little information is available on species in which females are solitary. In sea otters (Foote, 1970) and many other mustelids (martens, weasels, skunks, mink) and viverrids (civets, fossas, some mongooses), copulation is accompanied by intersex-
TABLE I MALEAGGRESSIONAGAINST FEMALES A N D INFANTSIN SELECTED NONPRIMATE MAMMALS‘ Species Fallow deer (Dama damn)
Social/mating system Polygynous; dominant males defend territories on leks
Context of male aggression Prolonged chases of fertile females by nonterritorial males
Potential costs to females
Female countentrategies
Energetic costs of avoiding male Remaining in territories of “sexual harrassment”; dominant males provides protection from other males potential wounding by male antlers Rocky Mountain bighorn sheep Romiscuous; multimale. Single males or groups of Potential injury from attacks by Females try to escape chasing (Ouis canodensis) multiiemale groups subordinate males chase blocking males; prevention of and blocking males; if females and push, butt. and female mate choice: unsuccessful, female mates. kick them until they submit to disruption of feeding; perhaps to avoid further copulation. “Blocking”: male restricted movements; attacks forceably sequesters female energetic costs of fleeing and mates with her; prevents her from approaching other males by herding, kicking, and pushing Wild horses and Assateague Polygyny; single-male, Males invade bands and try to Females occasionally suffer bite Wild hones: females kick, turn ponies (Equus caballus) multifemale bands steal femaks by herding. or wounds; in wild horses. 86% away. and run from males Iry to take over band by of females <6 months trying to force copulation; 41 challenging resident male; pregnant aborted when 18 attempts at forced after a male acquires new acquired by a new male: copulation were blocked by females by either method, he abortions were highly female. Ponies: females forces copuation by chasing, correlated with forced transfer bands several times biting. and mounting copulations: also stress, and appear to remain with reduced feeding efficiency males best able to protect them from harassment by other males African elephants (Loxo nia Romiscuous: fern s associate Males chase estrous femalesand Energeticcostsofescape; stress Females protest copulation africana) in groups with female kin; try to copulate attempts by young, solitary males seek estrous subordinate males and maintain proximity t o larger, females older males who protect them from other males
References Clutton-Brock e r a / . (1988); Clutton-Brock (1991)
Geist (1971): Hogg (1984)
Horses: Berger (1983, 1986) Ponies: Rutberg (1990)
Moss (1983): Poole (1989)
(continues)
TABLE I (Continued) Species
Sociallmating system
Context of male aggression
Potential costs to females
Female counterstrategies
Outof 14.419females Ildiedon On way to sea, females When females leave harem to Polygynous: dominant males Northern elephant seals sometimes permit copulation. land from injuries inflicted return to sea, Subordinate defend “harems” of up to 50 (Mirounga angustirostris) because copulating male during forced copulations: males chase females. bite females from other males escorts female to sea and unknown number died at sea: them. pin them to the ground. protects her from aggression many more suffer wounds and force copulations: by other males: females may subordinate males also invade aggregate on land to facilitate harems and try to force protection by dominant male copulations from sexual coercion by other males Males approach female with pup Females incur serious, bleeding Females counterattack and try Solitary; promiscuous andlor Crabeater seals (Lobodon to force males away: females wounds; if male separates and try to mate: males carcinophagus) poly e w u s move away from approaching mother and pup. pup dies sometimes force mothers and males pups apart: males bile neck and upper back when tryingto copulate Females flee raiding males and Subordinate males raid harems At end of season, 26% of Polygynous: dominant males Southern sea lions (Oraria sometimes escape: females females had fresh. bloody and then hit, bite, throw. and byronia) defend “harems” from other may aggregate to facilitate wounds: some pups die when abduct females and force males protection by dominant male separated from mothers copulations: subadult males from harassment by other abduct pups and try to mate males with them Potential injury from herding: Females struggle when invading Dominant males herd females Polygynous; dominant males Australasian sea lions males force copulation. but forced copulation back into their territories by defend “harems” from other (Neophoca cinerea) are rarely able to escape pushing and knockingfemales males over: invading males pin female down and force copulation Serious wounds: some fatalities Avoiding males and fighting Groups of males mob females Hawaiian monk seal (Monochus Polygynous: mating occurs in back: once bitten. females and try to mate; males bite schauinslandi) water become passive, perhaps to females on neck, head. and avoid further wounding back during copulation attempts
References L e Boeuf and Mesnick (1991): Mesnick and Le Boeuf (1991)
Siniff er a / . (1979)
Campagna el a / . (1988)
Marlow (1975)
Alcorn and Buelna (1989): Johnson and Johnson (1979)
Bottlenose dolphins (Tursiops rrunrarus)
Bisexual communities; promiscuous
Lions (Panrhera Ieo)
Bisexual groups: promiscuous
Farm cats (Felis carus)
Polygynous or promiscuous
Sea otters (Enhydro lufris)
Probably polygynous
Arctic ground squirrels
Polygynws or promiscuous
4 h)
(Spermophilus parryin
Stable coalitions of 2-3 males cooperate to herd estrous females: males prevent females from escaping by chasing. hitting. biting Stable coalitions of 2-1 males kill infants during group takeovers
Femalesare hit and bitten: some females have rakelike scars from bites: energetic costs of fleeing
Females sometimes escape from Connor el male coalitions
Infanticide acwunts for 27% of Mothers cooperate to defend all cub mortality; females young cubs from males and sometimes mortally wounded sometimes succeed; females while protecting cubs from may leave pride with older males cubs when new males take over: females delay conceptionafIer infanticide to increase probability that strong male coalition will join their pride: protection from infanticidal males may be one important selection pressure favoring association with female kin Cooperative defense by related Strange male may kill kittens Loss of kittens females: protection from infanticidal males may be one important selection pressure favoring association with female kin During copulation. the male Deep puncture wounds to nose Females fight back and sometimes struggle free grasps female by nose or face and face; eye damage; many females are scarred on nose with his teeth and sinks his and face; one female known teeth in to have died from infection in facial wound that hindered breathing Loss of young After juveniles emerge, related Infanticide by intruding males females share burrows and cooperatively maintain vigilance and defend young against intruding males ~-
01.
(1992b)
Packer and Pusey (1983a.b); Packer er a / . (1990)
Macdonald el
01.
(1987)
F w t e (1970)
McLean (1982, 1983)
(continues)
TABLE I (Continued) Species
Soeial/mating system
Context of male aggression
Potential costs to females
Female coun!erstrategies
References
Maternal aggression against male intruders deters infanticide; females mate with several males; males that have mated may be less likely to commit infanticide Pregnant females mate when they enter home range of strange male, and he does not subsequently harm their offspring Mothers attack unfamiliar males and often prevent infanticide, especially after day 2 postpartum Mothers selectively attack males shown to be infanticidal in separate tests
Wollf(1985); Wolffand Cicirello
-
White-footed mice (Peromyscus Promiscuous kucopus)
Infanticide by immigrating Loss of young males and resident males that had not sired young
Water voles (Aruicola rerresrris) Polygynous
Potential infanticide by strange males
Collared lemmings
Polygynous
Infanticide by introduced males Loss of young
Promiscuous
Infanticide by introduced males Loss of young
Potential loss of young
(Dicrosronyx groenlandicus)
Laboratory mice (Mus domesticus)
~
-_
(1989)
Jeppsson (19861
Mallory and Brooks (1978)
Elwood er 01. (1990)
All evidence is from studies conducted in the wild, except for the last two entries and data on maternal aggression in white-footed mice (Wolff, 1985).
MALE AGGRESSION AND SEXUAL COERCION
29
ual fighting (Enders, 1952; Ewer, 1973). With the exception of sea otters, little information is available on how serious the fighting is and whether females sustain serious injuries as a result.
B. COSTSOF MALEAGGRESSIONA N D FEMALE COUNTERSTRATEGIES As among nonhuman primates, quantitative data on the costs of male aggression in nonprimate mammals are rare. Le Boeuf and Mesnick (1991) estimate the probability that an adult female elephant seal will be killed by a male as .001 per season, and conclude that “this could be a significant selection pressure . . . that might have the effect of shaping the behavior and morphology of females to avoid being victimized.” Packer and Pusey (1983a)report that over one-fourth of all infant mortality in lions is due to infanticide by males. Female counterstrategies include physiological responses that delay conception (lions) or abort fetuses (the Bruce effect in many rodents; Huck, 1984). Frequent copulation and delayed conception in lions are hypothesized to increase the probability that a large male coalition will join the group, which in turn increases the chances that the females will be protected from a subsequent male takeover for long enough to bear and raise cubs (Packer and Pusey, 1983a,b). The Bruce effect has been interpreted as a means by which females cut their losses when infanticide appears likely (Huck, 1984). In contrast, Berger (1983)argues that abortion in female horses subject to forced copulation provides no benefit to the females, since infanticide will not occur if the fetus survives. (Kirkpatrick and Turner [1991] point out that forced copulations and induced abortion do not occur in all wild horse populations.) Pseudo-estrus during pregnancy, as described for several female primates confronted with strange males (e.g., grey langurs and red colobus), also occurs in water voles, and Jeppsson (1986) argues that it functions to reduce the vulnerability of the females to male infanticide. Behavioral counterstrategies frequently include attempting to escape sexually aggressive males. Fighting back occurs but is less common, presumably because of the risks of injury. Lionesses, for example, attack males trying to kill their young and are sometimes mortally wounded in the process (Packer and Pusey, 1983a). Experiments with laboratory mice show that females with pups can discriminate between infanticidal and noninfanticidal strange males and are more likely to attack the former (Elwood et al., 1990). In some rodents, maternal aggression is very effective in preventing infanticide (e.g., white-footed mice: Wolff, 1985; collared lemmings: Mallory and Brooks, 1978), but in others, it is not (e.g., artic ground squirrels: McLean, 1982).
30
BARBARA B. SMUTS AND ROBERT W. SMUTS
Sometimes, females submit to copulation with an aggressive male. Several authors interpret such submission as a tactic to avoid further aggression (bighorn sheep: Hogg, 1984; Hawaiian monk seals: Johnson and Johnson, 1979). Mesnick and LeBoeuf (1991, p. 272) characterize such tactics as trading sex for protection. Female association with particular, protective males appears to be the most common mammalian strategy to reduce vulnerability to male sexual aggression and infanticide. These protective associations range in duration from years (e.g., horses/ponies, lions) to weeks (elephant seal harems), days (fallow deer, mountain sheep), or mere minutes (elephant seals, when females attempt to return to sea). Wrangham (1986, p. 463) refers to such protective males as “hired guns” and emphasizes that females need to form these protective associations with some males only because of the coercive behavior of other males. Females employ diverse tactics to obtain the protection of dominant males. Female northern elephant seals (Cox and Le Boeuf, 1977) and female African elephants (Moss, 1983; Poole, 1989) emit a loud vocalization when mounted by subordinate males. This “protest” call functions to attract a more dominant male, who will chase the subordinate away. The female then often mates with the dominant male. Female elephants, bighorn sheep, and fallow deer sometimes actively maintain proximity to a dominant male, who provides protection from other males (Moss, 1983; Poole, 1989; Geist. 1971). Female ponies transfer from band to band several times, apparently in search of males best able to protect them from harassment by other males (Rutberg, 1990). As noted above, after losing cubs to strange males, female lions adopt behaviors apparently designed to attract a large male coalition. In a few cases, selection pressures for female association with “hired guns” may account for aspects of the species’ social or mating system, as argued for gorillas and chimpanzees, above. Clutton-Brock et nl. (1988), for example, hypothesize that female choice for protective males is responsible for the evolution of leks in fallow deer (see Wrangham, 1980b, for a similar explanation for the evolution of leks in birds). Trillmich and Trillmich (1984) hypothesize that the benefits of protection by dominant males from sexual aggression by other males explains female aggregations in several pinniped species. Finally, Packer e l al. (1990) show that groupliving in female lions cannot be explained by the benefits of cooperative hunting and argue instead that one of the most important selection pressures leading to female groups is the need for cooperative protection against male infanticide. In support of this hypothesis, survival of cubs after male takeovers was significantly enhanced when two or more females were present compared to just one (Packer et nl., 1990). Macdonald et al.
MALE AGGRESSION AND SEXUAL COERCION
31
(1987) make a similar argument for the evolution of communal rearing of young by related females in domestic farm cats.
C . SIMILARITIES A N D DIFFERENCES BETWEEN NONHUMAN PRIMATES A N D OTHERMAMMALS Male aggression against females and young in other mammals shows several striking parallels with nonhuman primates and also some intriguing differences. Parallels include female vulnerability to infanticide or induced abortion when strange males invade or take over their groups, male use of aggression to herd estrous females away from other males, and the high frequency of the female "hired gun" counterstrategy. Differences include the apparently higher frequency of aggression during copulation itself in other mammals (especially in pinnipeds, mustelids. viverrids) compared with nonhuman primates; the greater frequency of sexual harassment by more than one male at a time (e.g., several pinnipeds, bighorn sheep, fallow deer) in other mammals compsred with nonhuman primates: and a bias among other mammals (with striking exceptions, e.g., horses) toward brief associations with dominant males compared to the more typical longterm heterosexual associations of nonhuman primates. In addition, the use of female coalitions to thwart aggressive males appears to be rare in other mammals compared with nonhuman primates. All of these generalizations must remain tentative until data are available to allow more systematic comparisons between different mammalian taxa. Such systematic comparisons should prove extremely useful in helping to identify the ecological, demographic, and social factors associated with different kinds and intensities of male aggression against females and young, and different kinds of female counterstrategies.
VII.
VARIATIONI N MALE AGGRESSION AGAINST FEMALES
Even in the absence of many quantitative data, it is clear that the frequency and intensity of male aggression against females vary considerably among nonhuman primates and mammals in general. For example, although male aggression against females is common in a number of primates, including gorillas (Watts, 1992), chimpanzees (Goodall. 19861, baboons (Hausfater, 1975: Smuts, 1985), macaques (Oi, 1990; Manson, 1991), white-fronted and wedge-capped capuchins ( Janson, 1986; O'Brien. I991 1, black spider monkeys (McFarland Symington, 1987), and brown lemurs (Pereira et al., 1990; M. E. Pereira, personal communication), it is very uncommon in others, such as bonobos (Kano and Mulavwa, 1984; White,
32
BARBARA B. SMUTS A N D ROBERT W. SMUTS
1992), patas monkeys (Loy, 1989),red-backed squirrel monkeys (Boinski, 1987), brown capuchins (Janson, 1984, 1986), woolly spider monkeys (Strier, 1990, 1992),and black-and-white ruffed lemurs (Foerg, 1982;Kaufman, 1991). Similar variation exists among other mammals. It is difficult at present to investigate the factors responsible for this variation, because of enormous gaps in the data. As indicated at the start of this article, for most mammals, information on the presence or absence of male aggression against females and male sexual coercion is entirely lacking. It might be argued that when a detailed account of a species’ social behavior fails to highlight male aggression against females, it can safely be interpreted as an indication that such aggression is rare or absent. However, we disagree with this suggestion, since, until recently, many accounts of well-studied species such as baboons and chimpanzees (and humans), in which we now know that male aggression against females is common, failed to emphasize its frequency, or even failed to mention it at all. Thus, at present, our analysis of interspecific variation must be limited to those species in which authors describe male aggression against females or explicitly indicate its rarity or absence. Because these species represent a small proportion of all primates (and an even smaller proportion of all mammals), many of the hypotheses presented below will require modification in light of new data. Our purpose, then, is to stimulate further research and theorizing, rather than to attempt a definitive assessment of interspecific variation and its causes. Since all but the first of the factors described below is an aspect of the social structure of mammalian groups, it is important to begin by stating our assumptions with respect to the relative influence of ecological and social factors on social structure. We follow Wrangham’s model of primate social systems (1979,1980a;see also van Schaik and van Hooff, 1983; van Schaik, 1989). Wrangham argues that food distribution is the primary determinant of the distribution and grouping of females, which, in turn, is the primary determinant of male mating strategies and the distribution of males. Since male strategies may impose costs or confer benefits on females, male strategies may, however, exercise a secondary influence on female social patterns, which may then have a secondary influence on males. The interaction is complex and the extent to which male aggression against females and female counterstrategies are facilitated or constrained by ecological factors is not well understood. In general, we assume that ecological factors are primarily responsible for philopatry and femalebonding, as occurs in most Old World monkeys (Wrangham, 1980a). On the other hand, we assume that there is little or no ecological pressure for female grouping in any of the apes (Wrangham, 1979, 1987a), and hypothesize that male aggression is the principal selection pressure leading
MALE AGGRESSION AND SEXUAL COERCION
33
female gorillas to aggregate around (usually) one male and for female chimpanzees to associate loosely with a group of related males (see Sections IV,F and V,B). 1. Phylogeny cannot explain variation in male aggression toward f e mules. The examples given at the beginning of this section indicate that phylogeny cannot account for much of the observed variation in male aggression against females, since all of the major primate taxa (apes, Old World monkeys, New World monkeys, prosimians), as well as several families, subfamilies, and genera, include species reported to show both high and low levels of this behavior. 2. Although increased sexual dimorphism in body size and weaponry make females more vulnerable to male aggression (Strier, 1990; Le Boeuf and Mesnick, 1991), the effects of sexual dimorphism are often swamped by other factors (Fedigan and Baxter, 1984; Kappeler, 1991). Clearly, the ability of males to physically dominate females will influence the likelihood of male aggression against females (Le Boeuf and Mesnick, 1991). For example, severe aggression in the context of copulation appears to characterize a number of pinniped species in which males are much larger than females (e.g., elephant seals, sea lions). However, sexual dimorphism alone clearly does not determine levels of male aggression against females. Consider, for example, common chimpanzees and bonobos, which show similar degrees of sexual dimorphism in body size (Jungers and Susman, 1984) but very different levels of male aggression against females (see below). Similarly, although all lemurs are monomorphic (Kappeler, 1991), in some species (e.g., brown lemurs) adult males show considerable aggression toward adult females, while in others (e.g., ring-tailed lemurs), they show none (but note that male ring-tailed lemurs do attack infants separated from their mothers [Pereira and Weiss, 19911). In many of the monomorphic lemurs, and in hyenas, in which males and females differ little in size, females consistently dominate males (lemurs: Foerg, 1982; Young et al., 1990; Kappeler, 1991; Pereira et al., 1990; spotted hyenas: Frank, 1986a,b). Along the same lines, males may be very aggressive toward females in species in which there is little size difference between males and females (e.g., black spider monkeys: McFarland Symington, 1987; bottlenose dolphins: Connor et al., 1992a;wild horses: Berger, 1986; crabeater seals: Siniff et al., 1979) and even in species in which males are smaller than females (Hawaiian monk seals: Alcorn and Buelna, 1989). Finally, among species in which males are larger than females, the extent to which males dominate females and the frequency of male aggression against females do not appear to conform closely to the degree of sexual dimorphism. Patas monkeys, for example, are among the most sexually
34
BARBARA B. SMUTS AND ROBERT W. SMUTS
dimorphic monkeys, and yet male patas rarely aggress against females (Loy, 1989). In contrast, male aggression against females is common in macaques and chimpanzees, although in these species females are 70-80% as large as males. These patterns, in turn, may reflect differences in the extent to which females form coalitions against males.
3 . Frequent coalitions among females will reduce male aggression against females. In species in which females remain with their natal kin, they can improve their ability to resist male aggression by forming alliances with other females (Smuts, 1987b; Nadler, 1989a; Strier, 1990). Examples include lions, capuchins, and many species of “female-bonded” Old World monkeys. The effectiveness of female-female alliances may depend, in part, on the degree of confluence of female interests in their struggles against males. Patas monkeys, for example. live in small groups in which only one male remains in the group throughout the year, and patas females appear to present a consistently united front against this male, which may help to account for his very peripheral status and lack of aggression toward females, despite his much larger size (Loy, 1989; Chism et al., 1984). Among macaques, in contrast, which live in groups containing several female matrilines and more than one male, the interests of different females may often conflict, so that presenting a united front against particular males is not always possible. The contrast between bonobos (pygmy chimpanzees) and chimpanzees highlights the potential significance of female-female alliances against males. In bonobos, as in chimpanzees, females transfer from their natal groups around adolescence (Nishida and Hiraiwa-Hasegawa, 1987). However, bonobo females, in contrast to chimpanzee females, routinely ally with one another against males, both in the wild (Kano, 1987; Furuichi, 1989)and in captive groups (A. R. Parish, personal communication). Paralleling this difference in female alliances are striking differences in female-male dominance relationships and the frequency of male aggression against females. Among chimpanzees, males consistently dominate females (Goodall, 19861, and, as indicated above, male aggression against females is common. Among bonobos, in contrast, “almost all males of middle to lower ranks are subordinate to full [sic] adult females” and “even the alpha male is threatened or chased by a female or a group of females” (Kano, 1987, p. 601, and male aggression toward females is rare (Kano, 1987; Furuichi, 1989; White, 1992). The importance of female allies is further underscored by Idani’s (1991) observations that newly transferred females who have not yet formed strong bonds with resident females are considerably more vulnerable to male aggression. Wrangham (1986) argued that female bonobos associate with males in order to gain protection from sexual coercion
MALE AGGRESSION AND SEXUAL COERCION
35
by other males. However, the evidence just described, combined with the absence of reports of male agonistic support of females against other males, indicates that, contrary to Wrangham’s hypothesis, female bonobos gain protection from male aggression primarily through their alliances with other females. The significance of female-female alliances against males is also suggested by data on chimpanzees, orangutans, and black spider monkeys. These three are among the few polygynous anthropoid primates in which, presumably as a result of feeding competition (Wrangham, 1979; Rodman, 1984; McFarland Symington, 1987), females cannot afford to forage routinely with other females, and in all three male aggression against females seems to be particularly common (see above). 4. Females living in one-male groups and multimale groups will experience different types of male sexual coercion. In species in which a single male typically lives with several females, sexual coercion by the breeding male should be minimal (since he is the only mate available), except at those times when outside males approach the group. (During these events, the breeding male may attempt to herd ‘‘his’’ females away from other males [e.g., mountain gorillas: Sicotte, 1989; capped langurs: Stanford, 1991; red deer: Clutton-Brock er al., 19821). In one-male groups, the breeding male may provide important benefits to his females by protecting them from sexual harassment and/or infanticide by outside males. However, females under such systems periodically suffer intense sexual coercion, in the form of infanticide, when the breeding male dies (e.g., mountain gorillas) or is challenged (e.g., grey langurs, wild horses). Estrous females living (or breeding) in multimale groups, in contrast, are expected to suffer higher rates of male sexual coercion routinely, because the constant presence of rival males will often select for sexually coercive strategies. Females living in multimale groups are also expected to suffer higher rates of nonsexual aggression, such as during feeding, because of the presence of many males. However, such females are expected to be less vulnerable to male infanticide than are females living in one-male groups, for two reasons. First, females will gain protection from infanticide by possible fathers of their infants, and/or by males who protect infants in exchange for future mating opportunities with the mother (Smuts, 1985; Smuts and Gubernick, 1992). Second, the presence of many rival males decreases the benefits to males of infanticide, since male-male competition reduces the probability that the infanticidal male will subsequently fertilize the mother. 5. Associations with particular males will reduce female vulnerability to sexual aggression. As noted above, females living in one-male groups
36
BARBARA B. SMUTS AND ROBERT W. SMUTS
may gain protection from male aggression through their long-term association with the breeding male. In species living in multimale groups, females may form long-term bonds (e.g., savanna baboons) or associate on a shortterm basis (e.g., elephant seals) with one, or a few, adult males, in order to gain protection from other males. In savanna baboons, male protection extends to the infants of female associates even when the protective male is unlikely to be the father (Smuts, 1983, apparently in exchange for future mating benefits. At least among nonhuman primates, these relationships may function as alternatives to protective alliances with other females. Therefore, affiliative heterosexual relationships are more likely, or will be more important, when sexual dimorphism is great (because female allies are less valuable),as in baboons and gorillas, and/or when females transfer from their natal groups (because related females are unavailable as allies), as in gorillas and chimpanzees. 6. Male reliance on females for “political” support will reduce male sexual coercion. When males rely on females as allies against other males, their need to recruit female coalition partners may reduce aggression, including sexual coercion, toward females. This hypothesis is consistent with the observation that male sexual coercion is relatively rare in captive chimpanzees, in which female political support is important to male status competition (de Waal, 1982), compared with wild chimpanzees, in which it is not (Goodall, 1986). In a group of free-ranging rhesus monkeys in which the alpha female’s support was critical to the high-ranking males, they never showed aggression toward her, although lower ranking males did so (Chapais, 1983a,c). Similarly, in captive vervet monkeys, in which high-ranking females strongly influence male dominance status (Raleigh and McGuire, 1989), males typically leave a high-ranking female alone after she aggressively resists mounting attempts, but they often persist in trying to mate following similar refusals by lower ranking females (Keddy, 1986). It is not clear whether reliance on females for political support inhibits male aggression toward females in other mammals. 7. The existence of male-male alliances increases female vulnerability to sexual coercion. Male aggression against females or infants in nonhuman primates almost always involves single males, but notable exceptions include spider monkeys (Fedigan and Baxter, 1984; McFarland Symington, 1987),red-backed squirrel monkeys (Boinski, 1987),and chimpanzees (see above; Goodall, 1986; Nishida and Hiraiwa-Hasegawa, 198% in which males sometimes gang up on females, and red howlers (Crockett and Sekulic, 1984; Pope, 1990), in which groups of males invade troops, evict the breeding male, and commit infanticide. In black spider monkeys, red-backed squirrel monkeys, and chimpanzees, males remain in their
MALE AGGRESSION AND SEXUAL COERCION
37
natal groups and form long-term bonds with male kin, an unusual pattern among mammals. In red howlers, invading males are often closely related (Pope, 1990). Other mammals characterized by persistent male alliances also show cooperative male aggression against females (bottlenose dolphins: Conner et al., 1992a,b)or infants (lions: Packer and Pusey, 1983a). Male cooperative coercion of females appears to be especially widespread and significant in our own species (B. B. Smuts, 1992, 1993). For heuristic purposes, we have stated each of these hypotheses independently, but the challenge is to determine how these variables, and others, interact to produce observed levels of male aggression against females.
VIII.
EVALUATING THE SEXUAL COERCION HYPOTHESIS
In this article, we have described many examples of male aggression against females that are hypothesized to function as sexual coercion, that is, aggressive acts that appear to increase the male's mating success at some cost to the female. Here we briefly consider the kinds of evidence needed to determine, in particular instances, whether (a) male aggression against females increases male mating success and (b) male aggression against females inflicts costs on females. A.
EVIDENCE SHOWING THATMALEAGGRESSIONAGAINST FEMALES CORRELATES WITH INCREASED MATING SUCCESS
Quantitative evidence exists for a few species showing that male aggression is correlated with increased mating activity. For example, among Southern sea lions, when a peripheral male uses aggression to abduct a female from the group, he copulates more often than peripheral males that did not abduct afemale (Campagna et al., 1988).Assuming that copulations with abducted females occasionally lead to fertilization, this evidence indicates that abduction leads to reproductive benefits. In other cases, it may be harder to interpret correlational evidence. Among Japanese macaques, for example, dyads in which the male showed aggression toward the female during the mating season were significantly more likely to copulate than dyads in which the male showed no aggression (Enomoto, 1981). It is not clear, however, whether aggression toward females caused increased male mating success; it is possible that dyads that copulated showed a higher frequency of male aggression toward the female simply because the members spent more time together.
38
BARBARA B. SMUTS AND ROBERT W. SMUTS
B. EVIDENCE CONCERNING THE SPECIFIC SEQUELAE OF MALE AGGRESSION AGAINST FEMALES The difficulties mentioned above in interpreting correlational evidence emphasize the importance of prolonged observations of particular individuals to document the specific events that follow male aggression against females. For example, during focal samples of estrous female rhesus monkeys, Manson (1991) documented the effects of escalated attacks by males on females. Most such attacks occurred when the female’s nearest adult male neighbor was lower ranking than the attacker or from a different group. For each male attack on a female associating with another male, Manson determined whether the female subsequently first approached the attacker or her prior associate, and whether she eventually mated with either male. Following attacks, females approached their previous associates more often than they approached attackers, and they were also more likely subsequently to copulate with previous associates than with attackers. Manson (1991, p. 24) concludes that “male attacks on estrous females that were accompanying lower-ranking males did not, in the short run, induce the female to copulate with the attacker rather than the accompanying lower-ranking male. Attackers may have increased their chances of copulating with the victim on subsequent days, but these effects are more difficult to assess, because of problems in determining the ‘expected’ probability that a pair will copulate in the absence of attack.” Huffman (1987) reached similar conclusions for Japanese macaques. These studies illustrate a serious difficulty involved in determining the consequences of male aggression against females: although we can document the events following an aggressive event, we have no way to know for certain what would have happened had the male not shown aggression toward the female. There are several approaches to this problem. For a given time interval that is likely to encompass both male aggression toward females and male mating with those same females, one could compare rates of copulation by males with females they showed aggression toward compared with rates of copulation by those same males with females they did not show aggression toward. The results would have to be interpreted with caution, because the presence or absence of aggression in a particular dyad may reflect other aspects of the relationship. For example, if a male has reason to believe that a female is likely to prefer him as a mate, he may have less need to show aggression toward her than toward a female who does not prefer him. Data on frequency of aggression and rates of copulation would in this case be confounded by the effects of female preference. Another approach would be to compare the aggressive behavior and subsequent
MALE AGGRESSION AND SEXUAL COERCION
39
mating activities of different males, to see whether those who showed more aggression mated more. Again, however, one would need to consider carefully the possibility that differences among the males in the frequency of aggression reflected differences in their need to use aggression as a reproductive tactic. Suppose some males are in a better position to offer females benefits that lead females to prefer them as mates. Males less able to provide benefits might improve their mating success through the use of aggression, but if this strategy is generally less successful than providing females with benefits, the data will show a negative correlation between rates of male aggression and mating success. These hypothetical examples are not meant to indicate that it is impossible to determine whether male aggression sometimes increases mating success but rather to emphasize the need to examine male aggression against females in conjunction with detailed knowledge of individual life histories, particular social relationships, and the alternative reproductive strategies available to individuals. In investigating this phenomenon, it will be important to establish general patterns by collecting data on large numbers of individuals. However, because of the difficulties of interpretation discussed above, it will also be critical to obtain very detailed evidence on the relationship between aggression (or lack of it) and mating (or lack of it) in particular dyads over long periods of time. Such “case study” data should help to identify the significance male aggression toward females holds in particular species, or even among particular types of individuals (e.g., adolescents). An example of such a case study approach comes from Nadler and Miller’s (1982) research on mating in captive gorillas. Sexual behavior was quantified each day for four females paired with each of two males for two consecutive cycles. Several results suggested a causal relationship between male sexual aggression and copulation frequency. First, one male consistently showed more sexual aggression than the other, and he also consistently copulated more often. Second, when data for each male were examined separately, the frequency of copulation-days (days in which any copulation occurred) was directly related to the frequency of aggression shown toward different females. The authors considered two alternative explanations for these findings. First, perhaps the females were simply more attracted to the more aggressive male. This hypothesis was rejected, because females tried more often to avoid the more aggressive male. Second, perhaps the direction of causality was reversed, so that male aggression was stimulated by sexual interaction. To test this hypothesis, the authors examined the frequencies of female presenting (which typically preceded copulation) and of male aggression across the two consecutive cycles for each of seven pairs (one pair was removed from the study due
40
BARBARA B. SMUTS AND ROBERT W. SMUTS
to illness). In each pair, the frequency of presenting increased from cycle 1 to cycle 2, the result “expected if the females learned during cycle 1 that such presenting reduced male aggression” (Nadler and Miller, 1982, p. 236). If female presenting stimulated male aggression then male aggression should also have increased from cycle 1 to cycle 2, but the reverse was found for all seven pairs. The authors conclude that “male aggression, most evident in the first cycle, stimulated heightened levels of female presenting and copulation, rather than the reverse” (p. 237). A similar case study approach could be employed in group-living animals, by documenting patterns of sexual aggression and mating within dyads across time.
c.
EVIDENCE CONCERNING WHICH MALESAREMOSTLIKELY TO SHOW AGGRESSION AGAINST FEMALES, A N D WHICHFEMALES AREMOST OFTENVICTIMSOF MALEAGGRESSION
Such evidence, particularly when it is combined with knowledge about life histories and social relationships, may help to identify the functional consequences of male aggression against females. For example, the fact that estrous females in many species receive more aggression from males than do anestrous females provides support for the hypothesis that males use aggression to obtain mates. The fact that peripheral and/or subordinate males are often the ones most likely to show aggression toward estrous females indicates that aggression may sometimes be a competitive tactic adopted by males that are at a mating disadvantage.
D. EVIDENCE CONCERNING THE EFFECTS OF PRESENCE OR ABSENCE OF OTHERMALESON MALEAGGRESSION TOWARD FEMALES In bighorn sheep, dominant males associating with estrous females away from other males exhibit slow and gentle courtship. These same males aggressively herd females when rival males are present (Geist, 1971). Similarly, in an experimental study of male-female pairs of crab-eating macaques housed together, the rate of male aggression toward the female increased from a low frequency of once every 3 to 4 hr when a male and female were housed alone to over seven times an hour in the presence of a rival male (Zumpe and Michael, 1990). Such evidence supports the hypothesis that males use aggression against females to reduce the likelihood of losing mating opportunities to rival males. In such cases, however, we must be able to rule out the alternative hypothesis that males show less aggression toward females when other males are not present simply
MALE AGGRESSION AND SEXUAL COERCION
41
because females show less resistance when other males are not available as alternative mates. THE COSTSTO FEMALES OF E. EVIDENCE REGARDING MALE AGGRESSION
For a behavior to qualify as sexual coercion by our definition, it must not only benefit the male but must also inflict a cost on the female. Many more data are needed quantifying the costs to females of male aggression, which may range from subtle costs, such as increased energetic expenditure or loss in feeding efficiency, to dramatic costs, such as severe injury or even death. If these costs can be translated into effects on female reproduction, we may discover that, as a result of the costs they impose on females, male reproductive strategies sometimes decrease the reproductive rate of a species or population (Mallory and Brooks, 1978). The existence of male aggression against females does not in and of itself demonstrate a cost to females. In theory, a female might avoid an approaching male (i.e., be chased by him) or resist copulation or mateguarding to determine his health and vigor or to incite competition among surrounding males in order to identify the “best” male present (Thornhill and Alcock, 1983; Westneat et al., 1990). For example, female bighorn sheep repeatedly run away from groups of chasing males but eventually submit to copulation with the most dominant male of the chasing group. Is the female a victim of male aggression, or is she using the male tendency to chase estrous females as an efficient means of identifying the strongest male in the vicinity? The critical issue here is not whether the female benefits from mating with the strongest male (presumably she does benefit, given the alternatives) but whether the benefits the female receives are important in and of themselves (e.g., being chased allows her to mate with the male with the “best genes”) or whether the benefits are meaningful only because male aggression exists (e.g., submitting to copulation with the dominant male is the best way for the female to avoid further costs, given the existence of male sexual aggression). In other words, we need to ask whether, if the female had complete control over male behavior, would she choose to be subject to male aggression or not? Observational evidence alone may sometimes allow us to infer the answer to this question. If, for example, females routinely suffer serious injuries, presumably they would be better off if male aggression did not exist. Similarly, we may infer that male aggression is costly if females persistently resist it in ways that risk injury (e.g., fighting back) or endanger their infants. In contrast, female razorbills visit mating arenas, where they
42
BARBARA B. SMUTS A N D ROBERT W. SMUTS
have opportunities to mate with males other than the male they are paired with. In this situation, females frequently resist (always successfully) copulation attempts (Wagner, 1991). Because these visits are apparently completely voluntary, and because females sometimes visit the mating arenas after they have layed their final clutches (i.e., females do not need to visit these areas to be fertilized), Wagner (1991) concluded that exposure to male copulation attempts is beneficial rather than costly to females. In other cases, experimental techniques may help to determine whether females will choose to avoid male aggression, or its consequences, when they have the option to do so. Nadler's experiments with captive apes, described earlier, showed that when females could completely control their associations with males, copulations at times other than mid-cycle, which were normally associated with male aggression, ceased entirely (Nadler, 1982, 1988; Nadler and Miller, 1982). More experiments examin-, ing the interplay between male aggression and female mate choice are needed.
F. EVIDENCE FROM A WIDEVARIETYOF SPECIES, INCLUDING THOSE I N WHICHMALEAGGRESSION AGAINST FEMALES A N D INFANTS Is MINIMAL As noted above, because male aggression against females has so far received little systematic attention, it is difficult to know whether the absence of reports of male aggression against females indicates that it does not occur, or that it has been overlooked. For this reason, we have focused on those species in which male aggression against females or infants has been reported, and have said little about those in which it has not. However, if we want to understand the selective significance of this phenomenon and the factors responsible for variation in its frequency and intensity, we need to know not only about its occurrence, but also about the species and circumstances in which it occurs only rarely or not at all. This will require the collection and reporting of "negative evidence." Such evidence could prove critical to identifying effective female counterstrategies. For example, among savanna baboons, male infanticide has been reported on numerous occasions (Collins et al., 1984). In contrast, among their relatives the macaques, which have been studied equally intensively, it has been reported only once (Ciani, 1984). Macaques and savanna baboons have very similar social systems, but in macaques females routinely form coalitions against males, whereas in baboons they do not, presumably because baboons show much greater sexual dimorphism in body size and weaponry. This comparison suggests that the formation of female-female coalitions in macaques may be an effective counterstrategy against male
MALE AGGRESSION AND SEXUAL COERCION
43
infanticide. More data are needed to test this hypothesis, but it illustrates the way that comparative data on variation in female and infant vulnerability to male aggression may deepen our understanding of this phenomenon.
IX. IMPLICATIONS OF MALESEXUAL COERCION FOR SEXUAL SELECTION THEORY The evidence reviewed above indicates the widespread existence of male aggression against female mammals. Although not all male aggression against females occurs in a sexual context, much of it does, and a significant proportion of such aggression apparently functions as sexual coercion; that is, it increases male mating success relative to other males, at some cost to the female. Male aggression in general, and sexual coercion in particular, also occur in other animals (e.g., insects: Borgia, 1980; Thornhill, 1980; Arnquist, 1980; birds: Beecher and Beecher, 1979; McKinney et al., 1983; Emlen and Wrege, 1986). Male sexual coercion appears to have influenced myriad aspects of female behavior and life histories, including female choice of social partners and, in some cases, the form of the social system itself. These results suggest that sexual coercion is an important male reproductive strategy that can impose strong selection pressures on both sexes. Yet the significance of sexual coercion has not been widely recognized. We suggest that this lack of recognition results from the failure to acknowledge sexual coercion (usually male coercion of females) formally as a third form of sexual selection comparable to the two forms that have been recognized ever since Darwin: intrasexual competition for mates (usually between males) and intersexual mate choice (usually by females) (Darwin, 1871). Like these other forms of sexual selection, sexual coercion involves behaviors that influence mate selection and retention through interactions with conspecifics (Darwin, 1871). Similarly, successful coercion of females can increase male mating success at the expense of other males, just as do successful fighting or successful mate attraction. When sexually coercive strategies are discussed in the literature, they are usually treated either implicitly (e.g., Hogg, 1984) or explicitly (e.g., West-Eberhard et a/., 1987) as an aspect of male-male competition, probably because they are a means by which some males obtain mates at the expense of others. However, female choice is also a means by which some males obtain mates at the expense of others: yet Darwin (1871), Fisher (1930), Trivers (1972), and many others have clearly recognized the importance of conceptualizing mate choice as a distinct form of sexual selection. Similarly, it is imperative to identify intersexual coercion as a
44
BARBARA B. SMUTS A N D ROBERT W. SMUTS
form of sexual selection that is conceptually distinct from, but interacting with, intrasexual competition. We suggest that all three forms of sexual selection are intimately related, and that each influences and is influenced by the others. Bradbury and Davies (1987) proposed that nearly all mating systems include a mix of intrasexual competition and intersexual mate choice, and they argued that improved understanding of animal mating behavior requires explicit consideration of how these two forces interact. Empirical studies increasingly support the validity and usefulness of this approach (e.g., McPeek, 1992; Rosser, 1992). We wish to extend Bradbury and Davies’ argument to include explicit consideration of the potentially critical role that intersexual coercion and female resistance to it may play in this dynamic system. Thus, for example, previous theoretical treatments of social evolution have focused on how male-male competition and female choice interact in particular ecological circumstances to produce characteristic mating systems (e.g., Emlen and Oring, 1977; Clutton-Brock and Harvey, 1978). We suggest that an expanded theoretical perspective that emphasizes male sexual coercion and female strategies to resist such coercion will significantly improve our understanding of &heevolution of social systems, mating systems, and related aspects of animal behavior (see Section IV,F for examples).’ Increased attention to the potential significance of male sexual coercion and female resistance to it should help transform implicit assumptions into explicit hypotheses amenable to evaluation. A good example of the need to make assumptions explicit concerns the treatment of male-male contest competition (i.e., fighting, dominance displays, etc.) in the sexual selection literature. Authors frequently imply that the outcome of male-male contest competition largely determines differential male mating success. This conclusion treats females as passive resources. Others recognize the potential importance of female choice, but claim that it is often constrained, or negated, by the outcome of male-male competition (e.g., Thornhill, 1979). However, the outcome of male-male competition, in and of itself, constrains female choice only when dominant males succeed in keeping other males away from females, so that female options are limited to mating with the winners of male-male competition, or not mating at all. I In this article, we have emphasized male sexual coercion of females, along with male-male mating competition and female mate choice, but a complete understanding of social evolution will require investigation of female sexual coercion of males, as well as female-female mating competition and male mate choice. Female sexual coercion is expected to occur, at least occasionally. in “sex-role reversed” species, in which females compete intensively for mating opportunities with males (Gwynne, 1991).
MALE AGGRESSION A N D SEXUAL COERCION
45
If winning males are not able to keep other males entirely away from some females, then winning males gain a reproductive advantage if and only if they either (a) coerce females into mating with them, or (b) are freely chosen by females as mates (because they offer “good genes,” protection, resources, etc.). (Note that if females mate with dominant males because dominant males punish them if they do not, then it is not an instance of free choice but instead represents a response imposed by sexual coercion, and as such falls under [a], above.) Thus, unless males succeed in keeping all other males away from females (which is probably relatively rare in most mammals), the outcome of male-male contest competition has meaningful reproductive consequences only in conjunction with eitherfemale mate choice or male sexual coercion (or both).
To realize the implications of this insight, we must explore the complex interactions between the different components of sexual selection. Consider, first, how the possibility of effective female resistance to male sexual coercion might influence the intensity of male-male competition. If males cannot coerce females into mating with them, two possibilities exist. 1. Males may compete intensively if females benefit from choosing males that have demonstrated superior fighting ability. For example, CluttonBrock et al. (1988) suggest that female fallow deer benefit from associating and mating with dominant males because these males are best able to provide females with protection from sexual harassment by other males. In species in which females freely choose their mates, but males kill infants, females may choose to mate with dominant males because they provide the most effective protection against infanticide. Pereira and Weiss (1991) suggest that this is why female ring-tailed lemurs choose to mate with dominant males. These considerations may help to explain why in both species, despite the obvious exertion of female mate choice, males compete intensely and aggressively for dominance status. 2. In contrast, if females can freely exert mate choice but have no reason to mate with the males showing the highest competitive ability, male contest competition for mates should be minimal. Woolly spider monkeys may be a good example (Strier, 1990, 1992). In this species, females and males are the same size, perhaps because locomotor and energetic constraints set an upper limit on body size. Males show no sexual aggression toward females, and females freely choose their mates. Most strikingly, within groups, male woolly spider monkeys show absolutely no overt competition for mates (Strier, 1990, 1992). Spotted hyenas may be another example. This species, like many Old World monkeys, is characterized by strong female-female coalitions based on kinship (Frank,
46
BARBARA B. SMUTS A N D ROBERT W . SMUTS
1986a,b). However, unlike Old World monkeys, the sexes are similar in size, females consistently dominate males, and males do not try to coerce females into mating. Female ability to choose their mates may explain the mysterious absence in this species of overt aggression among males, although male hyenas do exhibit dominance relationships. The relationship between male dominance rank and male mating success varies widely in animals (Dewsbury. 1982). including primates ( Fedigan, 1983)and attempts to explain this variability have met with limited success. The above analysis suggests that differential ability of dominant males to coerce and sequester females, which has been almost entirely ignored, might help to explain why male dominance correlates with mating access much better in some studies than in others, and why males appear to compete more intensively in some species than in others. In most instances, of course, male ability to coerce females will not be uniform within species, but will vary within and between populations; similarly. some females will be better able to resist coercion than others (see examples given earlier for high-ranking female macaques and vervet monkeys) (Gowaty, 1992). In addition, the benefits to females of choosing “dominant” males (i.e., the winners of male contest competition) will also vary across females and across situations. Also, female mate “choice” and male sexual coercion will often be inextricably intertwined. For example, if dominant males are able to coerce females successfully. females may choose to mate with them to avoid the costs of coercion. On the other hand, (or in addition) females may choose dominant males because those males are best able to protect females (and/or their infants) from coercion by other males (Wrangham, 1979). These examples indicate that the interplay between male contest competition, male sexual coercion, and female choice will be dynamic and context-specific. Only by examining this interplay in all its subtlety and complexity will we be able to understand many critical aspects of animal societies. One such aspect involves female behaviors traditionally interpreted as tactics to facilitate mating with males who provide the “best genes.” Bartholomew (1970) argued that female pinnipeds congregate in tightly packed groups on land so that they can mate with dominant males who are genetically superior. Similarly, Cox and Le Boeuf (1977) argued that female elephant seals vocally protest copulations with subordinate males because they benefit from mating with dominant males who carry superior genes. A focus on male sexual coercion suggests the alternative hypothesis that female aggregation in pinnipeds, and female protest vocalizations in elephant seals, benefit females by increasing the probability that dominant males will protect them from sexual aggression by other males (Trillmich
MALE AGGRESSION AND SEXUAL COERCION
47
and Trillmich, 1984). Indeed, it is possible that many cases in which females appear to prefer dominant males as mates are better explained by the protective benefits those males provide than by their “superior genes” (Wrangham, 1979). Another aspect of animal societies that may be illuminated by consideration of sexual coercion as a selective force is the evolution of sexual dimorphism in body size and weaponry. Consistent with the views expressed here, Richard (1992) points out that in some polygynous mating systems female choice is paramount, and argues that, under such conditions, larger size in males may not be favored by natural selection even though variance in male mating success may be large. In addition, perhaps we need to rethink the assumption that intrasexual competition is the main selective force influencing relative body size in males and females. Attempts to account for variation in the degree of sexual dimorphism in body size in terms of male-male competition (Clutton-Brock et al., 1977; Alexander et al., 1979; Gaulin and Sailer, 1984) and/or female-female competition (Ralls, 1976; Hrdy, 1981; Jolly, 1984; Richard and Nicoll, 1987; Young et al., 1990)have met with limited success (e.g., Shine, 1988). Both sets of explanations ignore the most obvious consequence of sex differences in size and weaponry: differential ability of one sex to dominate the other. The possibility that intersexual conflict may be a selective force influencing male and female body sizes deserves exploration. Under certain conditions, selection may favor larger body size in females because it results in decreased vulnerability to male aggression. This hypothesis may help to explain, for example, lack of sexual dimorphism in spotted hyenas and ring-tailed lemurs, species in which females dominate males and aggressively defend offspring against potentially infanticidal males (Kruuk, 1972; Pereira and Weiss, 1991). Still another important aspect of animal societies that may be illuminated by recognition and study of male sexual coercion as a major selective force is the evolution and expression of long-term male-female associations and male parental behavior. We have argued above that male-male competition is usually ineffective as a reproductive strategy unless complemented by either male sexual coercion of females or female choice. We have also argued that female choice may often be based on female preference for effective male protection (Smuts and Gubernick, 1992) rather than for “good genes.” If these arguments have some validity, they suggest that male tendencies to associate regularly with particular females may have evolved: (a) to protect females and their offspring from aggression by other males, and (b) as an alternative to sexual coercion in the repertoire of male reproductive strategies (see Smuts [ 19921 for application of this argument to human social evolution). This in turn suggests that to understand why
48
BARBARA B. SMUTS AND ROBERT
W. SMUTS
males sometimes pursue either one of these strategies we need to know why they sometimes pursue the other. Whether males try to gain mates by imposing costs on females or by providing them with benefits should depend on the costs to the male of doing one or the other, a male’s ability to provide females with benefits, and the significance of these benefits to females. Consider, for example, two closely related species, brown capuchins and white-fronted capuchins, living in the same environment ( Janson, 1986). Both species live in matrilineal groups with several adults of both sexes, and the diet of both species includes large amounts of fruit. Brown capuchins feed on patchy, defensible resources, and, by tolerating females who mate with him and their young at food patches and helping to keep other males away from these patches, the alpha male offers females a critical benefit. As a result, Janson (1984, 1986) argues that the females consistently and actively choose the alpha male as their mate. Because females prefer to mate with the alpha male, he does not need to employ sexual coercion, and Janson never saw him do so. Critical to this system, perhaps, is the fact that the alpha male can offer important benefits to females as an incidental by-product of his own foraging strategies (which exclude subordinate males from food patches) at little apparent cost to himself. White-fronted capuchins, in contrast, specialize on foods that occur in larger, less defensible patches, and, in contrast to brown capuchins, females and young do not cluster around the alpha male while feeding. Janson (1986) argues that, because the alpha male cannot offer females foraging advantages, they have little to gain from mating with him and instead seek matings with all the males in their group. The alpha male pursues estrous females and tries to force copulations on them, but he cannot prevent the females from mating with subordinate males. This example shows how an apparently slight difference in the ecological context can dramatically alter the dynamic interplay between male-male competition, female choice, and sexual coercion to produce a radically different outcome. It suggests two conclusions. First, simple, causal models that attempt to explain behavior by invoking relatively gross factors, such as the form of the mating system or the habitat type, need to be replaced by more dynamic models that consider complex interactions between specific variables (Bradbury and Davis, 1987). Second, because small changes in particular variables can produce large differences in the way the three components of sexual selection interact, we should expect to see considerable variation in behavioral outcomes both between and within species, and even within the same group at different times. Sometimes, for example, females make friends with nonfathers, who provide protection to females and their offspring in return for future sexual
MALE AGGRESSION AND SEXUAL COERCION
49
access, as reported by Smuts (1985) for savanna baboons near Gilgil. When such friendships endure for several years, however, the friends are likely to be protecting their own offspring (Smuts and Gubernick, 1992). Berkovitch (1991), in contrast, found that in a different troop in the same population, females formed friendships mainly with probable fathers of their infants after mating with them. He suggested that the difference between his findings and those of Smuts (1985) might reflect subtle demographic differences between the two troops. Sometimes females prefer dominant males as both protectors and mates, probably because dominant males are the most effective protectors (e.g., red howlers, Sekulic, 1983b; Pope, 1990; brown capuchins: Janson, 1984, 1986). Savanna baboon females sometimes choose subordinates for both roles (Smuts, 1985). Rhesus and Japanese macaque females sometimes prefer dominant friends but subordinate mates (Huffman, 1987; Manson, 1991). Since dominant males frequently attempt to gain sexual access to their friends but usually fail (Huffman, 1987), it is clear that this arrangement is imposed by females. Why females should prefer, and dominant males should accept, the arrangement is a mystery that is likely to be solved only through insightful investigation and analysis of the complex dynamics of macaque social life.
X. CONCLUSION Although infanticide, physical aggression, and other modes of male sexual coercion of females have sometimes been viewed as important phenomena, they have not been recognized as manifestations of a single selective force comparable in evolutionary significance to competition between males and mate choice by females. We predict that the approach advocated here, by integrating a broad range of phenomena into a single theoretical framework, will generate new hypotheses to explain puzzling behavior and identify important problems that have previously gone unrecognized.
XI. SUMMARY Male aggression against females is a prominent feature of many primate societies. Data on the frequency and contexts of male aggression against females in primates suggest that males often use force, or the threat of force, to increase the chances that females will mate with them, and/or to decrease the chances that they will mate with other males. Such aggression is labeled sexual coercion. Infanticide is considered a form of sexual
50
BARBARA B. SMUTS AND ROBERT W . SMUTS
coercion, because it involves the use of force and often functions to increase male sexual opportunities. Male aggression against females and sexual coercion, including infanticide, also occur in many other mammals. Intriguing similarities to and differences from primates offer important opportunities for comparative studies. Females resist male aggression through a variety of counterstrategies, including alliances with other females and with male protectors, and modification of the timing of reproduction. Male aggression against females and sexual coercion impose substantial costs on females and provide important benefits to males and therefore represent a significant selection pressure influencing life histories and behaviors in both sexes. Variables hypothesized to account for interspecific differences in male aggression against females include sexual dimorphism in body size and weaponry, dispersal patterns, and differences in female-female, female-male, and male-male relationships. Recognition of intersexual coercion as a third form of sexual selection, along with intrasexual competition and intersexual mate choice, is critical to improving understandingof reproductive strategies and social systems in primates and other animals.
Acknowledgments We thank Patricia Adair Gowaty, David Gubernick, Magdalena Hurtado, Sarah Hrdy , Terri Lee, Joseph Manson, John Mitani, Susan Perry, Charles T. Snowdon, Karen Strier, and Richard Wrangham for criticizing the manuscript at various stages in its development and for making valuable suggestions for its improvement. The students enrolled in a graduate seminar at University of Michigan on male aggression against females that was taught by John Mitani and Barbara Smuts provided stimulating discussion that helped to hone the ideas presented here. This work was supported in part by NSF grant BNS-8857969 to Barbara Smuts. Amy Parish and Beverly Aist provided valuable research assistance.
References Abegglen, J. J. (1984). “On Socialization in Hamadryas Baboons.” Associated Univ. Presses, Cranbury, NJ. Agoramoorthy, G., Mohnot, S. M., Sommer, V., and Srivastava, A. (1988). Abortions in free ranging Hanuman langurs (Presbytis entellus)-a male induced strategy? Hum. E v o ~ .3, 297-308. Alcorn, D., and Buelna, E. K. (1989). The Hawaiian monk seal on Laysan Island, 1983. NOAA Tech. Memo. NMFS NOAA-TM-NMFS-SWFC-124, 1-46. Alexander, R. D., and Borgia, G. (1979). On the origin and basis of the male-female phenomenon. In “Sexual Selection and Reproductive Competition in Insects” (M. S. Blum and N. A. Blum, eds.), pp. 417-440. Academic Press, New York. Alexander, R. D., Hoogland, J. L., Howard, R. D., Noonan, K. M.. and Sherman, P. W. (1979). Sexual dimorphisms and breeding systems in pinnipeds, ungulates, primates and
MALE AGGRESSION AND SEXUAL COERCION
51
humans. In "Evolutionary Biology and Human Social Behavior" (N. Chagnon and W. Irons, eds.), pp. 402-435. Duxbury Press, North Scituate, MA. Altmann, J. (1980). "Baboon Mothers and Infants." Harvard Univ. Press, Cambridge, MA. Altmann. J. (1990). Primate males go where the females are. Anim. Behau. 39, 192-198. Andelman, S. (1985). Ecology and reproductive strategies of vervet monkeys (Cercopithecus aethiops) in Amboseli National Park, Kenya. Ph.D. dissertation University of Washington, Seattle. Arnquist. G . (1989).Multiple mating ina water strider: Mutual benefits or intersexual conflict? Anim. Behav. 38, 749-756. Baldwin, J. D. (1968). The social behavior of adult male squirrel monkeys (Saimiri sciureus) in a seminatural environment. Folia Primatol. 9, 281-314. Baldwin, J. D., and Baldwin, J. I. (1972). The ecology and behavior of squirrel monkeys (Saimiri oerstedi) in a natural forest in western Panama. Folia Primatol. 19, 161-184. Bartholomew, G . A. (1970). A model for the evolution of pinniped polygyny. Evolution (Lawrence. Kans.) 24, 546-559. Bateman, A. J . (1948). Intra-sexual selection in Drosophila. Heredity 2, 349-368. Beecher. M. D., and Beecher, 1. M. (1979). Sociobiology of bank swallows: Reproductive strategy of the male. Science 205, 1282-1285. Berger, J. (1983). Induced abortion and social factors in wild horses. Nature (London) 303, 59-6 I. Berger. J . (1986). "Wild Horses of the Great Basin." Univ. of Chicago Press, Chicago. Berkovitch, F. B. (1991). Mate selection, consortship formation, and reproductive tactics in adult female savanna baboons. Primates 32,437-452. Bernstein, I. S. (1968). The lutong of Kuala Selangor. Behauiour 32, 1-16. Bernstein, I. S. (1969). Spontaneous reorganization of a pigtail monkey group. Proc. Int. Cong. Primatol. 2nd, 1968 Vol. I , pp. 48-51. Bernstein, 1. S. (1980). Activity patterns in a stumptail macaque group. Folia Primatol. 33, 20-45. Bernstein, 1. S., and Ehardt, C. L. (1985). Agonistic aiding: Kinship, rank, age. and sex influences. Am. J. Primatol. 8, 37-52. Bernstein, I. S., and Ehardt, C. L. (1986). Modification of aggression through socialization and the special case of adult and adolescent male rhesus monkeys (Macaca mulatta). Am. J. Primatol. 10, 213-227. Boggess, J. (1979). Troop male membership changes and infant killing in langurs (Presbytis entellus). Folia Primatol. 32, 65-107. Boinski, S. (1987). Mating patterns in squirrel monkeys (Saimiri oerstedi). Behau. Ecol. Sociobiol. 21, 13-21. Borgia, G . (1979). Sexual selection and the evolution of mating systems. In "Sexual Selection and Reproductive Competition" (M. S. Blum and N. A. Blum, eds.), pp. 18-80, Academic Press, New York. Borgia, G. (1980). Sexual competition in Scatophaga stercoraria: Size- and density-related changes in male ability to capture females. Behaviour 75, 155-206. Bradbury. J . W., and Davies, N. B. (1987). Relative roles of intra- and intersexual selection. In "Sexual Selection: Testing the Alternatives" (J. W. Bradbury and M. B. Anderson, eds.), pp. 143-163. Wiley. New York. Bramblett, C. C., Bramblett, S. S., Bishop, D. A., and Coehlo, A. M. (1982). Longitudinal stability in adult status hierarchies among vervet monkeys (Cercopithecus aethiops). Am. J. Primatol. 2, 43-51 Brereton. A. (1981). Inter-group consorting by free-ranging female rhesus monkeys (Macaca mulatta). Primates 22, 417-423.
52
BARBARA B. SMUTS A N D ROBERT W. SMUTS
Busse, C. D. (1984). Tail-raising by baboon mothers toward immigrant males. A m . J. Phys. Anthropol. 64, 255-262. Butynski, T. M. (1982). Harem-male replacement and infanticide in the blue monkey (Cercopithecus mitis stuhlmanni) in the Kibale Forest, Uganda, Am. J . Primatol. 3, 1-22. Bygott, J. D. (1972). Cannibalism among wild chimpanzees. Nature (London) 238, 410411. Byrne, R. W., Whiten. A.. and Henzi. S. P. (1987). One-male groups and intergroup interactions of mountain baboons. I n ! . J. Primatol. 8,615-633. Campagna. C . , Le Boeuf, B. J., and Cappozzo, L. (1988). Group raids: A mating strategy of male southern sea lions. Behavior 105, 224-249. Carpenter, C. R. (1942). Sexual behavior of free-ranging rhesus monkeys (Macaca mrrlattu): Specimens. procedures and behavioral characteristics of estrus. J. Comp. Psycho/. 33, 113-142. Chance, M., Emory, G., and Payne, R. (1977). Status referents in long-tailed macaques (Macuca fascicrrlaris): Precursors and effects of a female rebellion. Primates 18, 61 1-632. Chapais, B. (l983a). Matriline membership and male rhesus reaching high ranks in their natal troops. I n "Primate Social Relationships: An Integrated Approach" (R. A. Hinde. ed.), pp. 171-175. Blackwell, Oxford. Chapais, B. (l983b). Structure of the birth season relationship among adult male and female rhesus monkeys. I n "Primate Social Relationships: An Integrated Approach" (R. A. Hinde, ed.), pp. 200-208. Blackwell, Oxford. Chapais, B. (1983~).Adaptive aspects of social relationships among adult rhesus monkeys. I n "Primate Social Relationships: An Integrated Approach" (R. A. Hinde, ed.), pp. 286-289. Blackwell. Oxford. Cheney. D. L. (1983a). Proximate and ultimate factors related to the distribution of male migration. I n "Primate Social Relationships: An Integrated Approach" (R. A. Hinde. ed.), pp. 241-249. Blackwell, Oxford. Cheney, D. L. (1983b). Extra-familial alliances among vervet monkeys. I n "Primate Social Relationships: An Integrated Approach" (R. A. Hinde. ed.), pp. 278-286. Blackwell. Oxford. Cheney. D. L., and Seyfarth, R. M. (1977). Behavior of adult and immature male baboons during inter-group encounters. Nature (London) 269, 404-406. Chism. J., Rowell. T., and Olson, D. (1984). Life history patterns of female patas monkeys. I n "Female Primates: Studies by Women Primatologists" (M. F. Small, ed.). pp. 175-190. Liss, New York. Ciani. A. C. (1984). A case of infanticide in a free-ranging group of rhesus monkeys (Macaco mulatra) in the Jackoo Forest, Simla, India. Primates 25, 372-377. Clarke, M. R. (1983). Infant-killing in a group of howling monkeys in Costa Rica. A m . J. Primatol. 5 , 241-247. Clarke, M. R., and Glander, K. E. (1984). Female reproductive success in a group of freeranging howling monkeys (Alouatta palliuta) in Costa Rica. I n "Female Primates: Studies by Women Primatologists" (M. F. Small, ed.), pp. 111-126. Liss. New York. Clutton-Brock. T. H. (1991). Lords of the lek. Nut. Hist. October, pp. 34-41. Clutton-Brock, T. H.. and Harvey, P. H. (1976). Evolutionary rules and primate societies. I n "Growing Points in Ethology" (P. P. G. Bateson and R. A. Hinde, eds.) pp. 195-237. Cambridge Univ. Press, Cambridge. Clutton-Brock, T. H., and Harvey, P. H. (1978). Mammals, resources, and reproductive strategies. Nature (London) 273, 191-195. Clutton-Brock, T. H..Harvey, P. H.. andRudder, B. (1977). Sexual dimorphism, socionomic sex ratio, and body weight in primates. Nature (London) 269, 797-799.
MALE AGGRESSION AND SEXUAL COERCION
53
Clutton-Brock, T. H.. Guiness. F. E., and Albon, S. D. (1982). “Red Deer: Behavior and Ecology of Two Sexes.” Univ. of Chicago Press, Chicago. Clutton-Brock, T. H., Green, D., Hiraiwa-Hasegawa, M., and Albon, S. D. (1988). Passing the buck: Resource Defence, lek breeding, and mate choice in fallow deer. Behau. Ecol. Sociobiol. 23, 281-296. Collins, D. A., Busse, C. D., and Goodall, J. (1984). Infanticide in two populations of savannah baboons. In “Infanticide: Comparative and Evolutionary Perspectives” (G. Hausfater and S. B. Hrdy, eds.), pp. 193-215. Aldine, Hawthorne. NY. Colrnenares, F., and Gomendio, M. (1988). Changes in female reproductive condition following male take-overs in a colony of hamadryas and hybrid baboons. Folia Primatol. 50, 157-174. Connor, R. C., Smolker, R. A., and Richards, A. F. (1992a). Two levels of alliance formation among male bottlenose dolphins (Tursiops sp.). Proc. Natl. Acad. Sci. U.S.A. 89, 987-990. Connor, R. C., Srnolker, R. A., and Richards, A. F. (1992b). Dolphinalliances andcoalitions. In “Coalitions and Alliances in Humans and other Animals” (A. H. Harcourt and F. B. M. de Waal, eds.), pp. 415-442. Oxford Univ. Press, New York. Cords, M. (1984). Mating patterns and social structure in redtail monkeys (Cercopithecus ascanius). Z. Tierpsychol. 64, 313-339. Cox, C. R., and Le Boeuf. B. J. (1977). Female incitation of male competition: A mechanism in sexual selection. Am. Nat. 111, 317-335. Crockett, C. M., and Rudran, R. (1987). Red howler monkey birth data. If. Interannual, habitat and sex comparisons. Am. J. Primatol. 13, 369-384. Crockett, C. M., and Sekulic, R. (1984). Infanticide in red howler monkeys (Alouatta seniculus). In “Infanticide: Comparative and Evolutionary Perspectives” (G. Hausfater and S. B. Hrdy, eds.), pp. 173-191. Aldine, Hawthorne, NY. Darwin, C. (1871). “The Descent of Man, and Selection in Relation to Sex.” John Murray, London. de Waal, F. B. M. (1982). “Chimpanzee Politics, Power and Sex among Apes.” Harper & Row, New York. de Waal, F. B. M. (1989). “Peacemaking among Primates.” Harvard Univ. Press, Cambridge, MA. Dewsbury, D. A. (1982). Dominance rank, copulatory behavior, and differential reproduction. Q. Rev. Biol. 57, 135-159. Eaton, G. G. (1984). Aggression in adult male primates: A comparison of confined Japanese macaques and free-ranging olive baboons. Int. J . Primatdl. 5 , 145-160. Elwood, R. W., Nesbitt, A. A., and Kennedy, H. F. (1990). Maternal aggression in response to the risk of infanticide by male mice, Mus domesticus. Anim. Behau. 40, 1080-1086. Emlen, S. T., and Oring. L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197, 215-223. Emlen. S. T., and Wrege, P. H. (1986). Forced copulations and inter-specific parasitism: Two costs of social living in the white-fronted bee-eater. Ethology 71, 2-29. Enders, R. K. (1952). Reproduction in the mink (Mustela uison). Proc. Am. Philos. Soc. %, 691-755. Enomoto, T. (1981). Male aggression and the sexual behavior ofJapanese monkeys. Primates 22, 15-23. Ewer, R. F. (1973). “The Carnivores.” Cornell Univ. Press, Ithaca, NY. Fairbanks, L. A., and McGuire, M. T. (1987). Mother-infant relationships in vervet monkeys: Response to new adult males. Int. J. Primatol. 8, 351-366. Fedigan, L. M. (1976). A study of roles in the Arashiyama monkeys (Macaca fuscata). Contrib. Primatol. 9, 1-95.
54
BARBARA B. SMUTS A N D ROBERT W. SMUTS
Fedigan, L. M. (1982). “Primate Paradigms: Sex Roles and Social Bonds.” Eden Press, Montreal. Fedigan, L. M. (1983). Dominance and reproductive success in primates. Yearb. Phys. Anthropol. 26, 91-129. Fedigan, L. M., and Baxter. M. J. (1984). Sex differences and social organization in freeranging spider monkeys (Areles geoffroyi). Primates 25, 279-294. Fisher, R. A. (1930). “The Genetical Theory of Natural Selection.” Oxford Univ. Press (Clarendon), London. Foerg, R. (1982). Reproductive behavior in Varecia uariegata. Folia Primarol. 38, 108-121. Foote, J. 0. (1970). Nose scars in female sea otters. J. Mammal. 51, 621-622. Fossey, D. ( 1984). Infanticide in mountain gorillas (Gorilla gorilla beringei) with comparative notes on chimpanzees. I n “Infanticide: A Comparative and Evolutionary Perspective” (G. Hausfater and S. B. Hrdy, eds.), pp. 217-236. Aldine, Hawthorne, NY. Frank, L. G. (1986a). Social organization of the spotted hyena Crocuta crocuta. I. Demography. Anim. Eehau. 34, 1500-1509. Frank, L. G. (1986b). Social organization of the spotted hyena Crocura crocuta. 11. Dominance and reproduction. Anim. Eehau. 34, 1510-1527. Furuichi, T. (1989). Social interactions and the life history of female Pan paniscus in Wamba. Zaire. Int. J. Primatol. 10, 173-197. Galdikas, B. M. F. (1985). Subadult male orangutan sociality and reproductive behavior at Tanjung Puting. A m . J. Primarol. 8, 87-99. Gaulin, S. J . , and Sailer, L. D. (1984). Sexual dimorphism in weight among the primates: The relative impact of allometric and sexual selection. Inr. J. Primarol 5 , 515-535. Geist, V. (1971). “Mountain Sheep.” Univ. of Chicago Press, Chicago. Goldizen, A. W. (1987). Tamarins and marmosets: Communal care of offspring. I n “Primate Societies” (B. B. Smuts, D. L. Cheney. R. M. Seyfarth, R. W. Wrangham. and T. T. Struhsaker, eds.), pp. 34-43. Univ. of Chicago Press, Chicago. Goldizen, A. W. (1989). Social relationships in a cooperatively polyandrous group of tamarins (Saguinus fuscicollis). Behau. Ecol. Sociobiol. 24, 79-89. Goodall, J. (1986). “The Chimpanzees of Gombe: Patterns of Behavior.” Harvard Univ. Press, Cambridge, MA. Goodall, J., Bandora, A., Bergmann, E., Busse, C., Matarna, H., Mpongo, E., Pierce, A., and Riss, D. (1979). Inter-community interactions in the chimpanzee population of the Gombe National Park. I n “The Great Apes” (D. A. Hamburg and E. R. McCown, eds.). pp. 13-53. Benjamin/Curnmings, Menlo Park, CA. Gouzoules, H. (1980). A description of geneological rank changes in a troop of Japanese monkeys. Primates 21, 262-267. Gowaty, P. A. (1992). Evolutionary biology and feminism. Hum. Nar. 3, 217-249. Gwynne, D. T. (1991). Sexual competition among females: What causes courtship-role reversal? Trends Ecol. Euol. 6 , 1 IS- 12 I . Hall, K. R. L. (1962). The sexual, agonistic, and derived social behaviour patterns of the wild Chacma baboon, Papio ursinus. Proc. Zool. SOC.London 10, 1-28. Hall, K. R. L. (1967). Social interactions of the adult male and adult females of a patas monkey group. I n “Social Communication among Primates” (S. A. Altmann. ed.). pp. 261-280. Univ. of Chicago Press, Chicago. Hall, K. R. L. (1968). Behavior and ecology of the wild patas monkey, Eryrhrocebus paras in Uganda. In “Primates: Studies in Adaptation and Variability” (P. C. Jay, ed.). Holt, Rinehart, & Winston, New York. Hammerstein. P., and Parker, G. A. (1987). Sexual selection: Games between the sexes. In “Sexual Selection: Testing the Alternatives” ( J . W. Bradbury and M. B. Anderson. eds.), pp. 119-142. Wiley, New York.
MALE AGGRESSION A N D SEXUAL COERCION
55
Harcourt, A. H. (1979). Social relationships between adult male and female mountain gorillas in the wild. Anim. Behau. 27, 325-342. Harding. R. S. 0.. and Olson, D. K. (1986). Patterns of mating among male patas monkeys (Erythrocebus patas) in Kenya. Am. J . Primatol. 11, 343-358. Hasegawa, T., and Hiraiwa-Hasegawa, M. ( 1983). Opportunistic and restrictive matings among wild chimpanzees in the Mahale Mountains, Tanzania. J . Efhol. 1, 75-85. Hasegawa, T., and Hiraiwa-Hasegawa, M. (19%). Sperm competition and mating behavior. I n “The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies” (T. Nishida, ed.), pp. 115-132. Univ. of Tokyo Press, Tokyo. Hauser, M. D. (1990). Do chimpanzee copulatory calls incite male-male competition? Anim. Behau. 39,596-597. Hausfater, G. (1975). Dominance and reproduction in baboons. Contrib. Primatol. 7, 1-150. Hausfater. G., and Hrdy, S. B., eds. (1984). “Infanticide: A Comparative and Evolutionary Perspective.” Aldine, Hawthorne, NY. Heltne, P. G., and Marquardt, L. A., eds. (1989). “Understanding Chimpanzees.” Harvard Univ. Press, Cambridge, MA. Henzi, S. P., and Lucas. J. W. (1980). Observations on the intertroop movement of adult vervet monkeys (Cercopithecus aethiops). Folia Primatol. 33, 220-235. Hill, D. A. (1990). Social relationships between adult male and female rhesus macaques. 11. Non-sexual affiliative behaviour. Primates 31, 33-50. Hogg, J. T. (1984). Mating in bighorn sheep: Multiple creative male strategies. Science 225, 526-528. Hrdy, S. B. (1977). “The Langurs of Abu: Female and Male Strategies of Reproduction.” Harvard Univ. Press, Cambridge, MA. Hrdy, S . B. (1979). Infanticide among animals: A review, classification; and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1, 13-40. Hrdy, S. B. (1981). “The Woman that Never Evolved.” Harvard Univ. Press, Cambridge, MA. Huck, U. W. (1984). Infanticide and the evolution of pregnancy block in rodents. I n “Infanticide: Comparative and Evolutionary Perspectives” (G. Hausfater and S. B. Hrdy, eds.), pp. 349-365. Aldine, Hawthorne, NY. Huffman, M. A. (1987). Consort intrusion and female mate choice in Japanese monkeys (Macaca fuscata). Ethology 75, 22 1-234. Idani, G. (1991). Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. Folia Primatol. 57, 83-95. Janson, C. H. (1984). Female choice and mating system of the brown capuchin monkey Cebus apella (Primates: Cebidae). Z . Tierpsychol. 65, 177-200. Janson. C. H. (1986). The mating system as a determinant of social evolution in capuchin monkeys (Cebus). I n “Primate Ecology and Conservation” ( J . G. Else and P. C. Lee, eds.), pp. 169-179. Cambridge Univ. Press, Cambridge. Jay, P. (1963). Mother-infant relations in langurs. I n “Maternal Behavior in Mammals” (H. L. Reingold. ed.), pp. 282-304. Wiley. New York. Jeppsson. B. (1986). Mating by pregnant water voles (Aruicola terrestris): A strategy t o counter infanticide by males? Behau. Ecol. Sociobiol.19, 293-2%. Johnson, B. W., and Johnson, P. A. (1979). “The Hawaiian monk seal on Laysan Island, 1978.” U.S. Dept. of Commerce, Natl. Tech. Inf. Serv., Washington, DC. Johnson, D. F., Modahl, K. B.. and Eaton, G. (1982). Dominance status of adult male Japanese macaques: Relationship to female dominance status, male mating behavior, seasonal changes, and developmental changes. Anim. Behau. 30,383-392. Jolly, A. (1984). The puzzle of female feeding priority. I n “Female Primates: Studies by Women Primatologists” (M. Small, ed.), pp. 197-215. Liss, New York.
56
BARBARA B. SMUTS A N D ROBERT W. SMUTS
Jones, C. B. (1980). The functions of status in the mantled howler monkey, Alouattapalliara Gray: Intraspecific competition for group membership in a folivorous neotropical primate. Primates 21, 389-405. Jungers, W. L., and Susman, R. L. (1984). Body size and skeletal allometry in African apes. I n “The Pygmy Chimpanzee: Evolutionary Morphology and Behavior” (R. L. Susman, ed.), pp. 131-177. Plenum, New York. Kano, T. (1987). Social organization of the pygmy chimpanzee and the common chimpanzee: Similarities and differences. In “Evolution and Coadaptation in Biotic Communities” (S. Kawano, J. Connell, and T. Hidaka, eds.), pp. 53-64. Univ. of Tokyo Press, Tokyo. Kano, T., and Mulavwa, M. (1984). Feeding ecology of the Pygmy chimpanzees (Pan paniscus) of Wamba. In “The Pygmy Chimpanzee: Evolutionary Morphology and Behavior” (R. L. Susman, ed.), pp. 233-274. Plenum, New York. Kaplan, J. R. (1977). Patterns of fight interference in free-ranging rhesus monkeys. Am. J. Phys. Anthropol. 47, 279-288. Kappeler, P. M. (1990). Female dominance in Lemur catta: More than just female feeding priority? Folia Primatol. 55, 92-95. Kappeler, P. M. (1991). Patterns of sexual dimorphism in body weight among prosimian primates. Folia Primatol. 57, 132-146. Kaufman. J. H. (1967). Social relations of adult males in a free-ranging band of rhesus monkeys. I n “Social Communication Among Primates” ( S . Altrnann, ed.), pp. 73-98. Univ. of Chicago Press, Chicago. Kaufman, R. (1991 ). Female dominance in semifree-ranging black-and-white ruffed lemurs, Varecia uariegata variegafa. Folia Primatol. 57, 39-41. Kawanaka, K. (1981). Infanticide and cannibalism in chimpanzees with special reference to the newly observed case in the Mahale Mountains. Afr. Stud. Monogr. 1, 69-99. Keddy, A. C. (1986). Female mate choice in vervet monkeys (Cercopithecus aethiops sabaeus). A m . J . Primatol. 10, 125-134. Keddy Hector, A. C., and Raleigh, M. J. (1992). The effects of temporary removal of the alpha male on the behavior of subordinate male vervet monkeys. Am. J . Primatol. 26, 77-87. Kirkpatrick, J. F., andTurner, J. W. (1991). Changes in herd stallions among feral horse bands and the absence of forced copulation and induced abortion. Behau. Ecol. Sociobiol. 29, 217-219. Koyama, N . (1970). Changes in dominance rank and division of a wild Japanese monkey troop in Arashiyama. Primates 11, 335-390. Kruuk, H. (1972). “The Spotted .Hyena.” Univ. of Chicago Press, Chicago. Kurnmer, H.(1%8). “Social Organization of Hamadryas Baboons.” Univ. of Chicago Press, Chicago. Kurland, J. A. (1977). Kin selection in the Japanese monkey. Contrib. Primatol. U ,1-145. Lancaster, I. B. (1972). Play-mothering: The relations between juvenile females and young infants among free-ranging vervets. I n “Primate Socialization” (F. E. Poirier, ed.), pp. 83-104. Random House, New York. Le Boeuf, B. J., and Mesnick, S. L. (1991). Social behavior of male northern elephant seals. I. Lethal injuries to adult females. Eehaviour 116, 143-162. Lindburg, D. G. (1971). The rhesus monkey in north India: An ecological and behavioral study. I n “Primate Behavior: Developments in Field and Laboratory Research” (L. A. Rosenblum, ed.), Vol. 2, pp. 2-106. Academic Press, New York. Lindburg, D. G. (1983). Mating behavior and estrus in the Indian rhesus monkey. In “Perspectives on Primate Biology” (P. K.Seth, ed.), pp. 45-61. Today and Tomorrow, New Delhi .
MALE AGGRESSION AND SEXUAL COERCION
57
Loy, J. (1985). The copulatory behavior of adult male patas monkeys, Erythrocebus patas. J . Reprod. Fertil. 45, 193-195. Loy, J. (1989). Sex and aggression among patas monkeys (Erythrocebus patas). Primate Rep. 23, 35-39.
Macdonald, D. W., Apps, P. J., Carr, G. M., and Kerby, G. (1987). Social dynamics, nursing coalitions and infanticide among farm cats, Felis catus. Adv. Ethol. 28, 5-66. MacKinnon, J. R. (1971). The orang-utan in Sabah today. Oryx 11, 141-191. Mallory. F. F., and Brooks, R. J. (1978). Infanticide and other reproductive strategies in the collared lemming, Dicrostonyx groenlandicus. Nature (London) 273, 144-146. Manson, J. (1991). Female mate choice in Cay0 Santiago rhesus macaques. Ph.D. dissertation, University of Michigan, Ann Arbor. Marlow, B. J. (1975). The comparative behavior of the Australasian sea lions, Neophoca cinerea and Phocarctos hooker; (Pinnipedia: Otariidae). Mammaliu 39, 159-230. Marsh, C. W. (1979). Female transference and mate choice among Tana River red colobus. Nature (London) 281, 568-569.
McFarland Symington, M. (1987). Ecological and social correlates of party size in the black spider monkey Ateles paniscus chamek. Ph.D. dissertation, Princeton University, Princeton, NJ. McKinney, F., Derrickson, S. R., and Mineau, P. (1983). Forced copulation in waterfowl. Behaviour 86, 250-294. McLean, I. G. (1982). The association of female kin in the arctic ground squirrel Spermophilus parryii. Behav. Ecol. Sociobiol. 10, 91-99. McLean, 1. G. (1983). Paternal behavior and killing of young in arctic ground squirrels. Anim. Behav. 31,32-44.
McPeek, M. A. (1992). Mechanisms of sexual selection operating ,on body size in the mosquitofish (Gambusia holbrooki). Behav. Ecol. 3, 1-12. Mesnick, S. L., and Le Boeuf, €3. J. (1991). Sexual behavior of male northern elephant seals. 11. Female response to potentially injurious encounters. Behaviour 117, 262-280. Mitani, J. C. (1985). Mating behavior of male orangutans in the Kutai Reserve. Anim. Behav. 33, 392-402. Mohnot, S. M. (1984). Langur interactions around Jodhpur (Presbytis entellus). I n "Current Primate Researches" (M. L. Roonwal, S. M. Mohnot, and N. S. Rathore, eds.), pp. 399-41 I. Univ. of Jodhpur, Jodhpur. Mori, A. (1979). Unit formation and the emergence of a new leader. Contrib. Primatol. 16, 155-181.
Mori, U., and Dunbar, R. 1. M. (1985). Changes in the reproductive condition of female gelada baboons following the takeover of one-male units. Z. Tierpsychol. 67, 215-224. Moss, C. (1983). Oestrous behavior and female choice, in the African elephant. Behaoiour 86, 167-196. Nadler, R. D. (1982). Reproductive behavior and endocrinology of orangutans. I n "The Orangutan: Its Biology and Conservation" (L.E. M. de Boer, ed.), pp. 231-248. Dr. W. Junk, The Hague. Nadler, R. D. (1988). Sexual aggression in the great apes. I n "Human Sexual Aggression: Current Perspectives" (R. A. Prentky and V. L. Quinsey, eds.), pp. 154-162. N.Y. Acad. Sci., New York. Nadler, R. D. (1989a). Sexual aggression in common chimpanzee, gorilla and orangutan. Primate Rep. 23, 5-1 1. Nadler, R. D. (1989b). Sexual initiation in wild mountain gorillas. Int. J. Prirnatol. 10,81-92. Nadler, R. D., and Miller, L. C. (1982). Influence of male aggression on mating of gorillas in the laboratory. Folia Primatol. 38, 233-239.
58
BARBARA B. SMUTS A N D ROBERT W. SMUTS
Nishida, T. (1979). The social structure of chimpanzees of the Mahale Mountains. In “The Great Apes” (D. A. Hamburg and E. R. McCown, eds.). pp. 73-122. BenjaminKummings, Menlo Park, CA. Nishida, T. (1990). A quarter century of research in the Mahale Mountains: An overview. In “The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies” (T. Nishida, ed.), pp. 3-35. Univ. of Tokyo Press, Tokyo. Nishida, T., and Hiraiwa-Hasegawa, M. (1985). Responses to a stranger mother-son pair in the wild chimpanzee: A case report. Primates 26, 1-13. Nishida, T., and Hiraiwa-Hasegawa, M. (1987). Chimpanzees and bonobos: Cooperative relationships among males. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R.W. Wrangham, and T. T. Struhsaker, eds.), pp. 165-177. Univ. of Chicago Press, Chicago. Nishida, T., and Kawanaka, K. (1985). Within-group cannibalism by adult male chimpanzees. Primates 26, 274-284. Nishida, T., Hiraiwa-Hasegawa. M., Hasegawa, T., and Takahata, Y. (1985). Group extinction and female transfer in wild chimpanzees in the Mahale Mountains. Z. Tierpsychol. 67, 284-301. Nishida, T., Takasaki, H.. and Takahata, Y. (1990).Demography and reproductive profiles. In “The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies” (T. Nishida, ed.), pp. 63-97. Univ. of Tokyo Press, Tokyo. Noe, R. (1990). A veto game played by baboons: A challenge to the use of the Prisoner’s Dilemma as a paradigm for reciprocity and cooperation. Anim. Behau. 39, 78-90. O’Brien, T. (1991). Female-male social interactions in wedge-capped capuchin monkeys: Benefits and costs of group living. Anim. Behau. 41, 555-567. Oi, T. (1990). Patterns of dominance and affiliation in wild pig-tailed macaques (Macaca nemestrina nemestrina) in West Sumatra. lnt. J. Primatol. 11, 339-356. Olson, D. (1985). The importance of female choice in the mating system of wild patas monkeys. Am. J. Phys. Anthropol. 66, 21 1 (abstr.). Packer, C. (1977). Reciprocal altruism in olive baboons. Nature (London) 265,441-443. Packer, C. (1979). Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim. Behau. 27, 1-36. Packer, C., and Pusey. A. E. (1979). Female aggression and male membership in troops of Japanese macaques and olive baboons. Folia Primatol. 31, 212-218. Packer, C . , and Pusey, A. E. (1983a). Adaptations offemale lions to infanticide by incoming males. Am. Nut. 121, 716-728. Packer, C., and Pusey, A. E. (1983b). Male takeovers and female reproductive parameters: A simulation of oestrous synchrony in lions (Panthera leo). Anim. Behau. 31,334-340. Packer, C . , Scheel, D., and Pusey, A. E. (1990). Why lions formgroups: Food is not enough. Am. Nat. 136, 9-19. Parker, G. A. (1979). Sexual selection and sexual conflict. In “Sexual Selection and Reproductive Competition” (M. S . Blum and N . A. Blum, eds.), pp. 123-166. Academic Press, New York. Pereira, M. E. (1983). Abortion following the immigration of an adult male baboon (Papio cynocephalus). A m . J . Primatol. 4, 93-98. Pereira, M. E., and Weiss, M. L. (1991). Female mate choice, male migration, and the threat of infanticide in ring-tailed lemurs. Behau. Ecol. Sociobiol. 28, 141-152. Pereira, M. E. Kaufman. R., Kappeler, P., and Overdorff, D. (1990). Female dominance does not characterize all of the Lemuridae. Folia Primarol. 55, 96-103. Poole, J. H. (1989). Mate guarding, reproductive success and female choice in African elephants. Anim. Behau. 37, 842-849. Pope, T. R. (1990). The reproductive consequences of male cooperation in the red howler
MALE AGGRESSION AND SEXUAL COERCION
59
monkey: Paternity exclusion in multi-male and single-male troops usinggenetic markers. Behav. Ecol. Sociobiol. 27, 439-446. Pusey. A. E. (1979). Intercommunity transfer of chimpanzees in Gombe National Park. I n “The Great Apes” (D.A. Hamburg and E. R. McCown, eds.), pp. 465-480. Benjamin/ Curnmings, Menlo Park, CA. Rajpurohit, L. S., and Sommer, V. (1991). Sex differences in mortality among langurs (Presbyris entellus) of Jodhpur, Rajasthan. Folia Primatol. 56, 17-27. Raleigh, M. J., and McGuire. M. T. (1989). Female influences on male dominance acquisition in captive vervet monkeys, Ceropithecus aethiops sahaeus. Anim. Behav. 38,59-67. Ralls. K. (1976). Mammals in which females are larger than males. Q. Rev. Biol. 51,245-276. Ransom, T. W. (1981). “Beach Troop of the Gombe.” Bucknell Univ. Press. Lewisburg, PA. Richard, A. F. (1992). Aggressive competition between males, female-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi. J . Hum. Evol. 22, 395-406. Richard, A. F.. and Nicoll, M. E. (1987). Female social dominance and basal metabolism in a Malagasy primate, Propithecus uerreauxi. Am. J . Primatol. 12, 309-3 14. Ridley, M. (1986). The number of males in a primate troop. Anim. Behau. 34, 1848-1858. Rijksen, H. (1978). “A Field Study on Sumatran Orangutans (Pongopygmaeiis abeli Lesson 1827):’ H. Veenman and Zonen, Wageningen. Robbins Leighton, D. (1987). Gibbons: Territoriality and monogamy. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds.). pp. 135-145. Univ. of Chicago Press, Chicago. Robinson, J. G. (1981). Spatial structure in foraging groups of wedge-capped capuchin monkeys Cebus nigrivittatus. Anim. Behav. 29, 1036-1056. Robinson, J. G. (1988). Group size in wedge-capped capuchin monkeys Cebus olivaceus and the reproductive success of males and females. Behau. Ecol. Sociohiol. 23, 187197. Robinson, J. G., Wright. P. C.. and Kinzey, W. G. (1987). Monogamous Cebids and their relatives: Intergroup calls and spacing. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth. R. W. Wrangham, and T. T. Struhsaker, eds.), pp. 44-53. Univ. of Chicago Press, Chicago. Rodman, P. S. (1973). Population composition and adaptive organisation among orangutans of the Kutai Reserve. In “Comparative Ecology and Behaviour of Primates” (R. Michael and J. Crook, eds.), pp. 171-209. Academic Press, New York. podman, P. S. (1984). Foraging and social systems of orangutans and chimpanzees. In “Adaptations for Foraging in Nonhuman Primates: Contributions to an Organismal Biology of Prosimians, Monkeys, and Apes” (P. S. Rodman and J. G. H. Cant, eds.), pp. 134-160. Columbia Univ. Press, New York. Rodseth, L., Wrangham, R. W., Harrigan, A. M., and Smuts, B B. (1991). The human community as a primate society. Curr. Anthropol. 32, 221-254. Rosser. A. M. (1992). Resource distribution, density, and determinants of mate access in puku. Behav. Ecol. 3, 13-24. Rowell, T. E. (1974). Contrasting adult male roles in different species of nonhuman primates. Arch. Sex. Behav. 3, 143-149. Ruehlmann, T. E., Bernstein, I. S., Gordon, T. P., and Balcaen, P. (1988). Wounding patterns in three species of captive macaques. Am. J . Primatol. 14, 125-134. Rutberg, A. T. (1990). Inter-group transfer in Assateague pony mares. Anim. Behav. 40, 945-952. Sekulic, R. (1983a). Male relationships and infant deaths in red howler monkeys (Alouarra seniculus). Z . Tierpsychol. 61, 185-202.
60
BARBARA B. S M U T S A N D ROBERT W. SMUTS
Sekulic, R. (1983b). Spatial relationships between recent mothers and other troop members in red howler monkeys (Alouatta seniculus). Primates 24, 475-485. Sekulic, R. (1983~).The effect of female call on male howling in red howler monkeys (Alouatta seniculus). Int. J. Primatol. 4, 291-305. Seyfarth, R. M. (1978). Social relationships among adult male and female baboons. 11. Behavior throughout the female reproductive cycle. Behauiour 64, 227-247. Shine, R. (1988).The evolution of large body size in females: A critique of Darwin’s fecundity advantage model. Am. Nut. 131, 124-131. Sicotte. P. ( 1989). Female migration and differential social development in infant mountain gorillas. Anthroquest 40, 3-4. Sigg, H., Stolba, A., Abegglen, J. J., and Dasser, V. (1982). Life history of hamadryas baboons: Physical development, infant mortality, reproductive parameters and family relationships. Primates 23, 473-487. Siniff, D. B. I.. Stirling, J. L. B.. and Reichle, R. A. (1979). Social and reproductive behavior of crabeater seals (Lobodon carcinophagus) during the austral spring. Can. J. Zool. 57, 2243-2255. Small, M. F. (1989). Female choice in nonhuman primates. Yearb. Phys. Anthropol. 32, 103- 127. Smuts, B. B. (1983a). Dynamics of special relationships between adult male and female olive baboons. In “Primate Social Relationships: An Integrated Approach” (R. A. Hinde, ed.), pp. 112-1 16. Blackwell, Oxford. Smuts, B. B. (1983b). Special relationships between adult male and female olive baboons: Selective advantages. In “Primate Social Relationships: An Integrated Approach” (R. A. Hinde, ed.), pp. 262-266. Blackwell, Oxford. Smuts, B. B. (1985). “Sex and Friendship in Baboons.” Aldine, Hawthorne, NY. Smuts, B. B. (1987a). Sexual competition and mate choice. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth. R. W. Wrangham, and T. T. Struhsaker, eds.), pp. 385-399. Univ. of Chicago Press, Chicago. Smuts, B. B. (1987b). Gender, aggression, and influence. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds.), pp. 400-412. Univ. of Chicago Press, Chicago. Smuts, B. B. (1992). Male aggression against women: An evolutionary perspective. Hum. Nut. 3, 1-44. Smuts, B. B. (1993). The origins of gender inequality: An evolutionary perspective. I n “Foundations of Gender Inequality” (A. Zagarell, ed.). New Issues Press, Kalamazoo (in press). Smuts, B. B., and Gubernick, D. J. (1992). Male-infant relationships in nonhuman primates: Paternal investment or mating effort?ln “Father-Child Relations: Cultural and Biosocial Contexts” (B. S. Hewlett, ed.), pp. 1-30. Aldinelde Gruyter, Hawthorne. NY. Smuts, R. W. (1993). Fat, sex, class, adaptiveflexibility and culturalchange. Ethol. Sociobiol. (in press). Sommer, V. (1987). Infanticide among free-ranging langurs (Presbytis entellus) at Jodhpur (RajasthadIndia): Recent observations and a reconsideration of hypotheses. Primates 28, 163-197. Sommer, V. (1988). Male competition and coalitions in langurs (Presbytis entellus) at Jodhpur, Rajasthan, India. Hum. Evol. 3, 261-278. Sommer, V. (1992). Infanticide among the langurs of Jodhpur: Testing the sexual selection hypothesis with a long-term record. In “Infanticide and Parental Care” (S. Parmigiani and F. vorn Saal, eds.). Harwood Academic, London (in press). Sommer, V., and Rajpurohit, L. S . (1989). Male reproductive success in harem troops of
MALE AGGRESSION AND SEXUAL COERCION
61
Hanuman langurs (Presbytis entellus) near Jodhpur (RajasthadIndia). Behav. Ecol. Sociobiol. 16, 245-248. Stanford, C. B. (1991). Social dynamics of intergroup encounters in the capped langur (Presbytis pileafa).Am. J . Primatol. 25, 35-47. Starin, E. D. (1981). Monkey moves. Nat. Hisr. 90, 36-43. Stewart, K . J., and Harcourt, A. H. (1987). Gorillas: Variation in female relationships. I n “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds.), pp. 155-164. Univ. of Chicago Press, Chicago. Strier, K. B. (1990). New World primates, new frontiers: Insights from the Woolly Spider Monkey or Muriqui (Brachyteles arachnoides). Inr. J . Primatol. 11, 7-19. Strier, K. B. (1992). Causes and consequences of nonaggression among the Woolly Spider Monkey or Muriqui (Brachyteles arachnoides). In “Aggression and Peacefulness in Humans and other Primates” ( J . Silverberg and J. P. Gray, eds.), pp. 100-1 16. Oxford Univ. Press, New York. Struhsaker. T. T. (1977). Infanticide and social organization in the redtail monkey (Cercopithecus ascanius schmidri) in the Kibale Forest, Uganda. Z. Tierpsychol. 45,75-84. Struhsaker, T. T., and Leland, L. (1985). Infanticide in a patrilineal society of red colobus monkeys. Z. Tierpsychol. 69, 89-132. Struhsaker, T. T., and Leland, L. (1987). Colobines: Infanticide by adult males. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds.), pp. 83-97. Univ. of Chicago Press, Chicago. Strum, S. C. (1982). Agonistic dominance in male baboons: An alternative view. Int. J . Primatol. 3, 175-202. Sugiyama, Y. (1967). Social organization of hanuman langurs (Presbytis entellus) in their natural conditions. Primates 6, 213-247. Takahata, Y.(1982). Social relations between adult males and females of Japanese monkeys in the Arashiyama B troop. Primates 23, 1-23. Teas, J. (1984). Rhesus monkey aggression and grooming social dynamics. In “Female Primates: Studies by Women Primatologists” (M. F. Small, ed.), pp. 237-247. Liss, New York. Thornhill, R. (1979). Male and female sexual selection and the evolution of mating strategies in insects. In “Sexual Selection and Reproductive Competition” (M. S. Blum and N. A. Blum, eds.), pp. 81-121. Academic Press, New York. Thornhill, R. (1980). Rape in Panorpa scorpion flies and a general rape hypothesis. Anim. Behau. u),52-59. Thornhill, R., and Alcock, J. (1983). “The Evolution of Insect Mating Systems.” Harvard Univ. Press, Cambridge, MA. Tokuda, K. (1961). A study on the sexual behavior in the Japanese monkey troop. Primates 3, 1-40. Tracy, K. K., and Crawford, C. (1992). Wife abuse: Does it have an evolutionary origin? In “Sanctions and Sanctuary: Cultural Perspectives on the Beating of Wives” (D. Counts, D., J. K. Brown, and J. Campbell, eds.), pp. 19-32. Westview Press, Boulder, Co. Trillmich, F., and Trillmich, G. K. (1984). The mating system of pinnipeds and marine iguanas: Convergent evolution of polygyny. Biol. J . Linn. SOC.21, 209-216. Trivers, R. L. (1972). Parental investment and sexual selection. In “Sexual Selection and the Descent of Man, 1871-1971” (B. Campbell, ed.), pp. 136-179. Aldine, Chicago. Trivers, R. L. (1985). “Social Evolution.” Benjamin/Cummings, Menlo Park, CA. Tsingalia, H. M., and Rowell, T. E. (1984). The behaviour of adult male blue monkeys. Z . Tierpsychol. 64, 253-268.
62
BARBARA B. SMUTS AND ROBERT W. SMUTS
Tutin, C. E. G. (1975). Sexual behaviour and mating patterns in a community of wild chimpanzees (Pun troglodytes schweinftrthii). Ph.D. dissertation, University of Edinburgh. Tutin, C. E. G. (1979). Mating patterns and reproductive strategies in a community of wild chimpanzees (Pun troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 6, 39-48. Valderrama, X., Srikosamatara, S., and Robinson, J. G . (1990). Infanticide in wedge-capped capuchin monkeys, Cebus olivaceus. FoIiu Primatol. 54, 171-176. van Noordwijk, M. A,, and van Schaik, C. P. (1985). Male migration and rank acquisition in wild long-tailed macaques. Anim. Behuv. 33, 849-886. van Noordwijk, M. A., and van Schaik, C. P. (1988). Male careers in Sumatran long-tailed macaques (Macuca fuscicularis). Behaviour 107, 24-43. van Schaik. C. P. (1989). The ecology of social relationships amongst female primates. I n “Comparative socioecology: The Behavioural Ecology of Humans and other Mammals” (V. Standen and R. Foley, eds.). pp. 195-218. Blackwell, Oxford. van Schaik, C. P., and van Hooff, J. A. R. A. M. (1983). On the ultimate causes of primate social systems. Behuviour 85, 91-1 17. van Schaik, C. P., and van Noordwijk, M. A. (1989).The special role of male Cebrts monkeys in predation avoidance and its effect on group composition. Behau. Ecol. Sociobiol.24, 265-276. Wagner, R. H. (1991). The use of extra-pair copulations for mate appraisal by razorbills, A k a tordu. Behuv. Ecol. 2, 198-203. Walters, J. R., and Seyfarth, R. M. (1987). Conflict and cooperation. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker. eds.), pp. 306-317. Univ. of Chicago Press. Chicago. Watanabe, K. (1979). Alliance formation in a free-ranging troop of Japanese macaques. Primates 20,459-474. Watts, D. P. (1983). Foraging strategies and socioecology of mountain gorillas (Pun gorillu beringei). Ph.D. dissertation, University of Chicago, Chicago. Watts, D. P. (1989). Infanticide in mountain gorillas: New cases and a reconsideration of the evidence. Ethology 81, 1-18. Watts, D. P. (1991). Mountain gorilla reproduction and sexual behavior. Am. J. Primotol. 24,211-225. Watts, D. P. (1992). Social relationships of immigrant and resident female mountain gorillas. 1. Male-female relationships. Am. J . Primatol., in press. West-Eberhard, M. J., Bradbury, J. W., Davis, N. B., Gouyon P. H., Hammerstein, P., Konig, B., Parker, G. A., Queller, D. C., Sachser, N., Slagsvold, T., Trillmich, F., and Vogel, C. (1987). Conflicts between and within the sexes in sexual selection: Group Report. I n “Sexual Selection: Testing the Alternatives” ( J . W. Bradbury and M. B.. Anderson, eds.), pp. 180-195. Wiley, New York. Westneat, D. F., Sherman, P. W., and Morton, M. L. (1990). The ecology and evolution of extra-pair copulations in birds. Curr. Ornithol. 7 , 331-369. White, F. J. (1992). Pygmy chimpanzee social organization: Variation with party size and between study sites. Am. J. Primatol. 26, 203-223. Winkler, P. (1988). Troop history, female reproductive strategies and timing of male change in Hanuman langurs, Presbyris entellus. Hum. Evol. 3, 227-237. Wolf. K., and Schulman, S. T. (1984). Male responses to “stranger” females as a function of female reproductive value among chimpanzees. A m . Nat. 123, 163-174. Wolfe, L. D. (1981). Display behavior of three troops of Japanese monkeys. Primates 22, 24-32. Wolff, J. 0. (1985). Maternal aggression as a deterrant to infanticide in Peromyscus Ieucopus and P . Maniculutus. Anim. Behuv. 33, 117-123.
MALE AGGRESSION AND SEXUAL COERCION
63
Wolff. J. 0.. and Cicirello. D. M. (1989). Field evidence for sexual selection and resource competition infanticide in white-footed mice. Anim. Eehau. 38,637-642. Wrangham. R. W. (1975). The behavioural ecology of chimpanzees in Gombe National Park, Tanzania. Ph.D. dissertation, Cambridge University. Wrangham. R. W. (1979). On the evolution of ape social systems. Soc. Sci. Inf. 18,334-368. Wrangham, R. W. (l980a). An ecological model of female-bonded primate groups. Eehauiour 75, 262-300. Wrangham, R. W. (1980b). Female choice of lest costly males: A possible factor in the evolution of leks. Z. Tierpsvchol. 54, 357-367. Wrangham, R. W. (1982). Kinship, mutualism. and social evolution. I n “Current Problems in Sociobiology” (King’s College Sociobiology Group, eds.), pp. 269-290. Cambridge Univ. Press, Cambridge. Wrangham, R. W. (1986). Ecology and social relationships in two species of chimpanzees. I n “Ecological Aspects of Social Evolution in Birds and Mammals” (D.I. Rubenstein and R. W. Wrangham, eds.). pp. 354-378. Princeton Univ. Press, Princeton. NJ. Wrangham, R. W. (1987a). Evolution of social structure. In “Primate Societies” (B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham. and T. T. Struhsaker, eds.), pp. 282-296. Univ. of Chicago Press, Chicago. Wrangham, R. W. (l987b). The significance of African apes for reconstructing human social evolution. In “The Evolution of Human Behavior: Primate Models” (W. P. Kinzey, ed.), pp. 51-71. State Univ. of New York Press, Albany. Young, A., Richard, A. F., and Aiello, L. (1990). Female social dominance, basal metabolic rate and prenatal maternal investment rate in primates. Am. Nut. 135, 473-488. Zumpe, D.. and Michael, R. P. (1990). Effects of the presence of a second male on pair-tests of captive cynornolgus monkeys (Macaca fascicularis): Role of dominance. Am. J . Primarol. 22, 145-158.
This Page Intentionally Left Blank
ADVANCES IN THE STUDY OF BEHAVIOR. VOL. 22
Parasites and the Evolution of Host Social Behavior ANDERSPAPEM ~ L L E REIJA R, DUFVA,A N D KLASALLANDER DEPARTMENT OF ZOOLOGY UPPSALA UNIVERSITY S-75 1 22 UPPSALA. SWEDEN
I. INTRODUCTION The main theme of this review is that parasites often have extensive negative effects on the fitness of their hosts, and that these negative effects are often directly related to host social behavior. Parasites constitute a large fraction of all organisms, and individuals of most organisms are infected with parasites at least some time during their life (Price, 1980). Parasites are therefore a potentially important selective force. An important factor enhancing transmission of parasites is the close proximity of hosts or groups of hosts, and parasites are therefore a major cost of sociality. We present a review of the evidence for a relationship between parasitism and sociality. However, social living is widespread among a wide array of organisms despite the costs of parasitism. Social living may be possible partly because hosts are able to reduce the effects of sociality on the risks of parasitism. This can be accomplished by means of a large number of behavioral adaptations which reduce the probability of becoming infected or which reduce the levels of parasite infestations once infected. These adaptations are described in the second part of this review. If parasites are a potentially more important selective force in social than in solitary organisms, this may result in different rates of coevolution between parasites and their hosts, all other things being equal. Discussion of this theme constitutes the final part of this review.
BACKGROUND A. PARASITOLOGICAL We present in this section a number of basic parasitological concepts which are essential for understanding parasite-host relationships. Parasites draw their food resources from the live bodies of other species, on or in which individual parasites spend most of their lives, causing some or 65 Copyright 0 1993 by Academic Press. Inc. All rights of reproduction in any form reserved.
66
ANDERS PAPE MBLLER ET AL.
even a great deal of damage (Price, 1980). Parasites are often subdivided into microparasites (viruses, bacteria, fungi, protozoa) and macroparasites (helminths, arthropods). Microparasites are characterized by small size, short generation times, and high rates of direct reproduction within their hosts. The duration of an infection is relatively short and they induce either lifelong immunity, chronic infection, or death of the host. Macroparasites have longer generation times than microparasites, and complete some part of their life cycle outside the host. Host immune responses generally depend on the number of macroparasites present, and are of relatively short duration, which makes the host susceptible to continuous reinfection. The conventional wisdom amongst parasitologists is that parasites usually do not reduce the fitness of their hosts severely. However, much experimental evidence suggests that parasites are often important selective factors which reduce the fitness of infected plants and animals (e.g., Elton, 1927; Fisher and Holton, 1957; Mattingly, 1969; Boycott, 1971; Burnet and White, 1972; Day, 1974; Page, 1976; Anderson and May, 1982; Burdon, 1987; Keymer and Read, 1989; Alexander, 1992; Moller et al., 1990). Damage can be measured in terms of reduced fitness and a reduced intrinsic growth rate of the host population. Many examples of severe negative effects of parasites on host fitness derive from studies in which the level of parasite infestation has been experimentally changed. For example, fumigation of the nests of cliff swallows (Hirundo pyrrhonora) with a weak pesticide reduced the level of infestation with ectoparasites, and this subsequently resulted in an improvement in the quality and the quantity of offspring produced by the avian hosts (Loye and Carroll, 1991). Another kind of perturbation experiment was performed on starlings (Srurnus uulgaris). If the green plants used by starlings as nest material were removed experimentally, the number of mites infecting nests increased dramatically, with a consequent decrease in the condition of the starling nestlings (Clark, 1991). This example clearly demonstrates that negative effects of parasites can be masked by antiparasite behavior of the host. Parasites have a broad range of effects on the fitness of their hosts, ranging from lowered reproductive and survival rates to sterilization and death. A few ectoparasites may not be very harmful, while a microparasitic disease may kill a host, or make it susceptible to predation, even if only present in small numbers. Large numbers of intestinal parasites can cause weight loss, anemia, reduced growth, and reproductive inefficiency (Hart, 1990). Some parasites may only severely affect a host during periods of stress related to malnutrition, cooccurrence of parasite species, social competition, and reproduction (e.g., Freeland, 1981a; Rau, 1983, 1984).
PARASITES AND HOST SOCIAL BEHAVIOR
67
Thus, traits reducing levels of infection should be favored by selection. Such adaptations include avoidance of infection by parasites and elimination of parasites once a host is infected. TRANSMISSION A N D HOSTDENSITY B. PARASITE Parasite transmission is the sometimes hazardous process of transfer of a parasite from one individual host to another. Adaptations to reduce this hazard include (a) transmission in space by motile free-living stages, by nonmotile free-living stages, or by vectors, and (b) transmission in time by resting stages (Kennedy, 1976). For many parasites the probability of encountering a new host may be very low if the host species is scarce or sparsely distributed, and infection may in practice only be possible when the host aggregates for a short period of time, as for breeding. The life cycle of such parasites is therefore often synchronized with that of their hosts so that infective stages are produced or released only when the hosts aggregate, or when their progeny appear (Kennedy, 1975). Hosts may reduce their immune responses during reproduction because of incompatibility between parent and offspring (Behnke and Wakelin, 1973; Grossman, 1985), and hosts may therefore become more susceptible to parasite infection during that stage of their annual cycle. One of the most important factors promoting transmission of ectoparasites is close proximity between infected and uninfected individuals, and the same principle applies to some extent to endoparasites (Janzen, 1968, 1973; Alexander, 1974; Dritschilo et af., 1975; Kuris et af., 1980). Transmission by direct contact depends on bodily contact between hosts, for example, between parents and their young, or between adults during copulation ( Jablonska, 1986), or during roosting in gregarious species (Marshall, 198 1). Venereal diseases require close bodily contact of infected and uninfected individuals. The risk of venereal disease should be directly related to the number of sexual encounters and the level of infection in the population (Anderson and May, 1991), and sexual fidelity of individuals could thus be the result of selection for the avoidance of new diseases. “Venereal diseases” in plants are transmitted by pollinators or other flower-visiting organisms, and again close proximity and density of hosts increase the probability of transmission (e.g., Baker, 1947; Jennersten et al., 1983; Jennersten, 1985). Many parasites are transmitted from one host to another by ingestion: for example, the larvae and eggs of intestinal parasites. The host may swallow the parasites because of fecal contamination of the food, or
68
ANDERS PAPE MBLLER ET AL.
through carnivory (Crompton, 1976). Parasites may also be swallowed during preening or grooming (Baker, 1975). The behavior of parasites enhances their probability of reaching the place most favorable for transmission. For example, larvae of the parasitic nematode Trichostrongylus tenuis migrate to the outermost tips of heather (Calluna vulgaris) plants, which are the major food of their red grouse (Lagopus lagopus scoticus) host (McGladdery, 1984). The density of free-living, infective stages of parasites is thus likely to be directly related to the density of infected hosts. The use of an intermediate host which is both abundant and vulnerable to predation will favor transmission in some cases. Certain parasites are able to change the appearance and/or the behavior of an intermediate host to facilitate their own transmission to a definitive host (e.g., Brown and Thompson, 1986). Parasitized intermediate hosts may become more vulnerable prey through reduced stamina (Lester, 1971; Giles, 1983), disorientation (Carney, 1969), increased conspicuousness (Kennedy, 1975; Hindsbo, 1989), and abnormal responses to environmental stimuli (Hindsbo, 1972; Bethel and Holmes, 1973, 1977; Moore, 1983, 1984a,b; Dobson, 1988). Vectors are intermediate hosts capable of transmitting parasites to a new, final host (Harwood and James, 1979). Arachnids and insects, including mites, ticks, bugs, lice, fleas, and flies, are the major vectors transmitting parasites and disease (e.g., Arthur, 1962; Muirhead-Thomson, 1968; Mattingly, 1969; Boycott, 1971; Burnet and White, 1972;Noble and Noble, 1976; Marshall, 1981; Cox, 1982). Blood parasites of the genera Plasmodium, Haemoproteus, and Leucocytozoon, together with filarial worms, are examples of parasites transmitted by vectors. Survival of the vectortransmitted parasites depends on contact between infected hosts, vectors, and susceptible hosts. Transmission of parasites by vectors therefore increases in efficiency in relation to the density of hosts (i.e., the close proximity of infected and uninfected individuals [e.g., Alexander, 1974; Harper, 1977; Hoogland, 19791). In conclusion, the efficiency of parasite transmission from one host to another appears to increase with host density for parasites that rely on contact transmission, ingestion by hosts, or vector transmission. C. PARASITEABUNDANCE AND HOSTSOCIALITY If the close proximity of host individuals or groups increases the probability of parasite transmission, we should expect increased levels of parasite infestation with increasing degrees of sociality. The fraction of parasite-infected host individuals (parasite prevalence) and the number of
69
PARASITES AND HOST SOCIAL BEHAVIOR
parasites per host (parasite intensity) increases with group size in colonies of breeding birds (Hoogland and Sherman, 1976; Brown and Brown, 1986; Mgller, 1987; Shields and Crook, 1987) and mammals (Hoogland, 1979; Rubenstein and Hohmann, 1989),in nonbreeding flocks of birds (Moore et al., 1988),and in primate troops (Freeland, 1976,1979)(Fig. la). Individual hosts living in large social groups may therefore on average suffer more from the detrimental effects of parasites than individuals living in smaller groups. However, levels of parasite infestation do not always increase with group size, because group living may provide hosts with a means of reducing the negative effects of parasitism by a simple dilution effect
12000 u)
10000
a
1
T
cn 8000
* 0
6000
L
2
4000
z'
2000
E
0
3
4
5
6
7
8
Group size
201
b
-r
u)
.c Q)
T
* 0
-r
10
L
Q)
n
T
E
3
z
0 3
4
5
6
7
8
Group size FIG. I. The loads of two kinds of parasites of feral horses in relation to group size. (a) Eggs produced by intestinal helminths; (b) number of blackflies. Values are means + S.E. (Adapted from Rubenstein and Hohmann. 1989.)
70
ANDERS PAPE M0LLER ET AL.
(Hamilton, 1971). This is the case for blackflies parasitizing herds of feral horses (Equus caballus); large groups have relatively lower infestation rates per individual than smaller groups (Fig. lb; Rubenstein and Hohmann, 1989; see also Freeland, 1976, 1977, 1979; Duncan and Vigne, 1979; Helle and Aspi, 1983; Rutberg, 1987). Optimal group size can be considered a compromise between the costs and benefits of group living. Host species suffering increased levels of parasitism with increasing group size for some parasite taxa, but reduced levels from others, should develop an intermediate optimal group size governed by the relative effects of the different parasite taxa on host fitness. There is evidence suggesting that intraspecific variation in levels of parasitism can be accounted for by variation in the degree of sociality. Is the evolution from asocial to social life also associated with an increase in parasite burdens? This question can be answered when the levels of parasitism of host species or higher taxa are related to their levels of sociality. Only three studies have addressed the question of whether social species harbor larger numbers of parasites than solitary species. Freshwater fish are infected by a number of different parasites, and Poulin (1991a) investigated whether the number of copepod and monogenean parasite species was related to variations in sociality across their hosts. The number of parasite species per host species was clearly positively related to the sampling intensity of fish species included in the study, and this sampling effect was controlled by using the mean number of parasite species per host species per study. However, there was no relationship between parasite abundance and host sociality. This was also the case if potentially confounding variables, such as host size (large hosts harbor more parasites), host age (older hosts may have had time to acquire more parasites), and host range (hosts with large ranges may encounter more parasite taxa), were controlled. Closely related taxa are likely to share characters such as sociality and parasite loads because the character states were acquired from a common ancestor, not because of convergent evolution. The study of ectoparasites on freshwater fish did not control for the effects of phylogenetic similiarity in sociality or abundance of parasites, and the conclusion that there is no relationship between sociality and parasite abundance is therefore only tentative. An alternative explanation is that socially living freshwater fish species may be subjected to frequent parasite attacks, but sociality may simultaneously function as a defense against parasitism. For example, large shoals of three-spined sticklebacks (Gasterosteus aculea?us)experienced a lower rate of parasite attacks than smaller shoals, and shoals did form directly in response to high parasite abundance (Poulin and FitzGerald, 1989).Second, Poulin (1991b) investigated whether group-
PARASITES AND HOST SOCIAL BEHAVIOR
71
living bird species harbored ectoparasites more frequently than solitarily living species. This was predicted to be the case for ectoparasites that are transferred to new hosts by means of contact transmission. but not for highly mobile ectoparasites. Group-living bird species did in fact host contact-transmitted feather mites more often than solitarily living bird species, but this was not the case for highly mobile hippoboscid flies (Poulin, 1991b). The relationship between parasite prevalence and host sociality remained when the confounding effects of host size and host migration habit were controlled statistically. Finally, an unpublished study of ectoparasites in the nests of birds demonstrated a positive relationship between host sociality and both the number of parasite species per host and the intensity of parasite infections (A. P. Mgiller, unpublished). This result remained even when controlling for the confounding effects of phylogeny, host size, host range, and sampling intensity of host species included in the study. In conclusion, there is some evidence in favor of the hypothesis that the evolution of sociality among hosts is associated with acquisition of more parasite species and higher parasite loads.
D. BEHAVIORAL ANTIPARASITE ADAPTATIONS Since the selective consequences of keeping one’s distance from other individuals so as to avoid parasite infection have been underrated, we attempt here to review the effects of selection arising from the parasiterelated cost of social behavior. Two components of social behavior may have become modified as a result of the influence of parasites, viz., group living and reproductive behavior. Group living may have been strongly influenced by parasites because of the cost of close proximity between individuals. Infected individuals, on the other hand, may benefit from social life, since sociality may provide protection of relatively weakened individuals from predators (e.g., Pulliam and Caraco, 1984). Copulation is frequently utilized by parasites for transmission, but the evolution and maintenance of sex may be an adaptation for promoting resistance to parasites (Jaenike, 1978; Hamilton, 1980; Hamilton et al., 1990). Generally, the detrimental effects of parasitism and disease should have selected against large groups until the benefits of group living exceeded the costs. Individual hosts can also be predicted to reduce the probability of parasite transmission by making prudent choices of group membership, including mate choice. Females may obtain indirect fitness benefits as a result of choosing genetically resistant mates which advertise their resistance in elaborate displays or extravagant plumages (Hamilton and Zuk, 1982;Zuk, 1991), but it is likely that direct fitness effects have been even more important than indirect ones (Clayton, 1991a).
72
ANDERS PAPE MOLLER ET AL.
We suggest that animals and plants are able to affect their risks of parasite infestations and the subsequent fitness costs in a number of different ways (Table I). The probability of parasite infestation is likely to increase (a) as the immigration rate into a group increases, (b) as the copulation rate by group members with individuals of unknown health status from other groups increases, (c) as the group is subjected to increasing levels of brood parasitism, and (d) as the proximity of neighboring groups increases. Group members are therefore expected to use behavioral and other measures to reduce the risks of fitness loss. We address each of these factors in the next sections. A number of factors may reduce the risk of parasitism. These factors consist of those preventing infection by parasites and those reducing levels of parasite infestation once group members have been infected. The preventive factors include (a) avoidance of sites within the home range infected with parasites, (b) dispersal and migration so as to avoid areas infected with high levels of parasites, (c)formation of mixed species groups so as to acquire the benefits of group living and avoid the increased costs of parasitism with increasing numbers of conspecifics, (d) testing of the quality of immigrants by means of aggressive behavior, (e) timing of reproduction when parasite abundance reaches a minimum level, and (f) synchronization of reproduction so as to avoid the detrimental effects of increasing numbers of parasites as the reproductive season progresses. The parasite-reducing factors include (a) allogrooming, (b) consumption
SOCIAL FACTORS INCREASING
TABLE I OR REDUCING THE RISKOF PARASITISM
Factors increasing the risk of parasitism Immigration by infected individuals Close proximity of conspecifics Copulation and sexual behavior Brood parasitism
Factors reducing the risk of parasitism Prevention of parasitism Migration/dispersal Avoidance of infected areas Mixed species groups Dominance behavior and test of the quality of immigrants Timing of reproduction Reproductive synchrony Reduction of parasitism Allogrooming Foraging behavior Group living Forced emigration
PARASITES AND HOST SOCIAL BEHAVIOR
73
of antiparasite or prophylactic food items. (c) forced emigration to avoid negative effects of infected group members. (d) emigration by healthy individuals to avoid the negative effects of parasites in a highly infected group, and (e) group formation in order to dilute the effects of parasites. Readers should be fully aware of the often circumstantial or anecdotal evidence for many of the predictions and hypotheses presented in this review. If they use the review as a shopping list for ideas in need of further theoretical, descriptive, or experimental study, we have fulfilled one of our major goals. The impact of the direct fitness effects of parasites on the evolution of host social behavior is reviewed in the following two sections on group living, and on reproduction and sexual selection, respectively. 11. GROUPLIVING A N D PARASITES
In this section we suggest how parasites may have affected group living in a number of important ways in both animals and plants. Close proximity between conspecifics and heterospecifics gives ample opportunities for parasite transmission, and parasites are therefore likely to have modified the pattern of dispersal of individuals. Plants differ in important ways from animals, primarily by being sedentary and by relying on pollinators or other agents for fertilization. However, most of the evolutionary scenarios suggested for animals may recur in modified ways in plants. A.
VARIATIONI N GROUPSIZE
The probability of infection by directly transmitted parasites is often positively correlated with group size (e.g., Hoogland and Sherman, 1976; Freeland, 1976, 1979; Hoogland, 1979; Jennersten et al., 1983; Brown and Brown, 1986; Mgller, 1987; Shields and Crook. 1987; Moore et al., 1988; Rubenstein and Hohmann, 1989), and the detrimental effects of parasites should therefore lead to a reduction in group size. Such changes in individual dispersion patterns may arise either because of a heritable variation in grouping tendency or because of cultural inheritance. Variation in group size should depend on both temporal and spatial variation in the abundance of parasites. For instance, many bird species vary geographically in their tendency to aggregate in colonies, and these differences have usually been attributed to differences in the abundance of food (e.g., Lack, 1968). However, spatial variation in the distribution of parasites may account just as well for such intraspecific variation, with smaller groups in areas where the effects of parasites are more severe (Duffy, 1983). If the benefits
74
ANDERS PAPE MBLLER ET AL.
of grouping are variable, individuals should show phenotypic plasticity in their tendency to aggregate in relation to the costs of parasites, and group living would be predicted to vary temporally and spatially, with the largest groups occurring when the parasite pressure is at a minimum. The net benefits of sociality are often assumed to increase and subsequently decrease with increasing group size. However, group size may not be stable because a solitary individual may gain a net benefit from joining a group, whereas this causes a decrease in average net benefit for other group members (Fig. 2; Pulliam and Caraco, 1984). Similarly, the optimal group size for individuals of a particular quality may not be the optimal group size for individuals of another quality (Fig. 2). As group size increases, so does the possibility for parasites to spread. Individual hosts suffering from parasitism may want to join a particular group in order to enjoy the benefits of group living (e.g., low costs of antipredator behavior or low predation risks), but participants already present may
b
No. of individuals in group FIG.2. Optimal group size in relation to levels of parasitism. (a) An individual in a small group with low average fitness per individual ( I ) may achieve a net fitness advantage by joining a group of the optimal size (21, thereby reducing the average fitness of individuals (3). (b) Individuals differing in quality (e.g., susceptibility to parasitism) may have different optimal group sizes.
PARASITES A N D HOST SOCIAL BEHAVIOR
75
attempt to prevent immigration by infected conspecifics by behaving aggressively. If this is not feasible, the benefits of group living for parasitefree individuals may fall below a net benefit threshold level. Such individuals subsequently may leave the group, and the equilibrium group level will stabilize at a generally lower level than previously. This scenario has not been explicitly tested. Seasonal variation in group size, as shown by many bird species such as larks, finches, and buntings living in pairs during the breeding season, but in flocks outside it, is usually attributed to seasonal differences in the importance of predation and in the dispersion of food or other essential resources (e.g., Lack, 1968). However, if parasites are more abundant and/or more effective during the breeding season of the host as a result of an immunological compromise during reproduction, then the tendency to form groups should vary inversely with the abundance of parasites and the risk of disease transmission. The detrimental effects of parasites on group-living hosts may occasionally be ameliorated by behavior patterns other than those mediating the spacing of hosts. These include grooming and choice of food plants with an antiparasite effect (see Section 11,F). The close proximity of conspecific hosts increases the opportunity for efficient transmission of parasites. This may modify the social behavior of hosts either directly as a result of reduced host population density, or by modification of host social behavior as a means of reducing parasite infestation levels. Parasites may considerably reduce the overall population density of their hosts. Large-scale animal husbandry and production of crops in monocultures are only possible when the effects of parasites are continuously being reduced by large-scale application of pesticides, plant pathology, and veterinary practice. Parasites have also been shown to reduce the density of their hosts in laboratory studies. In a well-known study of interspecific competition in two flour beetles, Tribolium confusum and T. castaneum, Park (1948) recorded a 20% reduction of population size in both host species when the cultures were infected by the sporozoan parasite Adelina tribolii, and observed that the growth of populations of T . castaneum was drastically reduced. Similarly, Lanciani (1975) showed in the laboratory that the parasitic water mite Hydrophantes tenuabilis negatively affected the survival, life span, and number of eggs produced in females of its aquatic hemipteran host Hydrometra myrae. As a consequence, the rate of population increase was reduced in the host species. Similar effects may regularly occur in nature (Gregory and Keymer, 1989; Minchella and Scott, 1991), although there is very little actual evidence so far (Hudson, 1986; Hudson e f al., 1985). Epidemiological models have clearly shown that parasites, in theory, are able to depress the density of their hosts, particularly at low to moderate levels of pathogenicity
76
ANDERS PAPE MOLLER ET AL.
(Anderson, 1979). Reductions of host density will directly reduce the rate of spread and particularly the intensity of damage caused by macroparasites, because effects of parasitism are often density-dependent. An interesting question then becomes whether parasites directly shape the social structure of their hosts because of reductions in host population density, or whether hosts have modified their social behavior as a means of reducing the detrimental effects of parasites. Since host behavior can often be modified on a very short time scale, for instance by cultural inheritance of behavior, hosts may be able to ameliorate the effects of parasites directly by altering their own behavior. B. MIXED-SPECIES FLOCKS Mixed-species grouping is common in many mammals, birds, and fish (e.g., Wilson, 1975), and in plants (e.g., Janzen, 1968,1973; Harper, 1977), and although utilization of a similar food source has been invoked as a null hypothesis, functions like parasite and predator avoidance have also been implied among animals (e.g., Lack, 1954, 1968; Wilson, 1975; Price et al., 1986). Mixed-species flocking would allow relatively easy transmission of parasites between heterospecific individuals because of close proximity. However, parasites and diseases are often strongly host-specific, apparently because of cospeciation of parasites and their hosts (e.g., Mattingly, 1969; Boycott, 1971; Noble and Noble, 1976; Price, 1980; Hafner and Nadler, 1988). Host specificity may reduce the probability of parasite transmission to heterospecificsand reduce the negative effects by parasites that do successfully transfer. Since the risks of infection by host-specific parasites are smaller in mixed-species than in single-speciesgroups of the same size, because there are fewer suitable hosts present, average group size can generally be larger for mixed-species than for single-species groups without increasing the risk of infection. Even if parasites are shared equally among individuals irrespective of species, then mixed-species flocking may be favored, because the costs of parasite transmission are smaller and the benefits of dilution are as large as in single-species flocks (Freeland, 1977). For example, the polyspecific associations of rainforest monkeys are directly related to the activity of the biting flies and mosquitos which transmit monkey malaria (Hepatocystis kochi) and arboviruses such as yellow fever (Freeland, 1977). These parasites are likely to have a considerable negative impact on the monkeys. The relatively low levels of intraspecific competition and the antipredator benefits of mixed-species flocks may provide individuals with the best of all possible worlds. The relatively low frequency of epidemics of plant disease in natural plant communities (Harper, 1977) may similarly be explained by isolation
77
PARASITES A N D HOST SOCIAL BEHAVIOR
through heterospecific neighbors; true monocultures are rare in nature, because density-dependent selection originating from parasites causes reduction in host population density. Particularly abundant host plant species are affected by parasites due to the negative effects of densitydependent parasitism (Harper, 1977).
C. GROUPDISPERSION Group dispersion-the spatial distribution of groups-may be affected by risks of parasite transmission. If a habitat is not totally saturated with groups (which may be as small as monogamous pairs), the defense of small exclusive areas by randomly dispersed groups will reduce the probability of finding other groups within a critical transmission distance (Fig. 3; Andren, 1989). As the defended area increases, the probability of sharing the nearest neighborhood with conspecifics decreases rapidly, and so does the probability of parasite transmission. Territoriality may thus have evolved partly as an effective disease-avoidance mechanism. Areas need not be directly defended by group members in order to maintain group dispersion as long as the costs of parasite transmission do not exceed the
0
10
20 30 Nearest neighbor distance
40
(in m at a density of 1000 groups/ km2)
FIG.3. Group dispersion as a defense against parasites. Defense of small exclusive areas leads to overdispersion of groups and hypothetically to reduced level of parasite transmission. The figure shows cumulative frequency distributions of nearest neighbor distances for randomly dispersed groups (A), for groups located within territories of I00 units in size (i.e., all territories cover 10% of the area) (B), and for groups located in territories covering 20, 33. and 50%. respectively, of the area (C, D, and E). One unit on the x-axis (in meters) equalsddensity/1000 (with density measured in number per km?. (From Andren. 1989.)
78
ANDERS PAPE MBLLER ET AL.
benefits of use of the same area by more than a single group. Mixedspecies groups may similarly be dispersed with a subsequently reduced overlap because of the effects of parasites. Since the high degree of host specificity of parasites only permits successful infection of closely related species (e.g., Mattingly, 1969; Boycott, 1971; Noble and Noble, 1976; Price, 1980), groups of congeners should be more dispersed than more distantly related species. Interspecific territoriality has been suggested to arise because of competition between closely related species for a common, limiting food resource (Murray, 1971),but the question remains open whether parasitism or competition is the most important selective agent. If parasites are the important factor, then parasitism is able to mediate the outcome of interspecific competition at a local level as well as on a larger geographical scale. Evidence suggests that interspecific competition is often mediated by the effects of parasites (Barbehenn, 1969; Cornell, 1974; Holmes, 1982; Freeland, 1983; Holt and Pickering, 1985; Price e t a l . , 1986, 1988; Gregory and Keymer, 1989). D. DOMINANCE BEHAVIOR Dominance behavior is a common phenomenon in animals that causes differential access among conspecifics to food and other limiting resources (e.g., Wilson, 1975). Dominant individuals sometimes may even expel conspecifics from a particular area, so that subordinates remain an outcast group away from important resources (e.g., Wilson, 1975; Morse, 1980). Subordinates are often young individuals (e.g., Morse, 19801, which suffer more severely from parasites than older, more dominant conspecifics (e.g., Christian and Davis, 1964; Noble and Noble, 1976; Cox, 1982; Holmes, 1982; Halvorsen, 1986; Noble et al., 1989). The more frequent and more severe parasite infections of subordinate host individuals can either be due to their lower overall quality and/or the less efficient immune system of young, stressed individuals. Since subordinate individuals often have a disproportionately large probability of being infected with parasites, dominance relationships may render dominant individuals less likely to become infected themselves. Once established, dominance relationships are often very effective, since subordinates yield to dominants with little protest (e.g., Wilson, 1975; Morse, 1980). As a result, risks of bodily contact and thus transmission of parasites are reduced. Male sex hormones (e.g., testosterone) have been shown to affect the dominance status and aggressive behavior of males, and dominant individuals have higher levels of plasma testosterone than low-ranked individuals (Eberhart et al., 1983; Keverne, 1986). Testosterone is required for the production of sexual characters and maybe for badges that show an individ-
PARASITES AND HOST SOCIAL BEHAVIOR
79
ual’s dominance status (Alcock, 1989). However, testosterone also has a suppressive effect on the immune system, which makes individuals with high circulating levels of androgens more vulnerable to disease (Grossman, 1985; Folstad et al., 1989; Masataka et al., 1990; Folstad and Karter, 1992). Dominant behavior or reliable signals of dominance rank such as badges may reduce the number of escalated fights with subordinate individuals which are likely to be infected. Individuals have to optimize their levels of dominance, expression of secondary sexual characters, and levels of immune defense. The positive relationship between androgen levels and the expression of secondary sexual characters and the negative relationship between androgens and immune defense may prevent males from cheating (i.e., behaving as more dominant that permitted by their overall phenotypic quality)(Folstad and Karter, 1992). Males producing very high levels of testosterone must pay for this in their reduced level of immune defense, and only high-quality individuals are likely to be able to pay this cost. Many animal species wear badges, which appear to signal the relative dominance status of their bearer to conspecifics, and as a result the number of fights involving direct bodily contact is reduced (Rohwer, 1977). For this reason, the risk of parasite transmission is probably similarly reduced. If there is incongruity between the status signaled by the badge and the behavior of an individual, then the number of escalated fights increases markedly (Rohwer, 1977).One possible reason why such incongruity leads to severe fights is that individuals behaving abnormally may suffer from diseases (Rohwer, 1977; Hart, 1990). If the incongruent individual is accepted without escalated fights, it will remain in the neighborhood, and the probability of direct or indirect parasite transmission will increase. However, if fighting quickly leads to the expulsion of incongruent individuals, then the probability of infection during a short, severe fight may be smaller than during a long-lasting residence without any fights.
E. DISPERSAL A N D MIGRATION
I
i
1
j
!
I
Dispersal is the transfer of a single individual from one site (or group) to another. The individual host’s decision whether or not to disperse, how far to travel, and where to settle may depend on a large number of factors, such as the costs of dispersal and the benefits of outbreeding (e.g., Swingland and Greenwood, 1983). One additional factor may be the level of parasite infection (Freeland, 1976). The decision of whether or not to disperse may depend on an individual’s own state of infection and that of conspecifics in the neighborhood and in the settlement area. Any individual’s decisions on dispersion should be related to the risks or parasitism
80
ANDERS PAPE MBLLER ET AL.
relative to the benefits of movement. Residents tend to dominate recently arrived conspecifics because of site-related dominance (e.g., Wilson, 1975; Morse, 1980), and the likelihood of becoming accepted, and therefore of successful establishment of a disperser, may depend on its state of infection. If parasitism affects the behavior of dispersers, residents may react toward prospective settlers in relation to their behavior. Individual dispersers showing signs of parasitism in their behavior and appearance should be treated more despotically by residents than should apparently healthy and vigorous individuals. Individuals that remain within the group are less likely to become infected with alien parasites than are individuals that move between groups, since animals that move between groups may carry parasites infectious to residents of established groups. For example, primate groups keep newcomers at the periphery of the group and often threaten or attack them, and this leads to behavioral and nutritional stress. If the newcomer is harboring parasites or a latent infection, this treatment will cause it to become visibly sick, and it may not be allowed access to the group (Altmann and Altmann, 1970; Freeland, 1976). The negative effects of parasitism may also be avoided if infected group members are forced to disperse, although we have been unable to find examples of such forced dispersal. Migration is long-distance, directed movement between sites, for instance, between sites used for reproduction and wintering sites. Individuals often migrate in flocks and over extended periods of time, and conspecifics from different geographical areas may differ in the timing and direction of their migration (e.g., Baker, 1978). Conspecifics belonging to populations from different areas might also differ in their parasite infections. Selection could affect an individual’s choice of traveling companions and hence the timing and the path of its migration, since this would reduce or prevent acquisition of more virulent parasites from conspecifics belonging to different populations. Many bird species show clear boundaries between populations migrating in different directions and wintering in different areas. For example, garden warblers (Sylvia borin) breeding in Western Europe migrate in a southwesterly direction, while individuals breeding in Scandinavia and Eastern Europe migrate toward the southeast. Such boundaries might be maintained and mediated by different parasite populations, since individuals of one host population might be competitively superior due to more severe effects of parasites on individuals belonging to the other population (e.g., Price, 1980; Holmes, 1982; Price er al., 1986, 1988; Gregory and Keymer, 1989). This would require consistent, long-term variation in host resistance and parasite virulence between regional host groups that exceeds the variation among individuals within groups.
PARASITES AND HOST SOCIAL BEHAVIOR
81
F. OTHERANTIPARASITE STRATEGIES Since parasites frequently reduce the fitness of their hosts, a variety of behavioral patterns may be involved in the avoidance or reduction of parasitism, for example, grooming and preening and foraging behavior. Ectoparasite numbers can be reduced by direct removal of parasites from pelage or plumage. Grooming and preening are efficient ways of reducing loads of ectoparasites as demonstrated in experiments in which hosts are prevented from performing cleaning behavior (e.g., Snowball, 1956; Bell et a/., 1962; Brown, 1972; Murray, 1987, 1990). For example, rock pigeons (Colurnba livia) prevented from preening had elevated levels of infestation by feather lice (Clayton, 1991a). Self-grooming implies licking and scratching parts of the body that host individuals are able to reach. Both self-grooming and allogrooming are common in mammals (e.g., Bolles, 1960; Freeland, 1981b; Hart and Hart, 1988; Wilkinson, 1986). Allogrooming is particularly frequent in highly social animal species such as primates (e.g., Seyfarth, 1983). and by engaging in allogrooming animals can obtain grooming for parts of the body that cannot easily be reached during self-grooming. Allopreening, which is commonly observed among mated pairs of birds, is primarily concentrated on the head and the neck of the receiver-the areas that an individual cannot easily reach itself (Harrison, 1965; Brooke, 1985; Simmons, 1985). Allopreening appears to reduce parasite loads, as demonstrated for penguins without a grooming partner. Single individuals had much higher parasite loads than mated individuals which received a considerable amount of allopreening (Fig. 4; Brooke, 1985). However, the possibility cannot be ruled out that some additional factor made penguins prone to tick infestation and also made them unattractive as mates. Birds also engage in anting, whereby the plumage is treated with formic acid, which is believed to reduce parasite infestation (Simmons, 1966). Dust bathing is also assumed to reduce parasite infestation (Simmons, 1985). It is unknown whether anting and dust bathing are more common among highly social bird species. Antiparasite behavior involving more than one species includes heterospecific cleaning behavior. Well-known is the aquatic cleaning symbiosis in which smaller fish remove ectoparasites from larger fish (Feder, 1966). Oxpeckers in Africa forage on large ungulates by pecking ticks and other ectoparasites from the skin of the hosts (Bezuidenhout and Stutterheim, 1980; Hart and Hart, 1988). Other examples are Darwin’s finches removing ticks from Galapagos tortoises(Geochelone eiephanropus)(McFarland and Reeder, 1974) and from marine iguanas (Amblyrhynchus cristatus)(Amadon, 1967; Carpenter, 1966). It is unknown whether cleaning symbioses
82
ANDERS PAPE M0LLER ET AL.
0
80
Macarmi Rockhopper
3 Y
-s Q 2
60
e
I
40
Y
i= 20
0
Unpaired
Paired Mating 8tstUS
FIG. 4. Parasite infestation of unpaired and paired macaroni (Eudypres chpsolophus) and rockhopper ( E . chpsocome) penguins. Unpaired individuals were unable to receive allopreening. (Adapted from Brooke, 1985.)
have evolved more often among highly social host species suffering from more intense parasite infestations. Animals avoid places of potential infection by selective foraging. The habit of ungulates not to eat grass growing in the vicinity of feces protects the animals from infestation by intestinal parasites (Michel, 1955; Odberg and Francis-Smith, 1977). Cattle (Bos taurus) are able to detect areas with high concentrations of tick larvae and avoid those areas (Sutherst et al., 1986). Cattle not only avoid grazing in infected areas, but they also defecate in areas away from grazing sites. It is unknown whether preferential foraging in uninfected areas is more developed among group-living ungulates. Felids and canids protect their young from parasitic exposure by keeping the nest or den free from eliminations (Hart, 1985). Also, sows (Sus scrofa) and piglets keep their sleeping quarters clean by defecating elsewhere (Buchenuer et al., 1982; Whatson, 1985). Nest sanitation patterns are also prevalent in birds. These include removal of fecal sacs, ejection of feces over the rim of the nest, and frequent renovation of the nest-lining material (Bucher, 1988). Choice of nest-lining material may also reduce parasite loads, since several plant species have repellent or pesticide properties (Wimberger, 1984; Clark and Mason, 1985; Clark, 1991). It is unknown whether nest sanitation patterns are more developed among social animals which may suffer from higher levels of parasitism.
PARASITES AND HOST SOCIAL BEHAVIOR
83
Baboons (Papio cynocepphalus)use several roosting sites and they regularly rotate between these roosts. They only stay for two nights at one site, apparently because parasite eggs start hatching on the third night. Baboons wait about 10 days before returning to a site, and this behavior reduces the risk of parasite exposure since most parasite larvae are likely to have died when the baboons return next time (Hausfater and Meade, 1982).
Hosts may select particular diets to fight their parasites, both in order to prevent and to eliminate infections. Observations of wild chimpanzees (Pan troglodytes) have shown that sick individuals eat plants which are not part of their regular diet (Takasaki and Hunt, 1987; Hart and Powell, 1990; Lozano, 1991; Newton, 1991). The plants eaten are used by local African people for medical purposes, and they may have similar effects in primates (Watt and Breyer-Brandwijk, 1962). Plant food items may also have prophylactic properties which prevent parasite infections if consumed on a regular basis (Lozano, 1991). Many antiparasite drugs are derived directly from plant compounds, and it is an intriguing possibility that animals may often fight their parasites by foraging for plants with antiparasitic effects. These habits should be particularly well developed in social species if they regularly suffer from intense parasite infestations.
G. CONCLUSION Different antiparasite behaviors may prevent infection by parasites or reduce levels of infestation once hosts are infected. Some of these behaviors may be more common among social animal species, although detailed comparative studies are absent. It is usually not known whether there is a direct causal relationship between the use of a particular antiparasite behavior and levels of parasitism.
111. PARASITES, REPRODUCTION, A N D SEXUAL SELECTION
Mating decisions and reproductive success of both animals and plants may be greatly influenced by parasites. Reproductive success is known to be considerably reduced by parasite infection in many animal and plant species (e.g., Elton, 1927; Fisher and Holton, 1957; Mattingly, 1969; Boycott, 1971; Burnet and White, 1972; Day, 1974; Page, 1976; Anderson and May, 1982; Burdon, 1987; Keymer and Read, 1989; Alexander, 1990; MOller et al., 1990), and prospects for future reproduction and survival may similarly be reduced or even completely eliminated through sterilization of the host (e.g., Noble and Noble, 1976; Jennersten, 1988). Reproduc-
84
ANDERS PAPE MBLLER ET AL.
tion requires close bodily contact in species with sexual reproduction, and particularly in those with internal fertilization; as a result the probability of parasite transmission is considerably increased. A whole series of venereal pathogens illustrate this point (e.g., Page, 1976; Anderson and May, 1991). Venereal diseases also occur among plant species as pollinator-transmitted diseases (e.g., Ustilago infection of caryophyllaceous hosts [Jennersten et al., 1983; Alexander and Antonovics, 19881). Even though sex may increase transmission of parasites, avoidance of parasitism may be the major force favoring the evolution and the maintenance of sex (Jaenike, 1978; Hamilton, 1980; Hamilton et al., 1990). Selection arising from the detrimental effects of parasites would favor individuals able to choose mates such that the probability of infection decreases. The ability to choose mates uninfected by parasites is important, and sexual selection, usually labeled as the combination of mate choice and intrasexual competition (Darwin, 18711, may be influenced by the risks of parasite transmission.
A. INTERSEXUAL SELECTION
Individuals of the choosy sex have a number of opportunities to assess the infection rate of potential mates. These range from long-distance assessment of display and overall health and vigor, to closer inspection of plumage, pelage, and skin, to direct detection of ectoparasites (Borgia and Collis, 1990; Clayton, 1990). There is some evidence that both parasite infection and disease directly affect display and plumage quality (e.g., Page, 1976; Hamilton and Zuk, 1982; Harrison, 1985; Zuk, 1991;Clayton, 1990, 1991a. and references therein). Mate choice for parasite-free individuals could considerably reduce the direct fitness consequences of parasitism. Mate choice may lead to the acquisition of mates with genes for resistance to those parasites presently exploiting the host population (Hamilton and Zuk, 1982). Because parasites and their hosts may continuously coevolve, generating new additive genetic variation in host resistance as well as the ability of parasites to exploit hosts, mate choice could be for “good genes,” which would be transmitted to offspring (Hamilton and Zuk, 1982). While the comparative evidence is ambiguous, the results from specific studies lend some support to this hypothesis (Hamilton and Zuk, 1982; Mgiller, 1990; Read, 1990; Clayton, 1991a; Zuk, 1991). Mate choice based on parasite avoidance can be beneficial, either because of the direct fitness effects on the adults and their parenting ability, or because of indirect fitness gains to be achieved, if resistance to parasites is heritable.
PARASITES AND HOST SOCIAL BEHAVIOR
85
The relative importance of direct and indirect fitness effects of mate choice as influenced by disease and parasitism remains to be established.
B. INTRASEXUAL SELECTION Intrasexual competition usually takes the form of competition between males for access to females (Darwin, 1871). The overall health and vigor of individuals are likely to depend partially on their past and present infection with parasites (e.g., Freeland, 1976; Page, 1976; Hamilton and Zuk, 1982; Read, 1988). The outcome of male-male competition is thus likely to be influenced by the effects of parasites, and winners of contests are predicted to have fewer parasites than losers (Howard and Minchella, 1990). Females should induce male-male competition, because individuals put under severe stress are more likely to reveal the presence of any serious pathogen than are relaxed individuals. Fighting and other aggressive behavior among males depends on circulating levels of androgens, which have a depressing effect on the immune system (Grossman, 1985; Folstad and Karter, 1992). Intense male-male competition should therefore reliably reveal the quality of males because prolonged periods of intense competition are likely to result in a reduced immune defense, particularly among low-quality individuals unable to cope with the costs of elevated levels of circulating androgens. Females choosing a mate after male-male competition has taken place therefore are likely to mate with males infected with relatively few or innocuous parasites. As a consequence, infection risks may be reduced for choosy individuals and their offspring.
C. SEXUAL SELECTION A N D VENEREALDISEASE I N PLANTS Mate choice and avoidance of venereal diseases are more complicated among plants since they are sedentary and many are dependent on pollinator services. Pollinators often simultaneously transfer pollen and diseases. Efficient pollination depends on attraction of efficient pollinators and the dispersion of conspecific and heterospecific plants in the neighborhood (e.g., Handel, 1983).Pollination limits seed set (e.g., Bierzychudek, 1981), and plants might increase fitness either by relying on self-fertilization or by increasing selection for more efficient floral displays, assuming that these would attract more pollinators. Traits that increase pollination levels will either be maintained by selection due to competition among males for access to females or due to competition among females for access to pollen
86
ANDERS PAPE M0LLER ET AL
and therefore indirect access to males, or both. For instance, a large number of flowers per plant are selectively advantageous primarily because they increase male reproductive success (Willson and Price, 1977; Queller, 1983). The form, size, and color of floral structures in plants may be the evolutionary outcome of interactions between plants and their pollinators (e.g., Darwin, 1862; Feinsinger, 1983). Much present-day intraspecific variation in the morphology of flowers is directly related to fitness, since floral structure has been shown to influence transfer of pollen and hence seed set (e.g., Waser and Price, 1981; Stanton et al., 1986; Galen, 1989). Stabilizing selection on flower morphology suggests that flowers at both the upper and the lower extreme are at a selective disadvantage, and pollinator specialization thus appears to be a driving force in the evolutionary divergence of floral traits. Mate choice in plants, which can result in more viable offspring (e.g., Mulcahy, 1971; Bertin, 1986; Marshall and Ellstrand, 1986), could occur as prepollination or postpollination choice. Prepollination preference for mates could depend on floral traits that manipulate pollinators by promoting the receipt of preferred pollen. However, data suggest that plants have little control over pollinators (Stephenson and Bertin, 1983). Female mate choice in plants could also rely on multiple matings and postpollination choice either through selective seed abortion (Stephenson, 1981), or through female-mediated differential growth of pollen tubes (Mulcahy, 1971; Snow and Spira, 1991). Since efficient pollen transfer also promotes disease transmission by pollinators or wind, there should exist a trade-off between offspring quality and risk of disease transmission. If floral traits were sexual ornaments promoting the fitness of plant individuals, one should expect strong directional selection on flower morphometrics. Frequent visits by specialist pollinators to the very attractive flowers of a single individual may increase its fitness both because of large seed set and because of efficient pollen transfer. Howe,ver, venereal diseases in plants may also be particularly efficiently transmitted to and from the plant individuals carrying the most attractive flowers. Plants therefore might benefit from attracting pollinators able to discriminate against parasitized and nonparasitized conspecific individuals. However, parasites can modify the appearance of plants and the phenology of their flowering, and through such manipulation improve their own dispersal (e.g., Jennersten, 1988; Alexander and Antonovics, 1988). Plant parasites may therefore indirectly manipulate the behavior of pollinators, because they are particularly attracted by large inflorescences, and flower morphology also plays an important role in the attraction of pollinators (Darwin, 1862; Willson and Price, 1977). Coevolutionary arms races between the plant and its
PARASITES AND HOST SOCIAL BEHAVIOR
87
pollinator-transmitted parasites are likely to ensue, and disease could influence the otherwise directional evolution of floral traits.
D. MATING SYSTEMS Mating systems among animals and plants have generally been considered to depend on the environmental potential for individuals of one sex to attract and monopolize individuals of the other sex (Emlen and Oring, 1977; Willson and Burley, 1983). Sexual reproduction may impose a considerable cost in terms of transmission of parasites and venereal diseases, but at the same time sex also allows recombination and the generation of efficient defenses against parasites. Animals with nonmonogamous mating systems may suffer from the effects of parasites and venereal diseases for two different reasons: (a) the risk of contracting diseases and parasites increases during sexual contact; and (b) animals with particular mating systems are more susceptible to infections. The probability of becoming infected with parasites should increase with an increasing number of mates, particularly those of low quality which are more likely to be infected with parasites, and the degree of polygyny and polyandry in particular populations may thus be influenced by their past and present parasite infection rates. The relative rarity of mating systems without pair bonds (promiscuity) in animals is not surprising, since such a mating system would greatly increase the probability of parasite transmission. Animals with different mating systems differ considerably in their levels of circulating androgens, and there is a positive relationship between the degree of polygyny and androgen levels (Wingfield et al., 1990). Male sex hormones directly affect levels of aggression and the expression of secondary sexual characters, but they also depress the efficiency of the immune system (Grossman, 1985; Folstad and Karter, 1992). It is therefore likely that susceptibility to parasites and diseases generally increases with increasing levels of androgens. Only high-quality individuals will be able to sustain high levels of androgens without compromising the immune system. The variance in the immune defense and thus in the levels of infestation with parasites and pathogens may therefore be larger in a highly polygynous mating system compared with a monogamous one. If female choice as opposed to male-male competition is very important, then aggregation and display at leks will be stressful to males and expose any severe pathogens or parasites to females. Males of lekking species spend a considerable amount of time displaying and fighting other males, and they are unable to acquire food or other important resources during display. High levels of aggression will be associated with elevated levels
88
ANDERS PAPE MBLLER ET AL
of circulating androgens, which have a depressing effect on the immune system (Grossman, 1985; Folstad and Karter, 1992). Only high-quality individuals will be able to display and fight at a high rate without compromising their immune defense, and females should prefer such males as mates.
E. MULTIPLEMATING Sperm competition, which is competition between sperm delivered by different males for the fertilization of a single clutch of eggs, is widespread among animal taxa (Parker, 1970; Smith, 1984). Species with apparent monogamous mating systems show deviations from stable pair bonds, and the frequency of extra-pair copulations is often high (e.g., Birkhead et al., 1987; Mgller and Birkhead, 1989; Birkhead and Mgller, 1992). Attempts by males to sequester females €or extra-pair copulations may increase the probability of transmission of parasites, and females are expected to attempt to avoid infected males. Male barn swallows (Hirundo rustica) successful in obtaining extra-pair copulations actually harbored fewer hematophagous mites and mallophaga than did unsuccessful males (Mgller, 1991). Hamilton (1990) has suggested that ornaments and elaborate sexual displays in monogamous animals have evolved because females thereby obtain an opportunity to assess quickly the quality of neighboring males in relation to the quality of their own mate. This hypothesis requires that most extra-pair copulations are invited, or at least not resisted, by females, but generally this does not appear to be the case (McKinney et al., 1984). The frequency of extra-pair copulations increases with group size in both birds and mammals (e.g., Gladstone, 1979; Birkhead et ul., 1987; Mgller and Birkhead, 1989; Birkhead and Mgller, 1992), and the probability of parasite transmission during extra-pair copulations may therefore also have selected for decreased group size. There is very little evidence available that venereal disease and parasite transmission are important costs of copulation with multiple partners in species other than humans. However, ectoparasites such as the chicken body louse (Menacanthus strumineus), which congregate near a chicken’s cloaca(Loomis, 1978), are likely to be transmitted from one host to another during copulation. Similarly, feather lice on the back of female pheasants (Phasianus colchicus) are transmitted during copulation since these parasites are found following copulation on sticky plates attached to the legs of male pheasants (N. Hillgarth, personal communication). Many animal species groom or shiver following copulation and this may be a way of getting rid of parasites that might have been transmitted during copulation (Hart, 1990). For example, rats (Rattus noruegicus) engage in genital
PARASITES AND HOST SOCIAL BEHAVIOR
89
grooming following copulation, and individuals prevented from doing so acquire bacterial genital infections more often than controls (Hart et al., 1987). However, the direct fitness consequences of these parasite infections acquired during copulation are not known.
F. BROODPARASITISM Females of several insect, fish, and bird species are intraspecific nest parasites and parasitize the offspring rearing ability of conspecific individuals (e.g., Yom-Tov, 1980; Anderson, 1984; Petrie and Mdler, 1991). Visits by strange females at a breeding site may increase the probability of parasite transmission, particularly if intraspecific nest parasitism is a “best-of-a-bad-situation” conditional strategy, and if intraspecific nest parasitic individuals are heavily infected and visit many different sites. Even if it may impose only moderate costs to rear the offspring of conspecifics, as in precocial bird species (Yom-Tov, 1980; Anderson, 1984; Petrie and Mgller, 1991), transmission of parasites may render intraspecific nest parasitism costly to victimized individuals. Interestingly, ectoparasites are sometimes found on bird’s eggs (e.g., Rankin, 1982), and any bird touching such eggs will become infected. Since the probability of intraspecific nest parasitism increases with the size of social groups (e.g., Brown, 1984), it is possible that parasite transmission through extra-pair copulations, intraspecific nest parasitism, and similar alternative reproductive strategies may also have played a role in the evolution of group size. G. TIMING OF REPRODUCTION Timing of reproduction is usually assumed to be tuned to the period when food is maximally available (e.g., Lack, 1954). Because conspecific hosts regularly get into close bodily contact only at this particular time of the year, the probability of disease and parasite transmission is generally high. Offspring with relatively weak immune defenses against parasites can also be readily colonized at this particular time of the year. Selection should modify the timing of reproduction in the host population to minimize the effects of disease and parasitism. Hosts could do that by preferentially reproducing earlier or later than the optimal timing for reproduction. of their parasites. It is likely that early reproduction among hosts would be selectively favored since environmental conditions for reproduction among ectoparasites improve late during the season. Timing of reproduction could change if there were selection on this trait, because it is heritable (van Noordwijk et al., 1981). It is not likely that hosts are able to reduce the effects of parasitism by
90
ANDERS PAPE M0LLER ET AL.
altering the timing of reproduction. Parasites have short generation times compared with those of their hosts. Selection on parasites is more intense than on their hosts, because parasites only constitute one of many selection pressures on the host population, while successful reproduction among the parasites is essential for their future success. This suggests that, on average, hosts will be unable to avoid the detrimental effects of parasitism by altering their timing of reproduction, because parasites will generally be able to respond to an altered timing of reproduction in the host population.
H. REPRODUCTIVE SYNCHRONY Reproductive synchrony may affect the probability of parasite transmission if a short, synchronous reproductive season restricts transmission possibilities relative to a long, asynchronous season (Emlen, 1986). Late reproducing host individuals often suffer from the detrimental effects of parasitism and disease more than the synchronous majority (e.g., Moss and Camin, 1970; Brown and Brown, 1986; Emlen, 1986; Loye and Carroll, 1991), perhaps as a result of the growth and buildup of parasite populations during the peak reproductive period of the host. Relative reproductive synchrony in host populations should therefore be affected by the seasonal variation in detrimental effects of parasites. Group-living animals reproduce highly synchronously compared to solitary animals, and it has been claimed that predation is the main agent selecting for this synchrony (Wittenberger and Hunt, 1985). Parasites may just as well have favored the evolution of synchronous reproduction. Flowering synchrony in plants promotes efficient pollen transmission, but also efficient transmission of diseases (e.g., Jennersten, 1985), and costs due to parasites may balance benefits due to pollen transmission and large seed sets. There should thus be a trade-off between efficient pollination and avoidance of plant diseases. Plant diseases are sometimes able to govern the flowering time of their hosts. For example, individual hosts of Ustilago infections actually flower earlier than uninfected individuals, thereby increasing flowering asynchrony ( Jennersten, 1985). Early and prolonged flowering by parasitized individuals clearly promotes efficient dispersal of the parasite, and the degree of flowering synchrony is likely to be the outcome of an evolutionary arms race between parasites and plant hosts. Parasites benefit from infecting early, and thus asyncronously, flowering hosts while plants benefit from flowering highly synchronously.
PARASITES AND HOST SOCIAL BEHAVIOR
I.
91
CONCLUSION
Parasites may exert a number of different selection pressures on reproduction among their hosts, particularly if parasites often synchronize their own reproduction with that of their hosts. A number of antiparasite adaptations have been suggested, but most of these are only supported by weak circumstantial evidence.
IV. SOCIALBEHAVIOR A N D PARASITE-HOST COEVOLUTION Parasites must continuously respond to the evolution of host resistance by adapting to the new host environments. Parasites may enter coevolutionary relationships with infected host populations, with changes in host resistance being followed by changes in infectivity and virulence of the parasites (Futuyma and Slatkin, 1983; Rollinson and Anderson, 1985; Wakelin and Blackwell, 1988; Alexander, 1992). Coevolution of parasites and their hosts may continuously generate new additive genetic variance in the resistance to parasites and in the ability of parasites to exploit their hosts (Clarke, 1979; Lewis, 1981; Hamilton and Zuk, 1982). Because of the more efficient spread of parasites among social organisms compared to solitarily living ones, it is likely that the intensity of selection due to parasites should on average be stronger for social individuals (Fig. 5 ) . Efficient spread of parasites and diseases among highly social individuals may cause rapid evolutionary responses by hosts to parasites, and this in turn should select for similarly rapid counteradaptations among parasites. The virulence of parasites exploiting highly social hosts could either increase or decrease as a response to more efficient host defenses (Fig. 5). It is unlikely that the virulence of parasites exploiting social hosts generally decreases, because the detrimental fitness effects of parasites on social hosts appear to be as strong or even stronger than among solitary hosts (e.g., Mgller et al., 1990). If the virulence of parasites exploiting highly social hosts generally increases, parasite-host coevolution may be more rapid among socially as opposed to solitarily living host populations. The reason for this is that parasites form a strong selection pressure on the host, which may respond by developing a more efficient defense against parasites. Parasites should respond to an improved level of host defense by increasing their virulence. Parasites may thrive better on very common host genotypes, and hosts may be better able to defend themselves against very common parasite genotypes (Haldane, 1949). Frequency-dependent selection on hosts will reduce the rate of dispersal of parasites and the amount of the damage they cause. Specialization by parasites exploiting
92
ANDERS PAPE MBLLER ET AL.
SOLITARY
SOCIAL
Host quality -+
a
a
SELECTION ON HOSTS
weak
intense
HOST DEFENSES AGAINST PARASITES
weak
strong
SELECTION ON PARASITES
weak
intense
PARASITE RESPONSE
weak increase in virulence
TO SELECTION FROM HOST
( i 1 reduced virulence (i i ) increased virulence
FIG. 5. Parasite infestation levels of solitary and social animals and the effects on the intensity of selection on the host and the parasite population.
socially living host species therefore may relatively quickly lead to speciation among parasites, and the number of parasite species exploiting social host species and their host specificity should, for this reason, be comparatively large. The probability of infection by ectoparasites increases directly with group size, and the detrimental effects of parasites will, as a counterplay, lead to reductions in host group size. Parasites will reduce host population density, and the largest depression of host population density should occur at low to moderate levels of parasite pathogenicity (Anderson, 1979). Reductions in population density of hosts may also lead to reductions in group size. Alternatively, changes in host group size could take place either because of a heritable variation in the tendency of grouping or because of cultural inheritance. Because the pattern of group living can be modified through rapid changes in behavior without any underlying
PARASITES AND HOST SOCIAL BEHAVIOR
93
genetic changes, whereas the responses of parasites to their hosts may mainly occur because of mutations, behavioral changes in hosts may not always be tracked by parasites in a coevolutionary manner. Rapid behavioral changes such as those described in this article may be an important way for vertebrates to combat parasites, and cultural inheritance may have played an important role in the adjustment of social behavior to the ubiquitous perils of parasitism and disease.
V.
SUMMARY
Parasites and diseases are important selective factors directly affecting the fitness of both animal and plant species. Close proximity to already infected individuals or to individuals belonging to a parasite reservoir is an important factor promoting transmission of parasites from one host individual to another. Selection arising from the detrimental effects of parasites therefore should strongly have affected the social behavior of both animal and plant species. Parasites should particularly have affected the grouping or the clumping behavior of animals and plants in a number of ways, including group size, size and composition of mixed-species groups, 'group dispersion, dominance and status signals, and various phenomena related to dispersal and migration. Reproduction and sexual selection should similarly have been molded by the selective forces of parasites, and mate choice, intrasexual competition, mating systems, alternative reproductive strategies, timing of reproduction, and reproductive synchrony should all have been modified. The effect of parasites as selective forces affecting the social behavior of animals may be ameliorated by rapid cultural changes among hosts, and cultural inheritance of behavior may be an efficient way for vertebrate hosts to escape the detrimental effects of parasitism and disease. Most of the data presented in this review are circumstantial and many of the ideas are highly speculative and in need of further theoretical, descriptive, and experimental study.
Acknowledgments
We are grateful for the comments provided by D. H. Clayton, W. D. Hamilton, 0. Jennersten, A. Keymer, C. Magnhagen, M. Milinski, A. Read, and S. Ulfstrand. The work was supported by a grant from the Swedish Natural Science Research Council.
94
ANDERS PAPE M0LLER ET AL.
References Alcock, J. (1989). “Animal Behavior,” 4th ed. Sinauer, Sunderland, MA. Alexander, H. M. (1992). Evolution of disease resistance in plant populations. In “Ecology and EvolutionofPlant Resistance” (R. S. Fritzand E. L. Simms, eds.). Univ. ofChicago Press, Chicago. In press. Alexander, H. M., and Antonovics, J. (1988). Disease spread and population dynamics of anther-smut infection of Silene alba caused by the fungus Ustilago uiolacea. J . Ecol. 76,91-104. Alexander, R. D. (1974). The evolution of social behavior. Annu. Reu. Ecol. Syst. 5,324-383. Altmann, S . A., and Altmann, J. (1970). “Baboon Ecology: African Field Research.” Univ. of Chicago Press, Chicago. Amadon, D. (1967). Galapagos finches grooming marine iguanas. Condor 69, 3 I I. Anderson, R. M. (1979). The influence of parasitic infection on the dynamics of host population growth. I n “Population Dynamics” (R. M. Anderson, B. D. Turner, and L. R. Taylor, eds.), pp. 245-281. Blackwell, Oxford. Anderson, R. M., and May, R. M., eds. (1982). “Population Biology of Infectious Diseases.” Springer, Berlin. Anderson, R. M., and May, R. M. (1991). “Infectious Diseases of Humans.” Oxford Univ. Press, Oxford. Anderson, M. (1984). Brood parasitism within species. In “Producers and Scroungers“ (C. J. Barnard, ed.), pp. 195-228. Chapman & Hall, London. AndrCn, H. (1989). Predation processes in fragmented boreal forest landscapes. Ph.D. thesis, Uppsala University, Uppsala, Sweden. Arthur, D. R. (1962). “Ticks and Disease.” Pergamon, Oxford. Baker, H. G. (1947). Infection of species of Melandrium by Ustilago uiolacea (Pers.) Fuckel and the transmission of the resultant disease. Ann. Eot. (London) 11, 333-348. Baker, J. R. (1975). Epizootiology of some haematozoic protozoa of English birds. J. Nut. Hist. 9, 601-609. Baker, R. R. (1978). “The Evolution and Ecology of Animal Migration.” Holmes and Meir, New York. Barbehenn, K. R. (1969). Host-parasite relationships and species diversity in mammals: An hypothesis. Eiotropica 1,29-35. Behnke, J. M., and Wakelin, D. (1973). The survival of Trichuris muris in wild populations of its natural hosts. Parasitology 67, 157-164. Bell, J. F., Jellison, W. I., and Owen, C. R. (1962). Effects of limb disability on lousiness in mice. I. Preliminary studies. Exp. Parasitol. 12, 176-183. Bertin, R. I. (1986). Non-random fruit production in Campsis radicans: Between-year consistency and effects of prior pollination. Am. N a t . 126, 750-759. Bethel, W. M.. and Holmes, J . C. (1973). Altered evasive behavior and responses to light in amphipods harboring acanthocephalan cystacanths. J . Parasitol. 59, 945-956. Bethel, W. M., and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behavior induced by larval acanthocephalans. Can. J. Zoo/.55,110-1 15. Bezuidenhout, J. D., and Stutterheim, C. J. A. (1980). A critical evaluation ofthe role played by the red-billed oxpecker Euphagus erythrorhynchus in the biological control of ticks. Onderstepoorr J . Vet. Res. 47, 51-75. Bierzychudek, P. (1981). Pollinator limitation of plant reproductive effort. Am. Nut. 117, 838-840. Birkhead, T. R., and M@ller, A. P. (1992). “Sperm Competition in Birds: Evolutionary Causes and Consequences.” Academic Press, London.
PARASITES AND HOST SOCIAL BEHAVIOR
95
Birkhead. T. R.. Atkin, L.. and M@ller,A. P. (1987). Copulation behaviour of birds. Behnviour 101, 101-138. Bolles. R . C. (1960). Grooming behavior in the rat. J. Comp. Physiol. Psychol. 53,306-310. Borgia, G., and Collis, K. (1990). Parasites and bright plumage in the satin bowerbird (Ptilonorhyncus violaceus). Am. Zoo/. 30, 279-286. Boycott. J . A. (1971). "Natural History of Infectuous Disease." Edward Arnold. London. Brooke, M. de L. (1985). The effect of allopreening on tick burdens of molting eudyptid penguins. Auk 102,893-895. Brown. A. F., and Thompson. D. B. A. (1986). Parasite manipulation of host behaviour: Acanthocephalans and shrimps in the laboratory. J . B i d . Educ. 20, 121-127. Brown, C. R . (1984). Laying eggs in a neighbor's nest: Benefit and cost of colonial living in swallows. Science 224, 518-519. Brown, C. R.. and Brown, M . B. (1986). Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67, 1206- I2 18. Brown. N. S. (1972).The effect of host beak condition on the size of Menacanrhus stramineus populations of domestic chickens. Poult. Sci. 51, 162-164. Buchenuer, D., Luft. C.. and Grauvogl. A. (1982). Investigations on the eliminative behavior of piglets. Appl. Anim. Ethol. 9, 153-164. Bucher. E. H. (1988). Do birds use biological control against nest parasites? Parasitol. Today 4, 1-3.
Burdon, J. J . (1987). "Diseases and Plant Population Biology.'' Cambridge Univ. Press, Cam bridge. Burnet, M., and White, D. 0. (1972). "Natural History of Infectious Disease," 4th ed. Cambridge Univ. Press, Cambridge. Carney, W. P. (1969). Behavioural and morphological changes in carpenter ants harboring dicrocoeliid metacercariae. Am. Midl. Nat. 81-82, 605-61 I. Carpenter, C. C. (1966). The marine iguana of the Galapagos Islands, its behavior and ecology. Proc. Calif: Acad. Sci. 34, 329-376. Chapman, B. R.. and George. J. E. (1991). The effects of ectoparasites on cliff swallow growth and survival. I n "Bird-parasite Interactions: Ecology. Evolution. and Behaviour" (J. E. Loye and M. Zuk. eds.). pp, 328-343. Oxford Univ. Press, Oxford. Christian, J. J., and Davis, D. E. (1964). Endocrines, behavior, and population. Science 146, 1550-1560. Clark, L. (1991). The nest protection hypothesis: The adaptive use of plant secondary compounds by European starling. In "Bird-parasite Interactions: Ecology, Evolution, and Behaviour" (J. E. Loye and M. Zuk, eds.), pp. 205-221. Oxford Univ. Press, Oxford. Clark. L., and Mason, J. R. (1985). Use of nest material as insecticidal and antipathogenic agents by the European starling. Oecologia 67, 169-176. Clarke, B. C. (1979). The evolution ofgenetic diversity. Proc. R. Soc. London. Ser. B . 205, 45 3 -474. Clayton, D. H. (1991a). Coevolution of avian grooming and ectoparasite avoidance. I n "Birdparasite Interactions: Ecology, Evolution, and Behaviour" (J. E. Loye and M. Zuk, eds.), pp. 258-259. Oxford Univ. Press, Oxford. Clayton, D. H. (1991b). The influence of parasites on host sexual selection. Parasirol. Today 7, 329-334. Clayton, D. H. (1991b). The influence of parasites on host sexual selection. Parasitol. Today (in press).
%
ANDERS PAPE M0LLER ET AL.
Cornell, H. (1974). Parasitism and distributional gaps between allpatric species. Am. Nal. lOS, 880-883. Cox, F. E. G. (1982). “Modem Parasitology.” Blackwell, Oxford. Crompton, D. W. T. (1976). Entry into the host and site selection. I n “Ecological Aspects of Parasitology” (C. R. Kennedy, ed.), pp. 41-73. North-Holland Pub. Amsterdam. Darwin, C. (1862). “On the Various Contrivances by Which Orchids are Fertilized by Insects.” John Murray, London. Darwin, C. (1871). “The Descent of Man, and Selection in Relation to Sex.” John Murray, London. Day, P. R. (1974). “Genetics of Host-parasite Interaction.” Freeman, San Francisco. Dobson, A. P. (1988). The population biology of parasite-induced changes in host behavior. Q . Rev. Biol. 63, 139-165. Dritschilo, W., Cornell, H., Nafus, D., and O’Connor, B. (1975). Insular biogeography: Of mice and mites. Science 190,467-469. Duffy, D. C. (1983). The ecology of tick parasitism in densely nesting Peruvian seabirds. Ecology 64, 110-1 19. Duncan, P., and Vigne, N. (1979). The effect of group size in horses on the rate of attacks by blood-sucking flies. Anim. Behau. 27, 623-625. Eberhart, J. A,, Keverne, E. B., and Meller, R. E. (1983). Social influence on circulating levels of cortisol and prolactin in male talapoin monkeys. Physiol. Behau. 30,361-369. Elton, C. S. (1927). “Animal Ecology.” Sidgwick &Jackson, London. Emlen, J. T. (1986). Responses of breeding cliff swallow to nidicolous parasite infestations. Condor 88, 1 10-1 11. Emlen, S. T., and Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197,215-223. Feder, H. M. (1966). Cleaning symbioses in the marine environment. In “Symbioses ( S . M. Henry, ed.), Vol. I . pp. 327-380. Academic Press, New York. Feinsinger, P. (1983). Coevolution and pollination. I n “Coevolution” (D. J. Futuyma and M. Slatkin, eds.), pp. 282-310. Sinauer, Sunderland, MA. Fisher, G. W.. and Holton, C. S. (1957). “Biology and Control of the Smuts Fungi.” Ronald Press, New York. Folstad, I., and Karter, A. J. (1992). Parasites, bright males and the immunocompetence handicap. Am. Nar. l39,603-622. Folstad, I., Nilssen, A. C., Halvorsen, 0.. and Andersen, J. (1989). Why do male reindeer (Rangifer f . farandus) have higher abundance of second and third instar larvae of Hypoderma farandi than females? Oikos 55, 87-92. Freeland, W. J. (1976). Pathogens and the evolution ofprimate sociality. Biofropica 8,12-24. Freeland, W. J. (1977). Blood-sucking flies and primate polyspecies association. Nafure (London) 269,801-802. Freeland, W. J. (1979). Primate social groups as biological islands. Ecology 60, 719-728. Freeland, W. J. (1981a). Parasitism and behavioral dominance among male mice. Science 213,461-462. Freeland, W. J. (1981b). Functional aspects of primate grooming. Ohio J . Sci. 81, 173-177. Freeland, W. J. (1983). Parasites and the coexistence of animal host species. A m . N a f . l21, 223-236. Futuyma, D. J., and Slatkin, M., eds. (1983). “Coevolution.” Sinauer, Sunderland, MA. Galen. C. (1989). Measuring pollinator-mediated selection on morphometric floral traits: Bumblebees and the alpine sky pilot, Polemonium uiscosum. Evolution (Lawrence, Kans.) 43,882-890. Giles, N . (1983). Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an
PARASITES AND HOST SOCIAL BEHAVIOR
97
intermediate host, the three-spined stickleback, Gusrerosreus aculeatus. Anim. Behav. 31, 1192-1 194. Gladstone, D. E. (1979). Promiscuity in colonial monogamous birds. Am. Nar. 114,545-557. Gregory, R. D., and Keymer, A. E. (1989). The ecology of host-parasite interactions. Sci. Prog., (Oxford) 73, 67-80. Grossman, C. J. (1985). Interactions between the gonadal steriods and the immune system. Science 227,257-261. Hafner, M. S., and Nadler, S. A. (1988). Phylogenetic trees support the coevolution of parasites and their hosts. Nature (London) 332, 258-259. Haldane, J. B. S. (1949). Disease and evolution. Ric. Sci., Suppl. 19, 68-76. Halvorsen, 0. (1986). On the relationship between social status of host and risk of parasitic infection. Oikos 47, 71-74. Hamilton, W. D. (1971). Geometry of the selfish herd. J . Theor. Biol. 31, 295-311. Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282-290. Hamilton, W. D. (1990). Mate choice near and far. A m . Zool. 30, 341-352. Hamilton, W. D., and Zuk, M. (1982). Heritable true fitness and bright birds: A role for parasites? Science 218, 384-387. Hamilton, W. D., Axelrod, R., and Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites (a review). Proc. Nafl. Acad. Sci. U.S . A. 87, 3566-3573. Handel, S. N. (1983). Pollination ecology, plant population structure and gene flow. In “Pollination Biology” (L. Real, ed.), pp. 163-21 1. Academic Press, New York. Harper, J. L. (1977). “Population Biology of Plants.” Academic Press, London. Hamson, C. J. 0. (1965). Allopreening as agonistic behaviour. Behuviour 24, 161-208. Harrison. C. J. 0. (1985). Plumage, abnormal. In “A Dictionary of Birds” (B. Campbell and E. Lack, eds.), pp. 472-474. Poyser, Calton, U.K. Hart, B. L. (1985). “The Behavior of Domestic Animals.” Freeman, New York. Hart, B. L. (1990). Behavioral adaptations to pathogens and parasites: Five strategies. Neurosci. Biobehav. Rev. 14, 273-294. Hart, B. L., and Powell, K. (1990). Antibacterial properties of saliva: Role in maternal periparturient grooming and in licking wounds. Physiol. Behau. 48, 383-386. Hart, B. L., Korinek, E., and Brennan, P. (1987). Postcopulatory genital grooming in male rats: Prevention of sexually transmitted infections. Physiol. Behav. 41, 32 1-325. Hart, L. A., and Hart, B. L. (1988). Autogrooming and social grooming in impala. Ann. N . Y. Acad. Sci. 525, 399-402. Hanvood, R. F., and James, N. T. (1979). “Entomology in Human and Animal Health.” McMillan, New York. Hausfater, G., and Meade, B. J. (1982). Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. Primates 23, 287-297. Helle, T., and Aspi, J. (1983). Does herd formation reduce insect harassment among reindeer? A field experiment with animal traps. Acra Zool. Fenn. 175, 129-131. Hindsbo, 0. (1972). Effects of Polymorphus (Acanthocephala) on colou and behaviour of Gammarus lacustris. Nature (London) 238, 333. Hindsbo, 0. (1989). Field observation on the behaviour of Succinea and Leucochloridium. Proc. Scand. Symp. Parasirol. Inform. 14th 20, 89. Inst. Parasitol. Abo Akademi, Finland. Holmes, J. C. (1982). Impact of infectuous disease agents on population growth and geographical distribution of animals. In “Population Biology of Infectious Diseases” (R. M. Anderson and R. M. May, eds.), pp. 449-455. Springer, Berlin. Holt, R. D., and Pickering, J. (1985). Infectious diseases and species coexistence: A model of Lotka-Volterra form. Am. Nat. 126, 196-211.
98
ANDERS PAPE M0LLER ET AL.
Hoogland, J. L. (1979). Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys spp.) coloniality. Behavioitr 69, 1-35. Hoogland, J . L., and Sherman, P. W. (1976). Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecol. Monogr. 46, 33-58. Howard, R. D.. and Minchella, D. J. (1990). Parasitism and mate competition. Oikos 58, 120- 122. Hudson, P. J. (1986). The effect of a parasitic nematode on the breeding production of red grouse. J. Anim. Ecol. 55, 85-92. Hudson, P. J., Dobson, A. P., and Newborn, D. (1985). Cyclic and non-cyclic populations of red grouse: A role for parasitism? I n “Ecology and Genetics of Host-parasite Interactions” (D. Rollinson and R. M. Anderson, eds.). pp. 77-89. Academic Press, London. Jablonska, J. (1986). Specificity of some mite species of the superfamily Analgesoideu t o bird hosts in Warsaw Zoo. Acra Parasirol. Pol. 31, 55-62. Jaenike, J. (1978). An hypothesis to account for the maintenance of sex within populations. Evol. Theory 3, 191-194. Janzen, D. H. (1968). Host plants in evolutionary and contemporary time. A m . Nat. 102, 592-595. Janzen, D. H. (1973). Host plants as islands. 11. Competition in evolutionary and contemporary time. Am. Nar. 107, 786-790. Jennersten, 0. (1985). “Pollination and fungal disease transmission: Interactions between Viscaria vulgaris, Ustilago and insects. Acra Univ. Ups. 793, 1-30. Jennersten, 0.(1988). Insect dispersal of fungal disease: Effects of Ustilago uiolucea on pollinator attraction in Viscaria vulgaris. Oikos 51, 163-170. Jennersten, 0.. Nilsson. S. G., and Wastljung, U. (1983). Local plant populations as ecological islands: The infection of Viscaria vulgaris by the fungus Ustilugo violacea. Oikos 41, 391-395. Kennedy, C. R. (1975). “Ecological Animal Parasitology.” Wiley, New York. Kennedy, C. R., ed. (1976). “Ecological aspects of Parasitology.” North-Holland Publ.. Amsterdam. Keverne, E. B. (1986). Neuroendocrine consequences of social status in talapoin monkeys. Primate Rep. 14, 35. Keymer. A., and Read, A. (1989). Behavioural ecology: The impact of parasitism. I n “Parasitism: Coexistence or Conflict?” (C. A. Toft and A. Aeschlimann, eds.). pp. 37-61. Oxford Univ. Press, New York. Kuris, A. M., Blaustein, A. R., and A M , J. J. (1980). Hosts as islands. A m . Nor. 116. 570-586. Lack, D. (1954). “The Natural Regulation of Animal Numbers.” Oxford Univ. Pres: (Clarendon), London. Lack, D. (1968). “Ecological Adaptations for Breeding in Birds.” Methuen, London. Lanciani, C. A. (1975). Parasite induced alteration in host reproduction and survival. Ecolog) 56,689-695. Lester, R. J. G. (1971). The influence of Schisrocephalus plerocercoids on the respiration of Gnsrerosreus and a possible resulting effect on the behavior of the fish. Can. J. Zoo/. 49, 361-366. Lewis, J. W. (1981). On the coevolution of pathogen and host. J . Theor. Eiol. 93,927-985. Loomis. E. C. (1978). External parasites. In “Diseases of Poultry” (M. S . Hofstad, B. W. Calnek, C. F. Helmboldt, W. M. Reid, and H. W. Yoder, Jr., eds.), pp. 667-704. Iowa State Univ. Press, Ames. Loye, J. E., and Carroll, S. P. (1991). Nest ectoparasite abundance and cliff swallow colony site selection, nestling development, and departure time. I n “Bird-parasite Interactions:
PARASITES A N D HOST SOCIAL BEHAVIOR
99
Ecology, Evolution, and Behaviour” (J. E. Loye and M. Zuk. eds.). pp. 222-241. Oxford Univ. Press, Oxford. Lozano. G. A. (1991). Optimal foraging theory: A possible role for parasites. Oikos 60, 39 1-395. Marshall, A. G. (1981). “The Ecology of Ectoparasitic Insects.” Academic Press, London. Marshall, D. L., and Ellstrand, N. C. (1986). Sexual selection in Raphunus sufivus: Experimental data on non-random fertilization, maternal choice, and consequences of multiple paternity. Am. N u t . 127, 446-461. Masataka, N., Ishida, T., Suzuki, J., Matsumura. S., Udono, S., and Sasaoka, S. (1990). Dominance and immunity in chimpanzees (Pan troglodytes). Ethology 85, 147-155. Mattingly, P F. (1969). “The Biology of Mosquito-borne Disease.” Allen & Unwin. London. McFarland, C. G., and Reeder. W. G. (1974). Cleaning symbiosis involving Galapagos tortoises and two species of Darwin’s finches. Z. Tierpsychol. 34, 464-483. McGladdery, S. E. (1984). Behavioural responses of Trichostrongylus tenuis (Cobbold) larvae in relation to their transmission to the red grouse, Lagopus I. scoricus. J . Helmintho/. 58, 295-299. Mckinney, F., Cheng, K. M., and Bruggers, D. J. (1984). Sperm competition in apparently monogamous birds. In “Sperm Competition and the Evolution of Animal Mating Systems” (R. L. Smith, ed.). pp. 523-545. Academic Press. Orlando, FL. Michel, J. F. (1955). Parasitological significance of bovine grazing behaviour. Nature (London) 175, 1088-1089. Minchella, D. J., and Scott, M. E. (1991). Parasitism: A cryptic detreminant of animal community structure. Trends Ecol. Evol. 6 , 250-254. Minchella, D. J.. and Scott. M. E. (1991). Parasitism: A cryptic detreminant of animal community structure. Trends Ecol. Evol. 6, 250-254. Mbller, A. P. (1987). Advantages and disadvantages of coloniality in the swallow, Hirundo rustica. Anim. Behav. 35, 819-832. Mbller, A. P. (1990). Parasites and sexual selection: Current status.of the Hamilton and Zuk hypothesis. J . Evol. B i d . 3, 319-328. Mgller, A. P. (1991). Parasites, sexual ornaments and mate choice in the barn swallow Hirundo rustica. I n “Bird-parasite Interactions: Ecology, Evolution, and Behaviour” ( J . E. Loye and M. Zuk, eds.), pp. 328-343. Oxford Univ. Press, Oxford. Mbller, A. P., and Birkhead. T. R. (1989). Copulation behaviour in mammals: Evidence that sperm competition is widespread. Biol. J . Linn. SOC.38, 119-131. Mbller, A. P., Allander, K., and Dufva, R. (1990). Fitness effects of parasites on passerine birds: A review. In “Population Biology of Passerine Birds: An Integrated Approach” ( J . Blondel, A. Gosler, J.-D. Lebreton, and R. McCleery, eds.), pp. 269-280. Springer, Berlin. Moore, J. (1983). Responses of an avian predator and its isopod prey to an acanthocephalan parasite. Ecology 64, 1000-1015. Moore, J. (1984a). Altered behavioral responses in intermediate hosts-an acanthocephalan parasite strategy. Am. Nut. U3, 572-577. Moore, J. (198413). Parasites that change the behavior of their host. Sci. Am. 250, 82-89. Moore, J., Simberloff, D., and Freehling. M. (1988). Relationships between bobwhite quail social-group size and intestinal helminth parasitism. Am. Nar. 131, 22-32. Morse, D. H. (1980). “Behavioral Mechanisms in Ecology.” Harvard Univ. Press, Cambridge, MA. Moss, W. W., and Camin, J. H. (1970). Nest parasitism, productivity, and clutch size in purple martins. Science 168, 1000-1003.
100
ANDERS PAPE MaLLER ET AL.
Muirhead-Thomson, R. C. (1968).“Ecology of Insect Vector Populations.” Academic Press, London and New York. Mulcahy, D. M. (1971). Correlation between gametophytic and sporophytic characteristics in Zea mays L. Science 171, 1155-1 156. Murray, B. G., Jr. (1971). The ecological consequences of interspecific territorial behavior in birds. Ecology 52,414-423. Murray, M. D. (1987). Effects of host grooming on louse populations. Parasitol. Today 3, 176- 178. Murray, M. D. (1990). Influence of host behaviour on some ectoparasites of birds and mammals. In “Parasitism and Host Behaviour” (C. J. Barnard and Behnke, eds.), pp. 290-315. Taylor & Francis, London. Newton, P. (1991). The use of medical plants by primates: A missing link? Trends Ecol. Euol. 6,297-299. Noble, E. R., and Noble, G. A. (1976). “Parasitology,” 4th ed. Lea & Febiger, Philadelphia. Noble, E. R., Noble, G. A., Schad, G. A., and MacInnes, A. J. (1989). “Parasitology: The Biology of Animal Parasites.” Lea & Febiger, Philadelphia. Odberg, F. O., and Francis-Smith, K. (1977). Studies on the formation of ungrazed eliminative areas in fields used by horses. Appl. Anirn. Erhol. 3, 27-34. Page, L. A., ed. (1976). “Wildlife diseases.” Plenum, New York. Park, T. (1948). Experimental studies of interspecific competition. I. Competition between populations of the flour beetles Tribolium confusum Duval and Tribolium castaneum Herbst. Ecol. Monogr. 18, 267-307. Parker, G. A. (1970). Sperm competition and its evolutionary consequences in the insects. Biol. Rev. Cambridge Philos. SOC.45, 525-567. Petrie, M., and M@ller,A. P. (1991). Laying eggs in others’ nests: lntraspecific brood parasitism in birds. Trends Ecol. Euol. 6, 315-320. Poulin, R. (1991a).Group-living and the richness of the parasite fauna in Canadian freshwater fishes. Oecologia 86, 390-394. Poulin, R. (1991b). Group-living and infestation by ectoparasites in passerines. Cordor 93, 4 18-423. Poulin, R., and FitzGerald, G. J. (1989). Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasrerosreus spp.). Behav. Ecol. Sociobiol. 24, 25 1-255. Price, P. W. (1980). “Evolutionary Biology of Parasites.” Princeton Univ. Press, Princeton, NJ. Price, P. W., Westoby, M., Rice, B., Atsatt, P. R., Fritz, R. S., Thompson, J. N., and Mobley, K. (1986). Parasitemediation in ecological interaction. Annu. Rev. Ecol. Sysr. 17,487-505. Price, P. W . , Westoby, M., and Rice, B. (1988). Parasite-mediated competition: Some predictions and tests. Am. Nar. 131, 544-555. Pulliam, H. R., and Caraco. T. (1984). Living in groups: Is there an optimal group size? In “Behavioural Ecology: An Evolutionary Approach” ( J . R. Krebs and N. B. Davies, eds.), 2nd ed., pp. 122-147. Blackwell, Oxford. Queller, D. C. (1983). Sexual selection in a hermaphoditic plant. Nature (London) 305, 153-172. Rankin, G . D. (1982). Mallophaga on the eggs of wading birds. Ibis W, 183-187. Rau, M. E. (1983). Establishment and maintenance of behavioral dominance in male mice infected with Trichinella spiralis. Parasitology 86, 319-322. Rau, M. E. (1984). Loss of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology 88, 311-373. Read, A. F. (1988). Sexual selection and the role of parasites. Trends Ecol. Euol. 3,97-102. Read, A. F. (1990). Parasites and the evolution of host sexual behaviour. In “Parasitism and
PARASITES AND HOST SOCIAL BEHAVIOR
101
Host Behaviour” (C. J. Barnard and J. M. Behnke, eds.), pp. 117-157. Taylor& Francis, London. Rohwer, S. (1977). Status signalling in Harris sparrows: Some experiments in deception. Behaviour 61, 107-129. Rollinson, D., and Anderson, R. M., eds. (1985). “Ecology and genetics of Host-parasite Interactions.” Academic Press, London. Rubenstein, D. I . , and Hohmann, M. E. (1989). Parasites and social behavior of island feral horses. Oikos 55, 312-320. Rutberg, A. T. (1987). Horse fly harassment and the social behavior of feral ponies. Ethology 75, 145-154. Seyfarth, R. M. (1983). Grooming and social competition in primates. I n “Primate Social Relationships: An Integrated Approach” (R. A. Hinde, ed.). pp. 182-190. Blackwell, Oxford. Shields, W. M.. and Crook, J. R. (1987). Barn swallow coloniality: A net cost for group breeding in the Adirondacks? Ecology 68, 1373- 1386. Simmons, K . E. L. (1966). Anting and the problem of self-stimulation. J. Zool. 149, 145-162. Simmons, K. E. L. (1985). Comfort behaviour. In “A Dictionary of Birds” (B. Campbell and E. Lack, eds.), pp. 101-105. Poyser, Calton, U.K. Smith, R . L., ed. (1984). “Sperm Competition and the Evolution of Animal Mating Systems.” Academic Press, Orlando, FL. Snow, A. A.. and Spira, T. P. (1991). Pollen vigour and the potential for sexual selection in plants. Nature (London) 352, 796-797. Snowball, G. J. (1956). The effect of self licking on cattle tick Boophilus microplus (Canestrini). Aust. J . Agric. Res. 7 , 227-232. Stanton, M. L., Snow. A. A., and Handel, S. N. (1986). Floral evolution: Attractiveness to pollinators influences male and female fitness in plants. Science 232, 1625-1627. Stephenson, A. G. (1981). Flower and fruit abortion: Proximate causes and ultimate functions. Annu. Rev. Ecol. Syst. U ,263-279. Stephenson, A. G., and Bertin, R. I. (1983). Male competition, female choice, and sexual selection in plants. I n “Pollination Biology” (L. Real, ed.), pp. 109-149. Academic Press, New York. Sutherst, R. W., Floyd, R. B., Bourne, A. S., and Daltwitz, M. J. (1986). Cattle grazing behaviour regulates tick populations. Experientia 42, 194-196. Swingland I . R., and Greenwood, P. J., eds. (1983). “The Ecology of Animal Movement.” Oxford Univ. Press (Clarendon), London. Takasaki, H.. and Hunt, K. (1987). Further medicinal plant consumption in wild chimpanzees. Afr. Stud. Monogr. 8, 125-128. van Noordwijk, A. J., van Balen, J. H., and Scharloo, W. (1981). Genetic variation in the timing of reproduction in the great tit. Oecologia 49, 158-166. Wakelin, D.. and Blackwell, J. M., eds. (1988). “Genetics of Resistance to Bacterial and Parasitic Infection.” Taylor & Francis, London. Waser, N. M., and Price, M. V. (1981). Pollinator choice and stabilizing selection for flower color in Delphinium nelsonii. Evolution (Lawrence, Kans.) 35, 376-390. Watt, J. M . , and Breyer-Brandwijk, M. G. (1962). “The Medicinal and Poisonous Plants of Southern and Eastern Africa,” 2nd ed. Livingstone, Edinburgh. Whatson, T. S. (1985). Development of eliminative behavior in piglets. Appl. Anim. Eehav. Sci. 14, 365-377. Wilkinson, G . S. (1986). Social grooming in the common vampire bat, Desmodus rotundus. Anim, Behau. 34, 1880-1889. Willson, M. F., and Burley, N. (1983). “Mate Choice in Plants.” Princeton Univ. Press, Princeton, NJ.
102
ANDERS PAPE MBLLER ET AL.
Willson, M. F., and Price, P. W. (1977). The evolution of inflorescence size in Asclepias (Asclepiadaceae). Evolution (Lawrence, Kans.) 31, 495-5 1 I . Wilson, E. 0 .(1975).“Sociobiology: The New Synthesis.” Harvard Univ. Press, Cambridge, MA. Wimberger. P. H. (1984).The use ofgreen plant material in bird nests to avoid ectoparasites. Auk 101, 615-618. Wingfield, J.. Hegner. R. E., Dufty, A. M., Jr., and Ball, G . F. (1990). The “challenge hypothesis”: Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nar. 136, 829-846. Wittenberger, J. F., and Hunt, G . L. (1985). The adaptive significance of coloniality in birds. Avian B i d . 8, 1-78. Yom-Tov, Y. (1980). lntraspecific nest parasitism in birds. B i d . Rev. Cambridge Philos. SOC. 55.93-108. Zuk,M. (1991). The role of parasites in sexual selection: Current evidence and future directions. Adu. Srudy Behau. 21, 39-68.
ADVANCES IN THE STUDY OF BEHAVIOR. VOL. ??
The Evolution of Behavioral Phenotypes: Lessons Learned from Divergent Spider Populations SUSANE. RIECHERT DEPARTMENT OF ZOOLOGY UNIVERSITY OF TENNESSEE KNOXVILLE. TENNESSEE 37996
I.
INTRODUCTION
The extent to which the behavior of a species changes from one local environment to another is an area of current ecological and evolutionary theory for which the spider Agelenopsis aperta (Agelenidae) has made an excellent test subject. Turesson (1922) referred to genetic differences in traits between populations of the same species as ecotypic variation. Although most studies of ecotypic variation have dealt with morphological and physiological characteristics (e.g., body color, the timing of reproduction, and temperature tolerances), it has been argued that, in animal evolution, behavior tends to change before morphology (e.g., von Wahlert, 1965; Krebs and Davies, 1981).Mayr (1963)states that for animals “a shift into a new niche or adaptive zone is almost without exception initiated by a change in behavior.” Many workers feel that it is behavior that sets the tempo of evolution, rather than the morphological traits that are most often the subject of evolutionary studies. The study of ecotypic variation in behavior is important because it can provide insight into how evolution by natural selection works as well as how it might be compromised by various phenomena. Most behavioral and ecological models assume that the organisms under investigation are in a steady or equilibrium state-that each population is “well adapted” to its environment. Both hypotheses about the system and the development of models of it are based on this assumption, but it is one which may be incorrect for a variety of reasons (e.g., recent change in the local environment, phylogenetic inertia [design limitations], gene flow [interbreeding among local population~]).Study of ecotypic variation in several fitness-linked behavioral traits of Agelenopsis aperta has led me to investiI03 Copyright 0 1993 by Academic Press. Inc. All rights of reproduction in any form reserved.
104
SUSAN E. RlECHERT
gate various explanations for failure of populations to reach adaptive equilibria with respect to their local environments. This review describes the spider system and the insight it has provided into both the underlying genetic bases of complex behavioral traits and evolutionary processes.
11. THE SPIDERSYSTEM
Agelenopsis aperta (Gertsch is a western representative of the “grass” spider genus (family Agelenidae) found throughout North America. It is an annual species (one generationlyear) that builds a flat horizontal “sheet web” with a vertical silk scaffolding which serves to interrupt the flight of insects, causing them to fall onto the sheet. The web is further characterized by the presence of a silk funnel which extends into some feature of the substrate (e.g., leaf litter, cracks in the ground, under rocks). It is nonsticky, merely serving as a detection device for the spider, which sits in wait of prey within the protected environment of the funnel. Agelenopsis aperta occupies a wide range of habitats from northern Wyoming to southern Mexico and from California to Central Texas. My work has centered on two populations located in the south-central part of this range: one inhabiting a desert grassland area in south-central New Mexico (NM), and the other a riparian area in southeastern Arizona (AZ).
A. DESERT GRASSLAND (NEW MEXICO) Daily temperature extremes and strong winds are characteristic of the desert grassland study area in Lincoln County, NM. Here prey availability is low, causing the spiders to be food-limited (Table I; Riechert, 1978a, 1981). Also, because A . aperta is a small ectotherm and its body temperature is strongly influenced by localized air and surface temperatures, by the degree of solar radiation, and by local wind velocities, most individuals in the grassland habitat have only a few hours a day in which to engage in prey capture activities. Furthermore, the length of time for which individuals can forage varies greatly with the microhabitat in which their web sites are located (Fig. 1; Riechert and Tracy, 1975). Prey availability also varies greatly with microhabitat type in the grassland habitat. The microhabitats that provide the better thermal environments to A . aperta also seem to have the highest insect densities (Riechert and Tracy, 1975). In this spider species, reproductive success can be equated with the quantities of food consumed. The more prey that are consumed the more offspring are produced by female A. uperta, but only
105
EVOLUTION OF BEHAVIORAL PHENOTYPES
TABLE I COMPARISON OF INSECT AVAILABILITIES TO Agelenopsis aperra
Prey availability (mg dry weight/ trap/day )
NM A2 TX
Mean
SE
24.9 106.5 115.7
5.5
1.1
14.8
AT
THREELOCALITIES"
Proportion of days optimal energy needs met (>20 mg dry weight) Between year variability Cumulative trap days
Mean (No. years)
CVh (%)
S E (%)
.35 .85 .80
.28(6) .87(5) .89(4)
91.5 9.3 21.2
21.9 0.8 7.6
NM. Desert grassland; AZ, riparian; and TX, riparian. Only prey encountering sticky traps and between 4 and 25 mm in body length (capture range of mature A. aperra) were included in the analyses. CV, Coefficient of variation computed on arcsine transformed data.
to a limit (Fig. 2a). Beyond this limit, rather than producing additional eggs, A. aperfa incorporates greater quantities of yolk in its eggs (Fig. 2b; Riechert and Tracy, 1975). Because the yolk is what the newly hatched spiderlings subsist on until they are able to obtain their first insect meal, I assume that the quantities of yolk a female is able to provide for her offspring affects offspring survival. Recent work by Fred Singer and myself on male reproductive success indicates that the body mass that A. upertu males are able to achieve as a result of their feeding history is a significant determinant of mating success as well. Males collected at those web sites that afford higher levels of prey weigh far more than males collected from lower quality microhabitats (Fig. 3). At maturity, males give up their sites and search for matings. We have found that the distances males can travel is a function of their body masses (Fig. 4a) and that mating success is also correlated with body mass (Fig. 4b). Note that, as is the case for most spider species, male A. uperta are smaller on average than females and small males not only are frequently chased off the webs by large females but may be killed during courtship as well. (Why are males smaller than females? Females need a larger frame to accommodate egg masses, while we have some evidence that there is a reproductive advantage for males to mature earlier and hence at a smaller body size than females [S. E. Riechert and F. D. Singer, unpublished data]). Active habitat discrimination is evidenced for members of this population (Riechert, 1985),with a preference shown for those few sites (3% of the
106
SUSAN E. RIECHERT
a
Surface 60.0
-
Shade
Sun
-@-
-----
upper lower
C
10.0
0
'
'
'
*
'
'
. .
1000
I
.
2000
Time
60.0 r 50.0 -
0
1000
Time
2000
'
EVOLUTION OF BEHAVIORAL PHENOTYPES
I07
available habitat cover) that afford the foraging time and prey availabilities requisite to survival and reproduction by females in most years (Fig. 5 ; Riechert, 1979, 1981). The high-quality sites in the grassland habitat are holes or depressions that are formed by the scouring effect heavy summer rains have in the area (Riechert, 1976). These protected sites provide the spiders with shade and often have accumulated litter which decreases the thermal radiation a spider receives. There is also less wind damage to webs that are built in these depressions than occurs on the grassland surface itself. The spiders do not cue in on the depressions because of their structural characteristics. Rather, they actively seek shade and, when in shade, move along temperature gradients to settle at their preferred body temperature of 30°C (Riechert, 1985).Agelenopsis aperta also responds to both olfactory and vibratory cues emitted by insects in locating its web sites in the vicinity of such insect attractants as flowering herbs and fecal material (Riechert, 1976, 1985). Thus, individual success in the NM grassland habitat is highly dependent on a spider’s ability to locate a web site in a microhabitat that provides it with sufficient insect prey to survive to reproduction. This population is food limited and the availability of adequate sites is a major selection pressure on individuals. Unlike the AZ riparian population described below, the grassland population receives no measurable predation pressure from foraging birds, the major visual predators on this spider species (Riechert and Hedrick, 1990). B. RIPARIAN(ARIZONA) The second population occupies a riparian (woodland) area in southeastern Arizona. This is characterized by a tree canopy, a grass and leaf litter forest floor, and the presence of a permament, spring-fed stream which serves as an insect reservoir. Prey are thus present in abundant supply (Table I ) and 89% of the habitat cover is appropriate to ensure spider survival to reproduction (Riechert, 1979). Interestingly, the 11% of the
FIG. I . Predicted Agelenopsis aperra body temperatures for the course of a clear day in mid June at (a) a surface site (poor quality) versus (b) a depression site (high quality) in the NM grassland habitat. Two curves reflect spider temperature in full sun and full shade, respectively. Actual spider temperature when out on the web will fall somewhere between these two curves depending on how much sunlight the individual is exposed to. (Note that, in actuality, little shade is available at surface sites.) Spider foraging is permitted only when body temperature falls between the upper and lower temperatures of its activity range, the area demarcated in the figure by the dashed lines. (Data from Riechert and Tracy, 1975.)
SUSAN E. RIECHERT
108
-
900-
a
I-
$
-
000-
t
700-
W
W
E 600-
V
3
a
n
500-
u)
W
s2
400-
300-
CORRELATION COEF F I C I EN T
II J
SIGN. AT P=
A
g
,.877
200-
A
4
100-
01
,
I
I
l
l
l
l
l
l
l
l
I
l
l
I
I
I
I
I
l
l
500 -
a
W
v 400-
a
FIG. 2. Regressions fitted to milligrams (a) and numbers (b) of eggs produced by adult female Agelenopsis upertu as a function of feeding history from penultimate instar to death. Correlation coefficients are product-moment. (From Riechert and Tracy, 1975).
109
EVOLUTION OF BEHAVIORAL PHENOTYPES
microhabitat cover present in the area that does not permit spider survival to reproduction does provide adequate shelter from thermal extremes and abundant prey (rock substrates). However, association with rocks in this habitat places individual spiders in jeopardy of being washed downstream during rains since this substrate type is located along the streambank that traverses the riparian habitat. Members of the riparian population utilize the same habitat cues as the grassland population in locating their web sites, though laboratory-reared AZ riparian individuals show significantly greater variability in their responses to habitat-related cues (i.e., thermal, olfactory, and vibratory)
...
. .
0 POOR'89
0 POOR'90
01 0
'
'
'
.
5
. . .
'
10
' ' . .
'
15
OBSERVATIONS RANKED BY WEIGHT
FIG.3. Relationship between the quality of a site a male A g e h o p s i s aperta occupies and its weight at capture as a juvenile for two different years. Poor sites are grassland surface with no insect attractants; excellent sites are depressions with insect attractants. Dashed lines, region of overlap between excellent and poor quality site weight scores (Note that 74% of the males collected at excellent quality sites weigh more than the heaviest male collected at a poor quality site.)
110
SUSAN E. RIECHERT
y--.m+.mr1.542
a
31 k tP
1-
E
c,
E C
I
-1
1
.
*:
1
-c '
100
0
200
300
male weight (mg) y = -0.024 + ,015~ r
b
: I -
.
v)
C
,506
.
01
. I
-
4
c,
E" 0
t
a
E a
E - 1 '
0
.
.
50
-
100
.
-
150
.
'
200
.
'
250
male weight (mg) FIG.4. Relationship between body mass and two aspects of male reproductive success: (a) distance moved by adult males in search of females (activity chamber estimates), and (b) number of matings achieved when successive females are offered at 3-day intervals in a laboratory context.
EVOLUTION OF BEHAVIORAL PHENOTYPES
111
than do grassland spiders reared under the same conditions (Riechert, 1985). Given a choice of substrates upon which to build webs, however, I found that this spider does avoid rocks, favoring leaf litter and the bases of shrubs as web-building sites (Riechert, 1979).
100
SITE QUALITY
W Poor
0 Average 80
W Excellent
60
40
20
0 Mild Typical Harsh ENVIRONMENTAL CONDITIONS
FIG.5 . Relative contribution (percentage of offspring) contributed to gene pool by spiders occupying different quality territories under varying environmental conditions in NM grassland habitat (mild, typical, and harsh years). Typical years have winter and summer rains only, and a clear, hot, and dry May-July coinciding with maturation of Agehopsis aperta; mild have late spring precipitation and cloud cover; harsh have little winter percipitation leading to an exceptionally hot and dry May-July. Data presented represent reproductive success/individual summed for all individuals occupying sites of the given quality. Note that since there are more average quality sites than excellent quality sites in some years, more offspring are contributed by spiders occupying average sites than excellent sites even though spiders at exellent quality sites produce more offspring/individual. (From Riechert, I981 .)
112
SUSAN E. RIECHERT
Bird predation is an important selection pressure on A . aperta in the riparian habitat. Several species of hummingbird (Trochilidae), American robins (Turdus migrutorius), grey-breasted jays (Aphelocoma ultramarina), rufous-sided towhees (Pipilo erythrophthalmus), white-breasted nuthatches (Sita carolinensis), and yellow-eyed juncos (Junco phueonotus) are all ground and low shrub foragers on arthropods in this habitat. In an experimental study of potential bird predation on A . aperta in this habitat, Riechert and Hedrick (1990) observed differential losses of spiders at sites exposed to predation over those protected by bird netting of 30.4% per week during the bird nesting season in one year and of 50.8% in another year. Of course, there was considerable temporal and spatial variation around these mean differential loss values, associated probably with the location of the experimental units relative to nesting birds in the study area. In summary, A . aperta is basically an arid-lands species that is subject to two major selection pressures: food limitation and risk of predation. The degree to which food versus predation is limiting to each of the main populations under study differs markedly, with the grassland population being food-limited and the riparian population under strong predation pressure by birds. 111. FITNESS-LINKED BEHAVIORAL TRAITS Turreson (1922) based his definitionof ecotypic variation on the observation that the traits that adapt different populations to local conditions have underlying genetic bases. He found that, when he grew seeds from divergent plant populations of a given species in a common environment, the divergent growth forms of the parent plants in nature were still manifest in the offspring. I have investigated several fitness-linked behavioral traits in the A . aperta system. Included are those that involve competition for food (contest behavior and territory size), foraging behavior itself, and response to predatory cues. For each of these traits, I have considered the ecological and evolutionary significance(fitness consequences) as well as determined relative experiential versus genetic influences. A. TERRITORIAL BEHAVIOR
Although food levels and the quantity of suitable habitat available differ markedly between the NM desert grassland and AZ riparian habitats, levels of competition for sites that offer high prey availabilities might not differ that much between the two populations if individuals in the grassland
EVOLUTION OF BEHAVIORAL PHENOTYPES
113
habitat could aggregate in local areas of high prey abundance. Such aggregations are not observed because A. aperta exhibits energy-based territorial behavior (Riechert, 1978a). Territoriality involves the defense of space. Thus, it may have two fitness-linked components: territory size and agonistic behavior. Agelenopsis aperta from both the NM grassland and AZ riparian populations defend space in excess of the web against intrusion by other members of the same species population. Territories are maintained throughout the lives of the females and until maturity in males. Territory size is adjusted to lows in prey availability rather than the mean prey availability encountered in a given habitat (Riechert, 1981). The holders of territories at highquality sites are thus assured of sufficient food to reproduce (Riechert, 198 1). NM grassland spiders generally saturate available high-quality sites in that habitat. Experimental removal of territory owners indicates that about 30% of the desert grassland population, at any given time, is floating without territories). There are high costs to floating in the desert grassland system, since individuals lose approximately 8% of their body weight per day while floating and will suffer mortality when this loss accumulates to approximately 25% (Riechert, 1981). On the other hand, AZ riparian spider numbers remain well below carrying capacity (48% saturation; Riechert, 1981). Because suitable web sites are abundant in the riparian habitat but scarce in the grassland habitat, between-population differences exist in territorial behavior: (a) grassland spiders maintain larger territories than riparian spiders (Table 11); (b) grassland spiders show higher levels of escalation and greater persistence in territorial disputes than riparian spiders (Riechert, 1979)( Table 111). These population differences in territory size and agonistic behavior have genetic bases (Maynard Smith and Riechert, 1984; Riechert and Maynard Smith, 1989). Hence, ecotypic variation is exhibited in A. aperta territorial behavior.
B. FORAGING BEHAVIOR Between-population differences in levels of prey available lead to the prediction that riparian A. aperta will include fewer prey types in their diets than grassland A. aperta. The hypothesis is based on the general prediction that, as high-ranking food types increase in abundance, lower ranked types should be dropped from the diet (Pyke, 1984). In this particular case, it follows from the fact that grassland individuals need to maximize their caloric intake while riparian individuals need to minimize their exposure to avian predators during foraging. Thus, grassland animals should take all prey that are encountered that will provide a positive energy
114
SUSAN E. RIECHERT
TABLE I1 RESULTSOF TERRITORY SIZEEXPERIMENTS FOR THREE POPULATIONS OF Agelenopsis aperta Nearest neighbor distance (CM) Feral individuals
Lab-reared individuals
Location of Population
n
Mean
SE
II
Mean
SE
NM grassland AZ riparian TX riparian
13
130.5 53.6
18.5"
24 2s
87 31
133.6 51.4 6.6
6.Zb
1.1"
2. I
21
6.4b 3.4
Data from Riechert (1981). Data from Riechert and Maynard Smith (1989).
gain, whereas riparian individuals should limit capture attempts to prey types that can be captured most quickly (i.e., provide least exposure to predation risk). (Note that the fact that risk of predation may increase with the time a spider is out on the web in a capture attempt will only further skew riparian spider behavior toward attacking prey that can be captured more quickly.) Figure 6 shows the attack rates NM grassland and AZ riparian spiders exhibit toward the major categories of prey encountered. The prey types are ranked by profitability, which is an index of the benefit received from consuming the prey divided by the cost required to procure it. There are distinct differences between the populations, with the NM grassland spiders overall exhibiting a higher capture attempt rate toward
TABLE 111 COMPARISON OF N M GRASSLAND VERSUS AZ RIPARIAN SPIDERBEHAVIOR I N TERRITORIAL DISPUTES (WITHIN-POPULATION CONTESTS)" Contest statistics (means) Estimated cost Context
NM grassland
AZ riparian
Number of bouts NM grassland
AZ riparian ~______
Owner heavier Equal weight Intruder heavier
483.7 556.7 1,012.5
160.4 215.4 145.5
2.9
2.0
3.1 4.0
2. I
2.1
a The contest cost estimate was derived by summing across all behavior patterns the escalation ranking of an act type (1-35) times its duration (seconds) in a given contest. Number of bouts refers to interactions between opponents separated by a retreat by one of the opponents off the web. Threshold for weight bias is 10%.
115
EVOLUTION OF BEHAVIORAL PHENOTYPES
prey than the AZ riparian spiders. Riparian spiders failed to exhibit the diet specialization predicted. The completion of laboratory rearings of the two populations of A. upertu suggest that the different attack rates toward the broad spectrum of prey is due to different inherent latencies to attack (Hedrick and Riechert, 1989). That is, riparian spiders take an order of W RIPARIAN
0
PREY TYPES
F 0:
P Y W
W
a
3
t
U 0
??
2 U J W
0"0 v)
F
t d
m 4
t Y
Bn
GRASSLAND
SM WASPS 0.t 'PREDACEOUS BEETLES 0.1 SPIDERS 0.2 'ANTS 0.2 4 M M BEETLES 0.2 SM HOPPERS 0.2 PLANT BEETLES 0.3 PLANT BUGS 0.3 'BEES 0.4 CRICKETS 0.6 PREDACEOUS BUGS 0.6 'MANTIDS 0.7 SM FLIES 0.8 medlan SOFT BEETLES 0.9 GRASSHOPPERS 1.2 LARVAE 1.8 BUlTERFLIES 2.4 LG FLIES 2 9 'LG WASPS 3.7 ROBBER FLIES 4.8 LACE WINGS 5.9 LARGE HOPPERS 5.9
MOTHS 8.3 WALKING STICKS 10.0 DAMSELFLIES 25.0 0.0
0.2
0.4
0.6
0.8
1.0
1.2
CAPTURE ATTEMPT RATE
FIG.6. Potential prey of Agelenopsis upertu ranked in order of increasing profitability (joules gainedkecond capture time; score to right of taxon). Bars represent capture attempt rates for AZ riparian and NM grassland spiders. *, Prey types observed to cause injury to A. aperta.
SUSAN E. RIECHERT
116
magnitude longer to respond to a prey item than do grassland spiders (Table IV).
C. ANTI-PREDATOR BEHAVIOR Desert grassland A. aperta have little risk of predation by birds because there are few perch sites available to these visual hunters and bird species diversity is low. Riparian spiders on the other hand, have at least eight species of birds that forage on them. Riechert and Hedrick (1990) assumed that exhibiting boldness toward an approaching bird is disadvantageous to AZ riparian spiders, and thus tested for between-population differences in response to such a cue. Specifically, we used the bulb portion of a camera cleaning brush to simulate the large-amplitude vibrations that an approaching bird might cause on A. uperta webs. We were interested in whether four puffs from this brush would cause foraging spiders to retreat into their funnels and, if so, how long it would be before the spiders would return to a foraging mode. We found that grassland spiders were less likely to retreat than AZ riparian spiders and that, when they did, their latencies to return to a foraging mode were significantly shorter (Table IV). These betweenpopulation differences in responses to predatory cues were evidenced in F, generation laboratory-reared individuals, indicating that this trait also has a genetic basis.
TABLE IV BETWEEN-POPULATION COMPARISONS OF LATENCIES TO ATTACK PREYA N D LATENCIES TO RETURN TO A FORAGING MODE FOLLOWING A PREDATORY CUE:"
NM grassland Mean Latency to attack crickets Feral individuals F, generation in lab. Latency to return to foraging following a predatory cue Feral individuals Fz generation in labs. (I
All data are in seconds.
SE
AZ riparian
Mean
SE
2.6 1.1
0.3 0.3
55.0 30.7
0.3 11.1
7.8 82.3
12.5 6.0
166.9 1195.4
147.8
31.3
EVOLUTION OF BEHAVIORAL PHENOTYPES
117
D. CORRELATED TRAITS Many contemporary studies of animal behavior attempt to explain behavioral evolution by focusing on one functional category of behavior at a time (e.g., foraging behavior, agonistic behavior, mating behavior) and measuring or inferring its contribution to the fitness of individuals. However, genes may influence many different characters, the manifold effects of a single gene being referred to as pleiotropism. Often there is resulting correlation between morphology and behavior, as in the classic work by Sturtevant (1915) in which Drosophila eye color was found to be genetically correlated with level of sexual activity. There also may be linkage between loci that are closely positioned on the same chromosomes such that they segregate together. In the light of these genetic phenomena, Dobzhansky (1956) stated that “a trait has no adaptive significance in isolation from the whole pattern that the organism exhibits.” Huntingford provides a nice example of the need to consider the suite of behaviors rather than single traits. She found that stickleback territorial aggression toward conspecifics during the breeding season covaries in the individual with “boldness” toward predators in the nonbreeding season. Thus, individual fish that are most successful in obtaining breeding sites are apparently also most vulnerable to predation. Huntingford (1976) hypothesized that territorial aggression and boldness toward predators shared some common factors(s) within the fish. More recently, intraindividual covariance between functionally different traits in some vertebrate species has been specifically attributed to the action of hormones such as testosterone. In several bird species, males with higher testosterone titers show enhanced levels of territorial aggression and courtship but lower levels of parenting than other males (e.g., pied flycatchers: Silverin, 1980; house sparrows: Hegner and Wingfield, 1987). My colleagues, John Maynard Smith and Ann Hedrick, and I have investigated the possibility that four seemingly unrelated fitness-related behaviors described in this section are under the same genetic influence. Riechert and Maynard Smith (1989) found that individual spiders within a population that tended to win territorial disputes also demanded larger territories. Spiders that exhibited longer latencies to attack prey also had longer latencies to return to a foraging mode following a predatory cue (Riechert and Hedrick, 1990).We have also established a link between the territorial behaviors and the attack and fear behaviors. A spider that showed a shorter latency to return to foraging following a predatory cue had a high probability of winning a territorial dispute against a spider that was equal in weight but had a longer latency to return to foraging.
I18
SUSAN E. RIECHERT
(Probability of being less fearful toward predatory cue and winning territorial dispute: NM feral individuals, .80; NM F, generation lab.-reared 3 9 ; AZ feral individuals, .70; AZ F, generation lab.-reared, .84.) Maynard Smith and Riechert (1984) developed a genetic model to explain the between-population differences noted at the time in territorial and agonistic behavior. The model assumed that genes controlled two antagonistic hormones, one governing levels of fear and the other levels of aggression. If we assume that there is directional dominance between the two populations in the genes that control levels of aggression and fear, as shown in Fig. 7, then the highly aggressive phenotype that results from crosses between the two populations is explained. Through study of the backcrosses and F, generation hybrids between AZ riparian spiders and NM grassland spiders we have further found that the aggression components of agonistic and territory size behaviors are controlled by genes on the sex chromosomes, while the fear component is controlled by multiple genes on the autosomes (Riechert and Maynard Smith, 1989). Finally, we conclude from these studies that all four traits probably represent pleiotropic effects of the same genes, rather than linkage among chromosomes. The genetic system is simply too complex and involves too many genes for linkage to be a likely cause. We also expect that these genes control the production of given hormones or threshold responses for their release.
PROPOSED MECHANISM OF INHERITANCE NM
X
AZ aa BB Low Low Aggresslon Fear
AA bb High High Aggression Fear YIELDS
F1 HYBRID NMAZ PROGENY Aa High Aggresslon
Bb Low Fear
FIG.7. Proposed directional dominance mechanism of inheritance of aggression and fear components of Agelenopsis aperra behavior. Phenotypes and genotypes for A 2 riparian and NM grassland individuals are shown, as well as the predicted outcomes of betweenpopulation matings. (From Maynard Smith and Riechert, 1984.)
EVOLUTION OF BEHAVIORAL PHENOTYPES
119
IV. ARIZONA R I P A R I A N POPULATION DEVIATION FROM ADAPTIVE EQUILIBRIUM As mentioned in the discussion of the various behavioral traits under consideration, riparian spiders repeatedly exhibit greater betweenindividual variability than do grassland spiders. For example, Fig. 8 shows the spread of points for latencies to return to foraging following a predatory cue in F, generation laboratory-reared AZ riparian spiders Riechert and Hedrick, 1990). Such anomalies were noted in a variety of data sets for this population, and led to my consideration of the possibility that AZ riparian spiders might not be at adaptive equilibrium with respect to their fitness-linked behaviors. The application of predictions from quantitative models to the specific traits has provided considerable insight into the problem.
A. ANALYSES OF EVOLUTIONARILY STABLESTRATEGIES Hammerstein and Riechert (1988), in one model, identified Evolutionarily Stable Strategies (ESSs) for each population that delineate the actions individual spiders should take in various contest contexts: (a) different body mass relationships between spiders disputing a territory, and (b) in the case of the grassland population, different site qualities. The potential actions an individual might exhibit following assessment of relative body mass and site quality were identified as: withdraw from the territory, display (visual or vibratory signaling that is non-injurious), and escalate (physical contact that is potentially injurious)(Riechert, 1984). Separate models were developed for each population since the external factors influencing contest behavior in each case were different (Table V,a). The value of holding a territory in the grassland, for instance, is much higher than in the riparian habitat because of what is referred to as “opportunity cost.” Opportunity cost reflects the availability of quality sites. If an individual loses a given territorial dispute, what is the probability that it will successfully obtain an adequate territory in a future dispute? For the riparian population, the probability is very high, since quality sites are abundant and floating is low in cost (Riechert, 1981). Thus, riparian spiders have low opportunity costs. But, in the grassland, the availability of quality sites is very limited and floating individuals suffer major fitness costs. Because grassland floaters lose so much of their body weight per day (Riechert, 198l ) , and because weight determines territorial dispute success (Riechert, 1978b), it is unlikely that an individual can remain a
120
SUSAN E. RIECHERT
floater for long and still be competitive. The value of winning a territorial dispute is thus much higher to grassland spiders: they have high opportunity costs. Bird predation on A. upertu is another selection pressure that should
0 GRASSLAND
OOO
00000
0 RIPARIAN
oooo0000
0
0
0 0
0 0 0
20
10
30
FAMILIES
FIG.8. Individual scores (one individual selected at random from each family) for latency to return to foraging following a predatory cue for F,generation descendants of NM grassland (0)and AZ riparian (0)populations. All trials were terminated at 1800 sec. (From Riechert and Hedrick. 1990.)
121
EVOLUTION OF BEHAVIORAL PHENOTYPES
TABLE V COMPARISON OF PAYOFF COMPONENTS (EXPECTED EGGMASS INCREMENTS A N D DECREMENTS, RESPECTIVELY,I N MILLIGRAMS WITH THE TERRITORIAL WET WEIGHT) OF EVENTSASSOCIATED DISPUTES OF TWO POPULATIONS OF Agelenopsis nperra Population
NM desert grassland AZ riparian a. Major payoff component Value of winning site Cost of leg loss Cost of lethal injury Cost of display b. Breakdown of display costs Energy expended Loss in food intake Loss to predation
16.7 14.2 93.7 0. I
4.8
lo-' 0. I 0
X
1.6 6.2 84. I 3.0 2.0
X
0.06 2.4
affect spider contest behavior: though it is a frequent event in the AZ riparian habitat, it is unknown for the NM grassland habitat (Riechert and Hedrick, 1990). Predation risk is a major fitness cost to AZ riparian spiders engaged in territorial disputes because the predation events occur when the spiders are on their sheet webs rather than in their funnels and territorial disputes occur on the web sheet (Hammerstein and Riechert, 1988; Riechert, 1988). Time exposed to predation, then, is an important cost to fitness in AZ riparian contests (Table V, a and b). When investigating the potential fitness payoffs of contest actions, we were interested to note that energy expenditure is a negligible cost compared to the costs to fitness of injury and mortality resulting from escalated fighting, mortality resulting from exposure to predation, and loss in foraging time in these contests (Table V, b; Riechert, 1988). Energy expenditure merely appears to be correlated with these costs. The ESS predictions for NM grassland spider behavior in various weight and site value contexts were found to approximate closely to the empirical strategy representation exhibited by individuals of that population (Hammerstein and Riechert, 1988). On the other hand, the empirical strategy representation of the AZ riparian population differed from the predicted ESS strategy set in a number of respects. AZ riparian spiders frequently displayed when it was predicted that they should have withdrawn from contests. There was also considerable escalation to fighting behavior, while no escalation was predicted for AZ riparian contests. Since the
122
SUSAN E. RIECHERT
predictions of the ESS model concerning the AZ riparian population were robust, Hammerstein and Riechert (1988) concluded that the observed deviation of the real contests from the predicted ESS was due to inadequacy of the model. For instance, we made no assumptions in the model, but rather obtained empirical measurements of all the parameters the model needed. Finally, the model presented by Hammerstein and Riechert (1988) represented the fourth model developed for the system, one which Maynard Smith, Hammerstein, and I feel takes into account all relevant information exchange and parameters. The failure of AZ riparian spiders to exhibit appropriate contest behavior (i.e., withdraw if you are the smaller opponent or an equal weight intruder, or display if you are the larger opponent or if equal in weight and the owner) has two major fitness costs to these spiders: risk of predation and risk of injury. Because territorial encounters occur on the web sheet and the opponents are not vigilant toward predators when engaged in fighting, predation risk is a major fitness cost to protracted display behavior in contests. Escalation in territorial disputes to physical contact and fighting has associated fitness costs as well because there is considerable risk of leg loss (7-36% depending on different body mass contexts) and mortality (0-33%). Note that the loss of even one leg reduces foraging efficiency by 10% and future contest success by 25% (Riechert, 1988).
B. OTHEREVIDENCE FOR ARIZONA RIPARIAN POPULATION DEVIATION FROM EXPECTATION Contest behavior is not the only trait the riparian population exhibits that deviates from expectations based on local prey availability and competitive criteria. Empirical data indicate that riparian spiders defend larger territories than are required to procure necessary prey even during drought years. Members of this population merely build smaller webs (Riechert, 1982) and exhibit a lower attack rate toward the broad spectrum of potential prey than do grassland individuals (Fig. 6; Riechert, 1991). Furthermore, inspection of Fig. 6 shows that AZ riparian spiders attack prey that can cause injury and mortality with the same frequency as prey types that can be more easily handled. This occurs despite the facts that (a)A. aperta can distinguish among prey types and (b) prey availabilities are such that, on most days, optimal food needs could be met in this habitat by restriction of the diet to a small subset of prey types that provide low handling times on the sheet web relative to joules of food obtained and no injury risk (Riechert , 1991).
EVOLUTION OF BEHAVIORAL PHENOTYPES
V.
123
FACTORS THATMAYHAVELIMITED ADAPTATION
The genetic studies completed by Riechert and Maynard Smith ( 1989) suggest that sufficient genetic variability exists so as not to limit adjustment to the ESS state indicated for the AZ riparian population. The robustness of the ESS model results, the degree of individual variability noted in AZ riparian spider behavior, and the fact that errant behavior is exhibited across a wide variety of traits all suggest that the failure of AZ riparian spiders to exhibit an adaptive equilibrium is a real phenomenon and not reflective of inadequate model development. Two other factors that are commonly cited as underlying maladaptation are recency of a change in local environment and high variability in the local environment. Neither of these factors seems pertinent to the AZ riparian situation. The spring-fed stream habitat has been present for at least 100 years and this stream supports high numbers of insect even in drought years. On the other hand, predation by birds applies strong selection pressure in the habitat against such behaviors as (a) maintaining excessively large territories, (b) spending time defending the larger territories, (c) engaging in lengthy displaying contests when withdrawal would have been the appropriate strategy, and (d) attacking prey that take a long time to subdue relative to the consumption benefits generated. Given the marked environmental constancy and high level of predation pressure against these aspects of behavior, it should take at most a few generations of selection to eliminate such behavior in A . aperta. There are two more likely alternative limiting factors: phylogenetic inertia and gene flow. A g e h o p s i s aperta is primarily an arid-land species. Its typical habitat is desert grassland or cactus scrub. The AZ riparian population can, in fact, be considered an island population which is surrounded by populations occupying more arid habitats. Under a phylogenetic inertia argument, I hypothesized that a major change in the “wiring” of the nervous system of A . aperta would be required to achieve the predicted changes in behavior. Under a gene flow argument, I hypothesized that sufficient mixing and consequent interbreeding occurs between riparian habitat A . aperta and more arid-land A. aperta from surrounding habitats to prevent the AZ riparian phenotype from becoming fixed.
A.
PHYLOGENETIC INERTIA
To test for potential phylogenetic inertia effects, I extended the study to a population of A . aperta occupying riparian habitats along the Pedernales
124
SUSAN E. RIECHERT
river in south-central Texas (TX riparian). This population is located at the eastern edge of the species range and differs from the AZ riparian habitat in that it is not surrounded by more arid habitats. My interest then, is in whether the TX riparian population, in the absence of potential gene flow, has achieved the “optimal” territorial and foraging behaviors predicted for riparian A. ugertu. I collected the same data on this population as for the AZ riparian and NM grassland populations. First, I established that levels of prey are similar in TX riparian habitats to those of the AZ riparian habitat (Table I). I also found that TX riparian spiders, like AZ riparian spiders, experience some level of bird predation (20%). Thus, I concluded that the selection pressures on the two populations are similar (Riechert, submitted). I also collected data on territory size, on spider behavior in territorial disputes, and on attack rates exhibited toward prey types offering different profitabilities. Both feral and laboratory-reared classes of TX riparian spiders showed significantly smaller territories than either NM grassland or AZ riparian spiders. In fact, TX riparian spiders defended only their webs; they did not defend additional space surrounding the webs (Table 11). The predicted and empirical strategy representations for AZ and TX riparian spider behavior in territorial disputes are presented in Table VI. The strategies predicted for these contests are context dependent, re-
TABLE VI PREDICTED A N D EMPIRICAL STRATEGY REPRESENTATION FOR A. uperru FIELD INDUCED CONTESTS OVER WEBSITES(RELATIVEPROPORTION) Empirical strategy representation Withdraw Predicted strategy Display If larger opponent If equal and owner Withdraw If smalleropponent If equal intruder
Display
Escalate
AZ
TX
AZ
TX
AZ
TX
.03 .08
.II
.60 .49
.85
*
.II
.82
37 .43
.04 .Ol
.26 .21
.53 .28
.54 .53
.46 .I2
.20 .20
.01
0
~~
Behavior was exhibited immediately following assessment of web site quality and relative weight of opponent. Withdraw refers to leaving web or web site, display to noninjurious visual and vibratory actions, and escalate to threat (intention movements made toward the opponent) and actual fighting for the A 2 riparian population and TX riparian population.
I25
EVOLUTION OF BEHAVIORAL PHENOTYPES
flecting the relative size (weight) of the two opponents in each contest as well as ownership status. The decisions exhibited by TX riparian spiders in these various contest contexts closely follow predicted behavior for a population existing with unlimited food but with a risk of predation by visual predators such as birds. Note the lack of escalation and the high frequency of withdrawal from the contests when the individual had a size or ownership disadvantage. The empirical strategy representation exhibited by TX riparian spiders differed significantly from that exhibited by AZ riparian spiders. Remember that AZ riparian spiders exhibited greater escalation and display than predicted by ESS modeling results (Hammerstein and Riechert, 1988). Because models of optimal foraging behavior predict that, as prey abundance increases in a system, predators will exhibit a narrower diet (i.e., show greater selectivity toward those prey types that are more profitable), both AZ and TX riparian spiders were predicted to limit prey intake to the most profitable subset of prey types. In contrast, the NM grassland spiders would need to capture a broader spectrum of prey types. Table VII shows the results of feeding trials for the three populations. As predicted, NM grassland spiders attacked prey of low- and high-profitability rankings with equal propensity and TX riparian spiders showed the high attack rate toward high-profitability prey and the low attack rate toward lowprofitability prey as predicted for a population with abundant food. As already discussed, AZ riparian spiders showed a low attack rate toward all prey regardless of its category. In summary, the TX riparian spiders appear to show behavior that is predicted for a population with unlimited food and predation by avian TABLE VIi COMPARISON OF ATTACK RATES TOWARD PREYOF DIFFERENT PROFITABILITIES FOR THREEPOPULATIONS"
Prey types Low profitability Ants Plant bugs Predaceous bugs High profitability Moths Damselflies
Profitability (j/sec capture effort)
.2 .3 .6
8.3 25.0
Capture attempt rates ( n ) NM grassland
AZ riparian
TX riparian
.96 .72 .53
.59 SO .67
.31 .21 0
.87
.54 .47
.95 .94
.%
Profitability scores and NM and AZ attack rates from Riechert (1991).
126
SUSAN E. RIECHERT
predators: they have small territories, do not risk injury and mortality in fighting over web sites, and limit their diets to prey that provide the highest energy rewards with least cost. Because this population of A . apertu has adapted to similar conditions to those to which the AZ riparian population is exposed, I conclude that phylogenetic inertia does not underly the deviation of AZ riparian spiders form predicted behavior. These results also lend support to the gene flow argument, since the major difference in conditions between the TX riparian and the AZ riparian sites was the presence of surrounding arid habitats occupied by A . aperta in the case of the AZ riparian area. B. GENEFLOW To investigate potential gene flow influences, I extended the study to neighboring habitats in the AZ riparian area: evergreen woodland, dry riparian, and cactus scrub. The AZ riparian habitat is a narrow strip of flat land dissected by a creek. As one leaves the influences of the waterway, the riparian woodland is replaced by an open, live oak woodland referred to as evergreen woodland. As one follows the creek further down the mountain toward the desert flats, the stream becomes intermittent and supports a dry riparian habitat which includes trees adapted to more arid conditions (e.g., mesquite). Beyond the influence of the waterway in this area, the predominant habitat is cactus scrub-cacti and arid-adapted shrubs are sparsely distributed along with patches of grass on a gravel substrate. Agelenopsis aperta inhabits all of these habitat types in the Chiricahua Mountain area. The prey availability relationships among the habitats A. aperta occupies in the Chiricahua Mountains are shown in Fig. 9. Dry riparian and evergreen woodland habitats afford similar prey levels to those in NM grass1and;whereas the cactus scrub has even lower levels of prey than offered in the NM grassland (Riechert, submitted). The behavior of spiders in the more arid AZ habitats is also similar to that of NM grassland spiders (Table VIII). Escalation in contests is frequent in occurrence and high attack rates are exhibited toward prey, regardless of their profitabilities. Two measures were used to test for potential gene flow between the AZ arid-land local populations and the AZ riparian population. The first entailed electrophoretic analyses of population genetic structure and the second consisted of monitoring the movements of spiders between adjacent AZ riparian and evergreen woodland habitats. Sewall Wright (1931) noted that the extent to which gene flow influences population genetic structure is dependent on the relationship between the number of immigrants (m)and the breeding size of the population (N)where
127
EVOLUTION OF BEHAVIORAL PHENOTYPES
'.O
i
R
AZ NM
0.8 -
I-
:
DG
I
0.0
L LOCAL POPULATIONS
FIG.9. Prey availabilities to different local populations of A. aperta in the Chiricahua Mountain area of Arizona with the NM grassland population included for reference. CS, AZ cactus scrub; DR, AZ dry riparian; DG, NM desert grassland; EW, AZ evergreen woodland; and R, AZ riparian. Optimal energy needs refer to prey levels equal to or greater than the 20 rng dry weight meal that this spider will consume when given the opportunity.
Nm
= effective population size. He found that an N m of greater than 1 is enough to overcome the effects of genetic drive and that an N m of greater than 4 is suggestive of general mixing. I calculated N m for the AZ populations in the Chiricahua Mountain area using the F statistic measure applied. to 17 loci, 11 of which were polymorphic. The mean N m for these loci was 4.96. I assume then that, at least at some time in their past evolutionary history, there was general mixing among these local populations. To determine whether exchange regularly occurs, I set up six 2-m drift fences within AZ riparian and evergreen woodland habitats and at the interface between them. When spiders hit a barrier, they turn and walk
128
SUSAN E. RIECHERT
TABLE VIIl COMPARISON OF CONTEST AND DIETCHOICE BEHAVIORS AMONG DIFFERENT LOCAL POPULATIONS OF Agelenopsis aperfa RANKEDFROM LEASTPREYAVAILABILITY TO GREATEST PREYAVAILABILITY ~~
Population
Probability of owner escalation
AZ cactus scrub NM grassland AZ evergreen woodland A 2 dry riparian AZ riparian
.79 .77 .68 .68 .43
Probability of attack profitability Low
High
.96 .77 .89 .62
.90 .91 .88
.s1
.77
.sI
along it. Thus, the placement of pitfalls along each side of the barrier ensures that all A. upertu intercepting the length of the barrier are collected. 1 found 97% of the AZ riparian spider movement to be within the boundaries of this habitat, while 42% of the evergreen woodland spider movement was into the riparian habitat. There was a net influx of spiders into the AZ riparian area from the neighboring more arid habitat. Adult males (56%) were the major migrants. Since A. upertu readily crossbreeds across populations, I conclude that the level of gene flow between AZ riparian and evergreen woodland spiders is high and that it is this mixing of behavioral phenotypes that limits AZ riparian population progress toward an adaptive equilibrium. This is because, each fall, adult males from the evergreen woodland move into the riparian habitat seeking matings. This leads to the intermixing of arid-land and riparian phenotypes. Spiderlings emerging the following spring from these matings are subjected to predation pressure and the arid-land phenotype is weeded out only to be reintroduced the following fall by migrant males.
VI. EXPERIMENTAL MANIPULATION OF GENEFLOW VERSUS SELECTION
To test the hypothesis that gene flow restricts adaptation in the AZ riparian situation, I set up eight enclosures in the AZ riparian habitat that restricted gene flow (Riechert, submitted). I released the same genetic complement of spiderling A. upertu into each enclosure following the removal of all native A. upertu from them. Four of the enclosures were covered with bird netting such that they were protected from predation
EVOLUTION OF BEHAVIORAL PHENOTYPES
129
by birds. The other four enclosures were left open and hence the spiders in them were exposed to bird predation. After 6 months, I tested the spiders in the enclosures for their responses to predatory cues (the fear test described earlier) and for their aggressiveness in encounters (probability of winning an equal-weight encounter over a web produced by a third individual). Spiders in the protected enclosures scored as being significantly (one way analysis of variance; p < .0008)less fearful in the fear test than spiders in the exposed enclosures. The spiders in the protected enclosures also won the majority of the contests when bouted against individuals collected from the enclosures that permitted bird predation (74%). Finally, there were four times as many spiders remaining in the protected enclosures than in the exposed enclosures, suggesting that the behavioral results reflect the weeding out of the more aggressive (arid-land phenotype) spiders in the exposed enclosures. Alternatively, the differences in behavior may have reflected experiential effects: the spiders exposed to bird predation may be more fearful because of predation attempts on them. I tested between these two alternatives by completing the behavioral trials on offspring of the above two treatments of test spiders. This was accomplished by allowing the spiders remaining in the respective enclosures after selection to mate and produce egg cases. The offspring (F,) resulting from these within-enclosure (and hence, within-treatment) matings were collected at emergence from their egg cases and were individually raised in the laboratory with unlimited food and no experience of conspecifics until they were large enough for their behavior to be scored. Note that, because I collected the F, generation spiders at the time of their emergence from egg cases, these individuals had not experienced the imposed selection regimes themselves. I obtained the same behavioral results as I had for the spiders actually put under selection pressure. Only one of the exposed enclosures produced offspring, whereas all four of the protected enclosures had emergent spiderlings. I attribute the lack of offspring in the exposed enclosures to the fact that the levels of bird predation pressure were sufficiently high that both sexes were not present in these enclosures at maturity and hence no reproduction took place. In comparing the fear test scores for spiders from the single replicate of the exposed treatment to the sets of scores for each of the four protected. treatments, the exposed treatment F, generation scored as significantly more fearful than all sets of protected treatment spiders ( t test results: p < .0006, .015, .00002, and .0006, respectively). Further, contests between equally matched F, offspring of selected spiders belonging to the exposed treatment versus the protected treatment were won by protected treatment opponents 86% of time.
130
SUSAN E. RIECHERT
The results of this experiment clearly indicate that one generation of selection in the absence of gene flow is sufficient to observe a marked shift in behavior. Because the offspring produced by individuals that had been subjected to different selection pressures scored similarly to the parent generation for the respective treatments, I conclude that the noted shift reflects the weeding out of the more arid-land phenotypes in the exposed enclosures. If the behavioral shift had been experiential (i.e., individuals exposed to bird predation were more fearful), then their offspring that had not been subjected to bird predation should have shown the broader spread of “fear” scores observed in the behavior of protected treatment spiders. They should also have won approximately 50% of the contests. They did not. The fact that A. aperta in nature exhibits a mixture of arid-land and riparian phenotypes in the riparian habitat offers strong support of the view that gene flow limits adaptation to local conditions in the riparian habitat. VII. DISCUSSION AND CONCLUSIONS The theme of adaptation underlies much of current evolutionary thought. As John Maynard Smith (1989) states, “Darwin was well aware that organisms are adapted before he thought of his theory: adaptation is the most obvious and all pervasive feature of living things, and one that any theory of evolution must explain.” Two recent treatments of specific systems are exemplary of the evidence for the operation of natural selection in nature (Endler, 1986; Grant, 1986). Even though the construct of adaptiveness encompasses behavioral ecology, ethology, and all other fields adjoining evolutionary biology, it is not without its critics. Adaptationists are criticized for too often not falsifying the hypothesis that a trait is not adaptive. How frequently, for instance, do papers get left unpublished because the study of adaptation has produced negative results, and how often has the conclusion been reached that there is some other adaptive explanation for the observed trait when it fails to meet the role predicted of it? The debate over adaptation actually relates to problems encountered in testing it. There must first of all be a means by which the adaptiveness of characters can be determined, that is, they must be measured in terms of their fitness consequences. There must also be a means of applying alternative explanations to the results of empirical studies. In my longterm study of the selection pressures operating on A. aperta, I have approached both of these problem areas. Through extensive ecological studies I have identified the relevant behavioral traits that determine indi-
EVOLUTION OF BEHAVIORAL PHENOTYPES
131
vidual success under various selection pressures that are important to this desert species. I have also eliminated various alternative models to natural selection as accounting for the proposed adaptiveness of these traits. For example, one alternative might be that the traits are not genetically determined but rather are influenced directly by experience with the environment, as in learning. As Brandon (1990) states, for evolution by natural selection to occur there must be variability in the trait, the trait must be heritable, and there must be selection on the trait. In the A. aperta system, population crosses and the laboratory rearing of population lines with no environmental experience prior to scoring of the various behavioral traits have demonstrated that environmental and experiential effects are minimal when compared to the influence of their underlying genetic bases. Another alternative explanation is that the traits might be correlated, as in pleiotropism, with other traits that are under selection. Then, the trait in question might merely be along for the ride (i.e., selectively neutral). There is evidence to suggest that the four traits I have investigated, territory size, agonistic behavior, latency to attack prey, and response to predatory cues, may be pleiotropic effects of the same genes or in some other way correlated. This does not, however, detract from the fact that they are all under selection pressure. This is because I have identified the relevant selection pressures and considered the fitness consequences of exhibiting various behavioral “strategies” in the respective populations. I conclude that the selection on all of these traits is, at least, in the same direction. It is not possible at this stage of my analysis of the system to determine whether selection on any one trait drives the system. I have indeed identified one population (AZ riparian) that fails to exhibit behaviors that are adapted to its local environment, one that affords abundant food and an ameliorated physical environment but has high levels of avian predation. I pursued two alternatives to adaptation that preliminary evidence deemed most plausible: phylogenetic inertia and gene flow. In identifying a population of this spider that exists under similar selection pressures to the AZ riparian population and that exhibits behaviors appropriate to these selection pressures, I was able to falsify the phylogenetic inertia or design constraints hypothesis. The test for phylogenetic inertia was completed on a population of A. uperta that was not subject to gene flow from surrounding populations under different selection pressures. The fact that this population was at adaptive equilibrium, while the AZ riparian population that had potential gene flowfrom more arid habitats was not, supported the gene flow hypothesis. I feel that it is clear from both (a) the empirical studies completed on the genetic structure of the local populations in the area and the movement
132
SUSAN E. RIECHERT
between AZ riparian spiders and the adjacent evergreen woodland habitat and (b) the experimental manipulation of predation pressure while limiting gene flow that it is gene flow that is restricting the AZ population from reaching an adaptive equilibrium. This appears to be a problem of scale then, where the genetic neighborhood (Wright, 1946) is greater than the selectively homogeneous environment (Brandon, 1990) of the AZ riparian habitat. Gene flow is important because it determines the extent to which changes in local populations may be independent. Just as there is a difference of opinion concerning the pervasiveness of adaptation, there are conflicting views on the role of gene flow in evolution. Slatkin (1985) presents a nice review of the arguments. Briefly, Mayr (1963) argued that gene flow is important in maintaining the genetic and phenotypic homogeneity of a species, because interpopulational breeding often occurs through dispersal. Others have since argued that between-population exchange may not be as great as is theoretically possible and that strong natural selection pressure should overcome any homogenizing effects that gene flow might produce (e.g., Erhlich and Raven, 1969; Endler, 1977; but see Brandon, 1990). Since this latter view appears to be the prevailing one (Slatkin, 1985), I have been particularly interested in the question of the extent to which strong selection pressures can be overcome by gene flow. The results of my selection experiment clearly conflict with the prevailing view. I prevented gene flow from occurring and subjected genetically homogeneous groups of animals to different selection pressures and observed a strong shift in behavior within one generation. I conclude that within a local area, gene flow can indeed underlie apparent cases of maladaptation. Just like the Red Queen’s remark to Alice in Through the Looking Glass, the AZ riparian population “takes all the running [it] can do, to keep in the same place.” Two possible responses of populations to this kind of problem include (a) reduction of the genetic neighborhood (Brandon, 1990), and (b) flexible behavior which would permit individuals to do well across a range of selective environments (Sultan, 1987). Agelenopsis aperta exhibits neither of these solutions. Perhaps, there are design constraints (i.e., there is phylogenetic inertia) which hinder such changes.
VIII. SUMMARY Comparison of the behavior of populations existing under markedly different prey availability levels and predation pressures permits the inves-
EVOLUTION OF BEHAVIORAL PHENOTYPES
I33
tigation of the evolutionary processes that underlie adaptation to local conditions. The long-term study outlined here involved the competitive, foraging, and antipredator behaviors of two spider populations, one that was food limited with no risk of predation by birds, and one that had abundant food but a high risk of bird predation. The behavior patterns investigated were found to have strong genetic bases and hence are subject to selection. Whereas the population existing under limited food was found to be at adaptive equilibrium with respect to its behaviors and the local environment, the population with abundant food was not. The potential contributions of gene flow and phylogenetic inertia to the observed deviations were tested, and gene flow was identified as the limiting adaptation. Finally, a selection experiment is discussed in which one generation of selection in the absence of gene flow is shown to be sufficient to cause a marked change in the behavioral phenotypes of spiders belonging to this maladapted population.
References Arnold, S. J. (1981). Behavioral variation in natural populations. Euolurion (Lawrence, Kans.) 35,489-515. Brandon, R. N. (1990). “Adaptation and Environment.” Princeton Univ. Press, Princeton, NJ. Dobzhansky, T. (1956). What is an adaptive trait? Am. Nar. 90, 337-347. Endler, J. A. (1977). “Geographic Variation, Speciation and Clines.” Princeton Univ. Press, Princeton, NJ. Endler, J. A. (1986). “Natural Selection in the Wild.” Princeton Univ. Press, Princeton, NJ. Erhlich, P. R., and Raven, P. H. (1969). Differentiation of populations. Science 165, 1228-1232. Grant, P. R. (1986). “Ecology and Evolution of Darwin’s Finches.” Princeton Univ. Press, Princeton, NJ. Hammerstein, P., and Riechert. S. E. (1988). Payoffs and strategies in spider territorial contests: ESS-analyses of two ecotypes. Euol. Ecol. 2+ 115-138. Hedrick, A. V., and Riechert, S. E. (1989). Population variation in the foraging behavior of a spider: The role of genetics. Ecologia 80, 533-539. Hegner, R. E., and Wingfield, J. C. (1987). Effects of brood size manipulations on parental investment, breeding success, and reproductive endocrinology of house sparrows. Auk 104,470-480. Huntingford, F. A. (1976). The relationship between antipredator behaviour and aggression among conspecifics in the three-spined stickleback. Anim. Behav. 24, 245-260. Krebs, J. R., and Davies, N . B. (1981). “An Introduction to Behavioral Ecology.’’ Sinauer, New York. Maynard Smith, J. (1989). “Evolutionary Genetics.” Oxford Univ. Press, Oxford. Maynard Smith, J., and Riechert, S. E. (1984). A conflicting tendency model of spider agonistic behaviour: Hybrid-pure population line comparisons. Anim. Eehau. 32, 564-578. Mayr, E. (1963). “Animal Species and Evolution.” Harvard Univ. Press, Cambridge, MA.
134
SUSAN E. RIECHERT
Pyke, G. H. (1984). Optimal foraging theory: A critical review. Annu. Rev. Ecol. Syst. 15, 523-575. Riechert, S . E. (1976). Web-site selection in a desert spider, Agelenopsis aperta (Gertsch). Oikos 27, 311-315. Riechert, S. E. (1978a). Energy-based temtoriality in populations of the desert spider Agelenopsis aperta (Gertsch). Symp. Zool. SOC. London 42, 21 1-222. Riechert, S. E. (1978b). Games spiders play: Behavioral variability in territorial disputes. Behau. Ecol. Sociobiol. 3, 135-162. Riechert, S. E. (1979). Games spiders play. 11. Resource assessment strategies. Behau. Ecol. Sociobiol. 4, 1-8. Riechert, S . E. (1981). The consequences of being territorial: spiders. a case study. A m . Natr. 117,871-892. Riechert, S. E. (1982). Spider interaction strategies: Communication versus coercion. In “Spider Communication; Mechanisms and Ecological Significance” (P. N. Witt and J . Rovner, eds.). Princeton Univ. Press, Princeton, NJ. Riechert, S. E. (1984). Games spiders play. 111. Cues underlying context associated changes in agonistic behavior. Anim. Behau. 32, 1-15. Riechert. S. E. (1985). Decision problems in multiple goal contexts: Spider habitat selection. Z . Tierpsychol. 70, 53-69. Riechert, S. E. (1988). Energetic costs of fighting. Am. Zool. 28, 877-884. Riechert, S. E. (1991). Prey abundance versus diet breadth in spider test system. Euol. Ecol. 5, 327-338. Riechert. S. E., and Hedrick, A. V. (1990). Levels of predation and genetically based antipredatory behavior in the spider, Agelenopsis aperta. Anim. behav. 40, 679-687. Riechert, S. E., and Maynard Smith, J. (1989). Genetic analyses of two behavioural traits linked to individual fitness in the desert spider, Agelenopsis aperta. Anim. Behau. 37, 624-637. Riechert, S . E., and Tracy, C. R. (1975). Thermal balance and prey availability: Bases for a model relating web-site characteristics to spider reproductive success. Ecology 56, 265-284. Silverin, B. (1980). Long-acting testosterone injections given to a population of wild male pied flycatchers. Anim. Behav. 28,906-912. Slatkin, M. (1985). Gene flow in natural populations. Annu. Rev. Ecol Syst. 16, 393-430. Sturtevant, A. H. (1915). Sex-linked characters inDrosophila repleta. Am. Natr. 49,189-192. Sultan, S. E. (1987). Evolutionary implications of phenotypic plasticity in plants. Euol. Biol. 21, 127-178. Turesson, G. (1922). The genotypic response of the plant species to the habitat. Hereditas 3, 211-350. von Wahlert, G . (1965). The role of ecological factors in the evolution of higher levels of organization. Syst. Zool. 14, 288-300. Wright, S. (1931). Evolution in mendelian populations. Generics 16, 97-159. Wright, S. (1946).Isolation by distance under diverse systems of mating. Genetics 31,39-59.
ADVANCES IN THE STUDY OF BEHAVIOR. VOL. 22
Proximate and Developmental Aspects of Antipredator Behavior E. CURIO ARBEITSGRUPPE FUR VERHALTENSFORSCHUNG FAKULTAT FUR BIOLOGIE RUHR-UNIVERSITAT BOCHUM D-4630 BOCHUM, GERMANY
I. INTRODUCTION
Since most animals are the prey of others, antipredator behavior is widespread. While primary defenses, e.g., crypsis, aposematism, and mimicry, forestall the attack of predators, secondary defenses act to deter the predator from an attack, assuming that the prey has enough time to deploy them (Edmunds, 1974). Because they engage the predator in an interaction with its prey, secondary defenses have become the center stage of much ethological work focusing on the prey’s behavior. In order to flee from, bluff, mob, or attack the predator, the targeted prey must localize and identify it. This follows from the fact that most secondary defenses are costly in terms of time, energy, and risk (e.g., Curio, 1978). Hence, there is a need to avoid being fooled by false alarms. Except for the ubiquitous startle responses of many prey animals required when there is no time for recognition, a large proportion of prey animals possess highly sophisticated mechanisms for the identification of predators. Basically, they fulfil two functions: First, they have to recognize a predator, or brood parasite, i.e., to discriminate it from what is often a large number of harmless yet similar species. Second, they have to link the outcome of this perceptual performance with the appropriately selected motor pattern. Whereas the relationship of the ensuing motor pattern with the predatory threat has received some attention (Edmunds, 1974; Kruuk, 1964), there has been no comprehensive treatment of the first mentioned (i.e., perceptual) function. This review is devoted to the diverse mechanisms subserving this perceptual function. Discussion is confined to vertebrates since it is on these I35 Copyright 0 1993 by Academic Press, Inc. All rights of reproduction in any form reserved.
136
E. CURIO
that some of the most penetrating analyses have been performed. In Section 11, three interrelated questions will be asked, focusing on three levels of increasing perceptual complexity. First, how is the core performance of decoding the compound stimulus which the adversary comprises organized? Because of their high stimulus specificity,the releasing mechanisms involved have proved eminently suited for a multifaceted stimulus analysis. Second, to what extent is the perceptual core performance governed by context external to the prey animal? (By thus restricting use of the term context I will streamline the discussion and ignore the inclusion of internal states encompassed by context as used by others [e.g., Smith, 19771.) The stimulus complexity embodied in the context surrounding the adversary is generally such as to defy any attempt to break it down into separable key stimuli, a procedure which has been successfully employed when analyzing the adversary pattern itself. Evidence suggests that an appropriate decoding of the adversary “Gestalt” within a given context depends on a higher order process of decoding, that is, risk assessment. The study of context is still in its infancy. Third, even more rudimentary is our knowledge of the effect on prey animals of indirect, hidden cues emanating from predators or their activities. Effects of this sort will similarly lead to the analysis of antipredator behavior in terms of “hidden-risk’’ assessment, thus rendering the picture of the underlying decoding processes extremely complex. Although we set out with a strictly causal approach, the unavoidable introduction of risk, afunctional concept, exemplifies an important point: Leaving out that functional idea would prevent us from identifying problems of causation; without considering risk, we would not even think of the existence of risk assessment, nor the many forms it can assume. In Section 111, I show that much enemy recognition is achieved by IRMs (innate releasing mechanisms). By IRM I mean a perceptual mechanism which achieves the identification of a (compound) stimulus without any prior experience with it. To examine the developmental nature of that identification process a deprivation experiment is usually set up. In it an animal is deprived of the very stimulus whose recognition one is going to test. There is a discussion of some complications jeopardizing this technique. Furthermore, it will be argued that IRMs tuned to genuine predators are less susceptible to learning than are IRMs decoding harmless, yet potentially dangerous species. These abilities pertain to the adversary Gestalt. However, there is a dearth of information on whether the decoding of context or hidden risk is innately programmed as is recognition of the adversary pattern per se. A variety of learning mechanisms, including cultural transmission of recognition, are discussed. In doing so, it
ASPECTS OF ANTIPREDATOR BEHAVIOR
137
becomes apparent that we are still a long way from understanding the developmental component processes underlying such learning. To streamline the review, I largely restrict it to antipredator behavior elicited by visual stimuli, thereby bypassing our extensive work on acoustic cues. Full statistical details of the experiments that are described are not given here, but may be found in the original papers describing the experiments that are referred to in the text.
11. CAUSAL ASPECTSOF ENEMY RECOGNITION A.
KEYSTIMULUS ANALYSIS
The Use of Dummies Because it is difficult to alter the key stimuli produced by a live predator, dummies of various degrees of realism have been used. In many cases, rather crude replicas of the real animal have permitted an analysis of the releasing stimuli involved. This approach was first pioneered by Portielje (1926), and later developed by many others (e.g., Tinbergen, 1951). It was also profitably employed in studying releasers in the social context (Kuenzer, 1975). In other cases, dummies had to be rather realistic in overall appearence (Curio, 1975) or posture (Robertson and Norman, 1976) to be effective. In particular, movement proved to be of vital importance (Curio, 1975; Owings and Owings, 1979), and mammalian species especially seem to require rather exact replicas of the natural stimulus situation. An ongoing antipredator behavior can profitably be seen, in part, as manipulating and probing the behavior of the predator (D. H. Owings and D. F. Hennessy, personal communication, 1981). Such a requirement cannot possibly be fulfilled by dummies. Movement of the whole stimulus object or of a part of it may be extremely brief and still trigger an antipredator response. Pied flycatcher (Ficedula hypoleuca) pairs that had overlooked a red-backed shrike (Lanius collurio) dummy in front of their nest hole, started mobbing it once it had been made to move up and down with its perch for only 1 second (Curio, 1975). Likewise, parent great tits (Purus major) responded immediately to a tawny owl (Strix aluco) dummy upon one turn of its head, with the response coming to an end only after removal of the stimulus (E. Curio, unpublished). It appears as if a minimum of movement is sufficient to capture the attention of the birds since, in both species, the vast majority of subjects responded to the static dummy equally strongly. This demonstrates that movement was dispensable. However, since the history of the 1.
138
E. CURIO
birds was not known, a more subtle role of movement cannot be excluded (Section III,D,2). Despite the unquestionable success of the dummy method, it remains to be shown that dummies elicit, at least qualitatively, the same response as the live stimulus. Two Darwin’s finch (Geospizcr) species were found to exhibit qualitatively the same response to a tethered live short-eared owl, a species inhabiting the same island, as they did to a stuffed mount of the same species. During presentations in the field, the live owl was docile. Upon discovering it, finches assembled round it and emitted the same monosyllabic mobbing calls in both types of trial. The only difference was that the birds approached the live owl significantly less closely (Fig. 1). In a very similar experiment, Knight and Temple (1986a; see also Gard et al., 1989) arrived at basically similar conclusions, except that a live crow (Coruus brachyrhynchos) was approached by red-winged blackbirds (Agelaius phoeniceus) more closely (“aggressively”) than a stuffed one. In another experiment, Darwin’s finches behaved in qualitatively the same way toward a tethered native snake (Drornicus sp.) as to a dummy snake, regardless of whether the latter was moved or was static (Curio, 1965). Furthermore, pied flycatchers on their breeding grounds have been shown to exhibit mobbing responses to both stuffed and live perched individuals of two of their commonest avian predators, the red-backed shrike and the tawny owl. The strength of response to the dummy shrike ( n = 133) did
0 21 E
.->
m
8 6
4
Geospizo fuliginosa
0
1
L,, 0
2
3
L
5
6
10
1
2
3
L
5
15m
J
Minimum Distance FIG.1. Comparison of effect of tethered live owl and dummy owl (Asio.flummeiis) on minimum distance of mobbing by individuals of two species of Darwin’s finches. The live owl is approached less closely (both species pooled: two-tailed pz = 2 x 10“. Mann Whitney U-test). (Redrawn from Curio, 1969.)
ASPECTS OF ANTIPREDATOR BEHAVIOR
I39
not differ from that given to the live predator (n = 33); if anything, there was a tendency to exceed it (Curio, 1975,Table I). Similarly, the responses given to a live tawny owl fell within the range of responses elicited by both mounts of a tawny owl and even the tiny pygmy owl (Glaucidiurn passerinurn)(Curio, 1975, Table 11). Hence, there is good evidence that dummies can justifiably be viewed as stimuli eliciting the full-blown response to the predators they represent, but the response strength thus obtained should always be calibrated against that elicited by the natural predator. Almost all studies of antipredator behavior employing predator dummies fall short of this control. Milinski (personal communication) has suggested an objection: That the stimulus value of a dummy may equal that of the real thing by chance. Although it is recognized as a weak form of predator, the strangeness of a mount per se may compensate for any stimulus deficiency. However, as will be shown below for a nonpredatory bird, the nature of a mount per se would not appear to intimidate prey birds. The skepticism about the dummy method expressed by Knight and Temple (1986a) appears not quite justified. They base it mainly on the fact that (a) a dummy used in their own study elicited a quantitatiuely different response compared to the real animal; (b) other authors (refs. in Knight and Temple, 1986a) who failed to employ the real animal as a control gave up experimenting with dummies (in one case-ironically-because the author was not sure whether the dummy-elicited response was deficient in any way). Their reason (a) undermines my insistence that one must control for any deficiency of a dummy against the standard of the live predator. Their reason (b) is based on negative evidence and therefore not very helpful. Knight and Temple (1986b, 1988) themselves used predator models without calibrating them against the live predators and without mentioning their previous skepticism. Loughry (1987) found that blacktailed prairie dogs (Cynornys ludouicianus) harassed an unrestrained snake in ways that differed subtly from responses to a tethered one. Most of the differences reflected the different locale of the two types of presentation: the mouth of burrows in natural encounters and above ground in staged encounters. However, differences between categories of animal (male/ female; parenthonparent) were consistent despite the two manners of presentation. The assertion of Loughry (1987) that this result was the first to validate the use of a restrained predator is clearly unwarranted in view of the earlier evidence summarized above. Lorenz (1943) had described in a number of birds a response (“Gespenstreaktion” = “ghost response”) that is elicited by a conspecific of unusual appearance, e.g., an albino. This response resembles the typical antipredator response of the species concerned on a number of counts.
I40
E. CURIO
According to Lorenz’s view, a predator dummy might trigger protective behavior because of its “Gespenst” character. In order to test for this potential effect of predator dummies, one would have to render a familiar object odd by, for example, mounting a specimen of a familiar, nonpredatory species and comparing it to similar-sized genuine predator stimuli. We performed this experiment with Geospiza difficilis, the sharp-beaked ground finch, living syntopically (= in the same habitat) with the extremely common Galapagos dove (Zenaida galupagoensis) on Tower Island (Genovesa). In experimentally naive finches, a stuffed Galapagos dove facing the subject elicits only a fraction of the fear response given to a stuffed forward-facing head of the short-eared owl that also occurs on Tower Island (see Fig. 23, Section 111,C). The dove is even less effective than is a torch, a novel stimulus, though this difference falls short of significance (Curio, 1969). The low stimulus effectiveness of both the dove and the torch rules out an alternative explanation based on novelty. One could submit that the owl surrogate is more effective than the dove because the owl is less common than the dove and, hence, some fear of novelty (Section II,A,3) might have rendered it more effective. This idea, however, can be dismissed since the lamp was even more novel than the owl; as this owl is active during the day, it was certainly familiar to the finches. The fact that the mounted dove released some fear may have been due to the novel circumstances under which it was presented to the finches. The mounted dove experiment thus seems to rule out the Gespenst hypothesis for the efficacy of dummies; the Galapagos dove was totally familiar to the finches, did not elicit a fear response in the wild, and was larger than the owl head. Therefore, being dead or mounted as a specimen per se can hardly trigger antipredator behavior, thus validating in yet another way the approach using predator dummies. The same confidence may not apply to a dead conspecific (Section II,B ,3,b). 2 . Suddenness A sudden movement or a loud noise set forth a variety of alert behaviors like freezing, crouching, precipitous flight, or facing the alerting stimulus for closer examination. Both of these alerting events may signal danger, since most predators rely on surprise, and surprise depends on speed of attack. The exact nature of the response will depend on many details of context, the subject’s history, and on the stimulus itself. The last of these may vary widely but still elicits a response, given some minimum intensity. Given this low stimulus specificity, examining the effect of context appears more rewarding than examining stimulus quality. The startle response, a simple muscle twitch, has been studied in European starlings (Sturnus vulgaris) by Pomeroy and Heppner ( 1977). This
ASPECTS OF ANTIPREDATOR BEHAVIOR
141
response is very quick, averaging 76.4 msec for visual and 80.6 msec for acoustical stimuli. Because of their greater realism, studies of the more complex takeoff response to sudden movements deserve closer attention. Davis (1975) studied socially induced takeoff responses in domestic pigeons, the vertebrate with the highest recorded flicker fusion frequency (15O/sec) (ref. in Frankenberg, 1981). On being alarmed by an electric current through a perching grid an actor pigeon took flight and other observer pigeons followed suit immediately. Response latency to the electric stimulus was 250 msec but there was no measurable time difference between the alarmed actor’s takeoff and that of the observers. The actor’s takeoff was not preceded by any preflight activities whereas spontaneous, noninduced flights were. The more prevalent were these preflight activities the less contagious were spontaneous takeoffs. Although subtler differences, as yet undiscovered, between both types of takeoff may exist, it appears likely that preflight activities suppress socially induced takeoffs of observers. (These inhibitory signals must differ from those that spark off the synchronized takeoffs of pigeon flocks not preceded by any external alerting stimulus.) The impact of the social context on protective takeoff has been studied by Frankenberg (1981) in a more natural setting in European blackbirds (Turdus merufa).Following up my suggestion, he examined experimentally the “alerting others” hypothesis of avian mobbing behavior. This predicts that birds that perceive others mob are alerted to flee from imminent danger, which normally would be the very predator that elicited mobbing from the actor(s). An actor blackbird was induced, in its cage, to mob a stuffed owl that an observer blackbird was prevented from seeing (Fig. 2). The observer in a neighboring cage was allowed to see and hear the actor, and it was additionally exposed to a startle stimulus, a wooden lever that the actor could not see. This lever could be made to rotate suddenly through an arc of 180”,in a movement across the observer’s field of view to the observer’s view, thereby triggering an escape response away from the startle stimulus. Without the actor’s mobbing, the observer took 600 msec to takeoff, whereas with the actor’s mobbing preceding the sudden startle stimulus, response latency fell to 300 msec. This alerting effect of the actor occurred prior to its mobbing the owl, and thus was due to subtle signs of the actor’s incipient alert behavior. The benefit to the observer bird is considerable; with an accipiter hawk attacking at a speed of 65 km/hr, an unwarned blackbird would escape after 12 m of approach, an alerted one would have about 6 m, a meaningful difference. In another experiment by Frankenberg (1981), both the actor and the observer were allowed to perceive the startle stimulus, all other features of the experiment remaining the same (Section III,D,4,a). As a conse-
142
E. CURIO
: :
Front Lid
C
S t i mulus,
Observer l m
FIG.2. Experimental setup for testing the effect on the startle response of an observer blackbird of an actor blackbird’s mobbing that is induced by a little owl (Arhene nocruu) mount. Curtains (C) prevent the actor from seeing the startle stimulus visible to the observer and prevent the observer from spotting the owl. The actor’s mobbing is started by removal of the front lid. (Redrawn from Frankenberg, 1981.)
quence of this, the actor bird was found to show the same decrease of its response latency as did the observer. Hence, a blackbird’s own predator mobbing and/or being alerted facilitates its escape should the necessity arise. This is quite remarkable since the actor might have anticipated an attack from the owl, not the innocuous wooden lever, and yet its escape response was not compromised. Perhaps any conflict between an anticipated attack by the owl and the actual movement of the lever was offset by the bird continually monitoring the source of danger, whereas the observer could only infer a danger from the actor’s behavior. This possibility could be tested by scoring the actor’s latency upon an attack from the owl; one would expect it to decrease still further. There were mutual effects between the two blackbirds, one of which is reminiscent of Davis’s (1975) experiment with pigeons. After the observer took off on seeing the startle stimulus when it was hidden from the actor, the latter stopped mobbing, and after a latency averaging 3.9 sec took off itself. It later resumed mobbing and this induced the same response in the observer. The magnitude of its delay to takeoff contrasts with virtually no delay in the pigeons, perhaps due to the more social nature of the latter species. The impact of the observer’s startle response on the same response in the actor demonstrates unequivocally that a social influence
ASPECTS OF ANTIPREDATOR BEHAVIOR
143
overrode the effect of the unchanging enemy stimulus. The actor’s takeoff latency was about 13 times the observer’s when it responded to the startle stimulus (3.9 vs. 0.3 sec). This cautions against comparing the two takeoff responses directly. A startle stimulus may imply a real danger or an apparent danger. Discrimination between the two takes time, although there is no direct evidence for the tacit assumption that an artificial startle stimulus takes the same response time as does a biologically more meaningful stimulus pattern. If the startle stimulus persists and if, on closer examination, it turns out to involve a predatory threat, a typical startle response will give way to a different class of responses. These consist of predator exploration, mobbing, or attack behavior, depending on the species, past experience, and context (see also Andrew and Clayton, 1979; Clayton and Andrew, 1979). Depending on the time available for identification, one and the same innocuous stimulus may elicit a startle response when appearing suddenly, or be ignored if examined for some minimum period of time. Harmless flying birds like blackbirds or wood pigeons (Columbapalurnbus) triggered an aerial predator call in my silver pheasants (Lophuru n. nycrhemeru) when they suddenly came into view as they crossed the edge of a nearby roof. If flying individuals of the same two species were detected while approaching from a longer distance, giving the pheasants time for identification, those predator calls were produced much less often. The distinct avoidance by the pheasants of house walls may be regarded as a means to keep as large a section of the sky as possible under surveillance and thus forestall the surprise attack of raptors (E. Curio, unpublished). Similarly, carrion crows (Coruus corone) sent black-headed gulls (Larus ridibundus) into precipitous flight when appearing over the rim of a steep slope but were ignored when seen flying for longer (Kruuk, 1964). From these observations springs the hypothesis that greater opportunity for enemy identification is linked to fewer startle responses and, hence, to a lower rate of misidentifications. This idea is supported by yet another line of evidence. The threshold for startle responses is lowered and vigilance perhaps increases when the scope for surprise attack increases. Lohrl (1950b) found that marsh tits (Parus palustris) emitted aerial predator calls in foggy weather more often and to a broader range of flying birds (see also Ferguson, 1987). Furthermore, vigilance for predators increases under several conditions: 1. When the potential victim is closer to a site more liable to attacks (Lendrem, 1983). 2. When the potential victim is at the periphery of a flock, that is, in a
144
E. CURIO
more vulnerable position (Altmann, 1958; Goldman, 1980; Jennings and Evans, 1980; Prins and Iason, 1989). 3. When the potential victim is in a smaller flock (Lazarus, 1972; Bertram, 1980; Caraco et al., 1980; Hoogland, 1979). The detection time for a sudden stimulus is longer in smaller groups (Dimond and Lazarus, 1974: Quelea quelea; Magurran et al., 1985: Phoxinus phoxinus). Despite a decrease of the individual scanning rate with flock size, the corporate vigilance of the flock as a whole increases (Caraco, 1979). 4. When the potential victim has recently perceived a predator nearby (Caraco et al., 1980; Lendrem, 1980, 1984a,b; Poysa, 1987). In whitebrowed sparrow-weavers (Plocepasser mahali), Ferguson (1 987) found the individual scanning rate did not decrease with increasing flock size and that larger flocks attracted predators more often. This greater vulnerability of flocks is hypothesized to cancel the usual inverse relationship between vigilance and flock size. This raises the question why so many other species can afford to lower individual vigilance as flock size increases. Elgar (1989) lists a large number of confounding factors and calls for an experimental approach to the flock size-vigilance relationship. 5 . When the potential victim wears a conspicuous plumage as compared to other times of the year (Lendrem, 1983). 6. When the potential victim has a poor knowledge of its home range. The longer the period for which the home range has not been monitored for predators the more vigilant a bird is during a current episode of monitoring. When patrolling an area of our garden where they had not been for a long time, my silver pheasants were more on the alert, scanned more often, and bunched more closely together, especially the chicks before their independence (E. Curio, unpublished, 8 years of observations). Similarly, a nest-building blue tit (Parus caeruleus) spent more time in scanning for predators after longer absences from the nest box (Lendrem, 1980). The time scales over which this memory window works can apparently vary tremendously. The silver pheasants patrolled parts of their common home range at intervals of many days or even weeks; the blue tit’s nest visits were spaced apart by seconds or minutes. Given that the threshold for a startle response tends to vary as a function of context (see above), one would predict that startle responses should be commoner in less frequently visited parts of the home range. This idea has so far gone untested. 3. Novelty a . General. A stimulus will be called “novel” here if it fulfils two criteria: First, it elicits antipredator responses based on pattern recogni-
ASPECTS OF ANTIPREDATOR BEHAVIOR
145
tion, as opposed to the simple startle stimuli relying on mere conspicuousness (Section Il,A,2). The following qualify as such responses: concealment of self and offspring, mobbing, distraction displays, and attacking the predator. According to Ratner (1967), freezing should be included here too, though I think it is more common in response to startle stimuli. Second, the object is encountered for the first time in an individual’s lifetime. For the fear of novelty to work there must have been “previous encoding of the familiar” (Bronson, 1968). The research reported below fulfils this criterion since the birds under study have in no case been deprived of patterned stimulation (about the value of restricted deprivation see Section 111,A). Sometimes objects fitting the first criterion have been called “strange,” especially if a response could be triggered by some dummy that, at first glance, bore little resemblance to a real predator. However, the term has never been operationally defined and, on closer inspection of the examples that have been quoted, novelty could not be ruled out as a sufficient explanation, and/or failure to match in all respects a true enemy stimulus pattern could not be ruled out either. Here I therefore examine whether either novelty or enemy-specific cues are sufficient for analyzing the information content encoded in the objects triggering antipredator behavior. A discussion of the role of novelty in shaping the development of antipredator responses and the processes underlying it will be deferred to Section III,B and II1,C. b. The Stimulus Effectiveness of Novel Objects. Objects tested for the effect of novelty fall largely into two classes. In order to know whether only predators elicit protective behavior in their prey, novel nonpredatory species have been tested and compared to predator species of the same class of vertebrates. Novel objects should ideally not contain any key stimuli that are known to be features of sympatric enemies. Novelty was ensured by picking similar-sized species that live in allopatry with the species to be tested. Kaspar Hausers deprived of any experience with heterospecifics have been used to test for the effectiveness of any species, both harmful and harmless. This potentially very powerful technique depends on having excellent raising and maintenance skills (e.g., Schleidt, 1964). The other class of stimuli comprise artificial, inanimate objects that are as dissimilar as possible to the range of objects in the natural world of the species to be tested. Such stimuli could be used to test if novelty per se were effective. Studies using both types of stimulus are illustrated in Fig. 3. Of the two studies with captives (b and c), one was validated by comparing the responses of caged birds to nesting ones in the wild (c). As can be seen,
20
0
80
60
LO
100% Q
C
era^ Pigeon
A
m
, 0
,
, 20
,
, LO
,
, 60
,
, 80
,
, 100 %
FIG.3. Relative stimulus value of objects that differ in naturalness and/or predatory threat t o pied flycatcher (a), European blackbird (b), both in Germany, and small ground finch (Geospizafuliginosa),on Santa Cruz Island in the Galapagos (c). Stimulus value is expressed as a percentage of the maximally effective predator stimulus known in experimentally naive birds. Stimulus presentations in b and c involved an initial movement of the dummy. either horizontally or upward above a screen, respectively. In a, dummies were presented stationary in front of the nest hole. All stimulus values within species are significantly different. [Based on data in Curio, 1975 (a). Curio, 1969 (c); and Curio et a / . , 1978a (b).]
ASPECTS OF ANTIPREDATOR BEHAVIOR
147
a stuffed novel bird (Coracias garrulus in a, Philemon corniculatus in b, a long-billed Columba livia var. domestica in c) elicits invariably weaker, though qualitatively identical, responses compared with those to genuine natural predators, that were likewise presented as mounts. Results parallel to c were also obtained with two other island forms of Darwin's finches (Geospiza d$jcilis). All three island forms, including Geospiza fuliginosu from Santa Cruz Island, had not seen Galapagos hawks (Buteo galapagoensis) before, though G . fuliginosa had existed in sympatry with this predator until recently (Curio, 1969). Analogous results, supporting the hypothesis of greater response to the predator, have been obtained with nesting great tits (Parus major) tested with live exemplars of stimuli (two owl species and a sparrow hawk Accipiter nisus [Curio et al., 19831 vs. cockatiel Nymphicus hollandicus [W. Fleuster, unpublished results]. See also Toenhardt, 1935: many German woodland birds; von St. Paul, 1948: Lanius collurio, L . senator; Scaife, 1976a: Gallus gallus var. domesticus; Galloway, 1970: Cinclodes antarcticus; Kobayashi, 1987: Eutamias sibiricus). A puzzling exception is the Falkland thrush (Turdusf. fulcklandii) which treated both a control rubber snake and a stuffed cat with little fear but survived attacks from introduced cats and rats much better than the tussock-bird (Cinclodes) despite the latter's more sophisticated enemy recognition (Galloway, 1970).Perhaps the measure of avoidance used, attendance times at afeeder with a dummy, was inappropriate. Furthermore, for unknown reasons the bullfinches (Pyrrhula pyrrhula) of Kramer and von St. Paul (1951) did not differentiate between raptors and harmless species, although both of these stimulus classes elicited more response than clearly novel inanimate objects. With the exception of the studies in the wild (great tit and other woodland and Falkland Island birds; part of the Eutamias study), all the animals mentioned above were predator-naive when tested. In two cases, the novel harmless bird was larger than the predator species. Therefore body size alone cannot explain the superiority of the latter, but is known to enhance responsivity: Pied flycatchers mob a red-backed shrike significantly less (Fig. 3a) when it is half the normal size (Curio, 1975; see also Geospiza, Section II,A,4,a; and Kramer and von St. Paul, 1951). Likewise, the superiority of the predator compared to novel birds cannot be explained by novelty per se, as the predator was of the same novelty (Fig. 3c and a large fraction of birds yielding the same stimulus values for both stimuli in Fig. 3a), or this was very likely (Fig. 3b). This conclusion touches on the hawk-goose controversy sparked off by Lorenz in Tinbergen (1951), a discussion of which is deferred to Section III,B. In view of the disproportionately large number of harmless bird species as opposed to predatory ones living in sympatry with prey birds, any
148
E. CURIO
control for the efficacy of the raptor stimulus pattern must logically remain open-ended. However, the evidence supporting the hypothesis of a perceptual mechanism encoding rather predator-specific patterns of information is strong. Controlled experiments involving songbirds of different bird taxa (Furnariidae, Muscicapinae, Turdinae, Geospizinae, Paridae, Laniidae, Phasianidae) and a mammal (Sciuridae) have established the superiority of at least one predator stimulus pattern over mere novelty. The basis seems to be some innate releasing mechanism evolved during periods of sympatry with the predator under consideration. An alternative explanation proposing that enemy recognition in these taxa is due to experience with the predator under consideration can be dismissed in a number of cases: these involve tests with animals known to be predator-naive either because they are “natural Kaspar Hausers” living allopatrically from certain predators (Geospizinae, Muscicapinae), or because they have been hand-raised (Laniidae, Muscicapinae, Phasianidae, Sciuridae), as is discussed more fully below (Section III,A,2). The moderate effectiveness of novel harmless birds raises the question of whether all novel objects possess properties apt to elicit protective behavior. To control for the “animal nature” of the novel bird stimuli employed, inanimate objects were presented to experimentally naive birds (Fig. 3b,c). These objects have a lower stimulus value than novel birds, though it is still above zero. To the inanimate objects shown in Fig. 3 can be added the effect of an empty cage on nesting great tits (Curio, 1989). The clearly intermediate nature of novel birds permits us to categorize them as a stimulus class sui generis. In the pied flycatcher various incomplete shrike dummies have a stimulus value of zero and therefore probably qualify as effectively inanimate (e.g., Fig. 3a; Curio, 1975: Fig. 22). Other studies have also found an extremely low stimulus value of novel inanimate objects as compared to the predator but have failed to look for the relative effectiveness of novel harmless species (e.g.; Galloway, 1972; but see Galloway, 1970). The almost total ineffectiveness of these zero value stimuli raises the question of whether they are decoded in a way different from equally novel, harmless but “animate” objects or their live counterparts. A working hypothesis is as follows: For a subject to identify a thing as “bird” it must fulfil minimal requirements in terms of naturalness, for example, have an upright rather than an inverted posture (Fig. 3a), and of surface texture, color pattern, and so on. Thereafter more specific stimulus properties are decoded. This would suggest that birds decode objects in a sequential way: first, a categorization into inanimate versus animate; second, a categorization within each of these classes, for example, bird versus mammal, then, within birds, harmless bird versus raptor, etc. At each
ASPECTS OF ANTIPREDATOR BEHAVIOR
149
level of this sequence of perceptual events different key stimuli would be required (see also Section II,A,6,d). Differences of releasing value among inanimate novel objects may be due to stimulus pattern complexity. A multicolored plastic bottle ranks next to a honeyeater (Fig. 3b), yet a wooden box used to bring either of these two stimuli into view of the subjects and moved the same way ranks lower (Curio et al., 1978a). The findings on novelty have important implications for our understanding of fear responses if one accepts that a potential or real danger activates a motivational system termed fear. In an influential review, Bronson (1968) advocated the view that all fear responses can be related to degrees of novelty. Accordingly, maximum fear is seen as elicited by “absolute novelty.” In a perceptive critique of this novelty theory, Murphy (1978) found the concepts of fear and the related one of exploration ill-defined. She did not question the feasibility of ranking all stimuli along one novelty dimension. However, she hinted at the problem that, for example, the change of the animal from one environment (cage) to another new one inhibited responses that the reciprocal change did not, that is, when the new environment was made to be the familiar and the familiar the new one. The protective responses reported here demonstrate further that the unidimensionality of the novelty theory is untenable. Given the same “absolute” degree of novelty, objects fall into at least two, if not three classes of pattern quality, as measured by response strength. A description of the corresponding stimulus-response contingencies in terms of merely one stimulus dimension would miss most important aspects of protective behavior. Two puzzling aspects of response to novelty have received merely passing attention. First, some European woodland birds have been observed vigorously mobbing nonpredatory objects like a live death’s-head hawk moth (Acherontia atropos) caterpillar (Meinertzhagen, 1959) and models of a scorpion, but not a lizard, on a bird table (Meinertzhagen, 1955). Although not controlled, these observations should be followed up experimentally. They may suggest that, apart from the object categories mentioned above, there are more. There may be cultural transmission of aversion to particular food objects via mobbing (cf. Rothschild and Lane, 1960). Second, Heinroth (1917) and Heinroth and Heinroth (1924-1934) first described the fact that many captive birds respond by panicking when seeing certain colors. More examples came to light later (Koenig, 1951: Merops apiaster; Sauer, 1954: Sylvia communis). A closer analysis of these fear responses would also have to include a consideration of UV patterns. These are now known to play a vital role in the recognition by many birds of plumage patterns, flowers, and fruit (Burkhardt, 1990).
I50
E. CURIO
4. Predator K e y Stimuli: Identification and Properties
a . Localized versus Diffuse Key Stimuli. The plumage pattern of the red-backed shrike male is conspicuous from a long distance. This pattern, not the feathering, is all-important since a plain plastic model is as effective as a stuffed mount in eliciting mobbing by pied flycatchers. Removal of the conspicuous eye stripe (including the equally dark eye) renders the model almost ineffective (Fig. 4a,b). The same happens if, in another experiment, one removes the whole color pattern except for the black bar (Fig. 4c). These changes of the whole pattern demonstrate that both the eye stripe and the “rest” of the shrike’s pattern are localized key stimuli or contain such stimuli. The two pattern components must combine in the receiver to yield the full response. A green or red eye stripe is much less effective than the natural black one (Curio, 1975, Fig. 21). Therefore, it came as a surprise that a reversal of contrast of the eye bar-only pattern (Fig. 4d) lowers the response to about the same level. This seems to indicate that a black-white contrast of either sign is somewhat effective but falls short of the composite natural pattern. In another experiment, it was shown that only a bar aligned with the beak will do: other locations-and another orientation-of the bar are virtually ineffective (Fig. 5 ) . To examine if the eye stripe operates in. an all or none fashion, various shades from jet black to light grey, the color of the head, were tried (Fig. 6). This last model is the same as that in Fig. 4b. As the contrast between the stripe and the rest of head declines, stimulus efficacy falls in parallel. Hence, the eye stripe is a key stimulus that is allowed to vary in intensity, including a concomitant change in response strength. Conversely, if the rest of head is made to vary from white to black with the eye stripe held constant (Ostwald gray level p), there is little if any change in stimulus value as long as there is a minimum of contrast (Curio, 1975, Fig. 25). Taken together, these dummy experiments suggest that almost any deviation from the male shrike’s natural pattern is inferior to it. That the red-backed shrike female also represents an inferior pattern will become the starting point of a new perspective on releasing mechanisms (Section II,A,6). As well as the red-backed shrike, owls provide an example of a localized key stimulus for enemy recognition. Whereas pied flycatchers still recognize an owl whose yellow eyes have been changed to same-colored, convex triangles (Fig. 7 a,b), they fail to do so when the number of eyes has been reduced to one (Fig. 7c). The slight though nonsignificant increase of stimulus value with a further reduction of eye number to zero (Fig. 7d) might be due to the restoration of bilateral symmetry. From these comparisons, it follows that the presence rather than the shape of eyes is
I51
ASPECTS OF ANTIPREDATOR BEHAVIOR
0
50
100 *I.
I
I
I
93
31
P
I n. s I
10
1
d
9
FIG.4. The stimulus effect ( = median value) of the eye stripe of the red-backed \hrike. its presence and the sign of its contrast in the pied flycatcher. Numbers below bars denote sample sizes of experimentally naive birds. Any one of stimulus values b-d is statistically different from a. (Redrawn from Curio. 1975.)
crucial for owl recognition (see also Inglis et al., 1983). The breakdown of recognition due to the elimination of one eye suggests two things: (a) Two eyes act as a configural or Gestalt stimulus. The alternative explanation, that eyes add up by each contributing a certain stimulus value, can be dismissed: the one-eyed owl should then have about half the stimulus value of the intact owl. (b) Like the red-backed shrike's eye stripe, the eyes of the owl combine in the receiver, that is, display coaction with the rest of the owl to produce the full response. In other species, eye color has been alleged to affect responsiveness (Kerlinger and Lehrer, 1982; Inglis et al., 1983), but luminance and/or contrast with the background could have been the relevant cues. In an
I52
E. CURIO 50 I
0 I
61
100 *I.
1
1
P = .904
I 21
C
I 08
I 19
I 20
FIG.5. The stimulus effect of the position and orientation of the black eye stripe of the red-backed shrike on the pied flycatcher. P is based on a two-tailed Mann Whitney U-test. Other conventions are as in Fig. 4. (Redrawn from Curio, 1975.)
iguana, eye size was found to be important (Burger er ul., 1991). More importantly, Coss ( 1978a, 1979) demonstrated in jewelfish (Hemichromis bimaculurus) and in primates (Coss, 1970, 1978b),and Jones (1980)in chickens, that two horizontally oriented facing eyes are superior to one, three, or four eyes or unnatural orientations. This again supports the configurational
153
ASPECTS OF ANTIPREDATOR BEHAVlOR
p-!?
.,‘
0
50
100 m.i
I
I
1
I
61 0
W‘15
Ok h \ 20
c
I
P = ,031 8
FIG.6. The stimulus effect of the shade of the eye stripe p-d (scored after Ostwald) in otherwise unchanged red-backed shrike models. Conventions as in Fig. 4. (Redrawn from Curio, 1975.)
stimulus idea, contrary to the idea of simple stimulus summation (see also Karplus and Algom, 1981). In a most penetrating analysis, Inglis et cil. (1983) found in starlings (Sturnus uufgaris) that two eyes were slightly superior to three eyes only when surrounded by a simple head outline; otherwise, the reverse was true, which is perhaps an artifact. Strangely, changing the orientation of a pair of eyes from horizontal to vertical only slightly reduced their aversiveness. This finding differs from all previous ones, and what Inglis et a f . (1983) call “inconsistencies” among different studies could well be species differences. Despite the functional similarity of their role in relation to the whole enemy Gestalt, the eyes appear to differ markedly from the eye stripe.
154
E. CURIO
I
73
I
I
1
0
50 100 % FIG.7. The stimulus effect of the shape and the number of eyes in a mounted pygmy owl (Claucidictm posscrinum) on pied flycatchers with nestlings. (a) Normal mount: (b) Perspex eyes of natural coloration and near to natural gloss and “corneal” curvature: (c) one eye; (d) both eyes covered with tiny chicken feathers resembling the face color (conventions as in Fig. 4). (Redrawn from Curio. 1975: courtesy of Academic Press. London.)
When presented in isolation, the black bar fails to elicit any response; it does not even have any effect when presented on an oblique wooden dowel the size of a shrike (Curio, 1975; Fig. 22). The owl’s eyes alone have not been tried on the pied flycatcher, but Scaife (l976b) presented a pair of yellow glass eyes to naive domestic chicks and elicited avoidance responses as strong as those given to a stuffed kestrel (Fulco tinnr4nculus). The Gestalt of the eye or eyes may be, due to their intrinsic structuring. a much more powerful aversive stimulus than is the eye stripe (see also Section III,D,3). Similarly, Gallup et al. (1971) found in young chickens that isolated glass eyes prolonged tonic immobility, an antipredator response. From this the authors erroneously concluded that the stimulus effect of simulated eyes is “contextually independent of other facial and/or bodily features of potential predators” (p. 80). All that the study showed is that simulated eyes suf$ce to bring about immobility rather than that there is no coaction with other stimuli which are part of the whole predator. In view of the universality of owl recognition in potential owl victims, the question arises whether the key stimuli used to decode the owl pattern
155
ASPECTS OF ANTIPREDATOR BEHAVIOR
are the same across species (Curio, 1963). The general answer is no, but it deserves qualification. On the Galapagos, where the short-eared owl preys partly on Darwin’s finches, the eyes possess virtually no releasing value when examined on the entire owl (Fig. 8A). Note that this is the way the owl’s eyes were examined in pied flycatchers. If, however, the owl’s head is presented alone, the eyes exert a dramatic effect (Fig. 8B); their elimination renders the head virtually ineffective (see also Smith and Graves, 1978). The finches on Wenman Island are owl-naive but the same effect as in Fig. 8 can be found, though less strongly, on other islands where the owl is a real threat (Curio, 1969). From the experiments on the Galapagos it follows (a) that the role of the owl’s eyes in decoding the owl is not universal, and (b) that, again, the eyes interact with the “rest of the owl” pattern, yet in a way that differs as a direct consequence of (a). For Geospiza, the eyes are a dispensable key stimulus, for Ficedula they are indispensable. The manner of interaction of
1
1
1
I
20 40 60 80 100 % FIG.8. The stimulus value (arithmetic mean) of the eyes depends on the “rest” of the compound stimulus representing an entire owl (A) or its head (B). Results are for the sharpbeaked ground finch (Ceospizo c/ij$ci/is sc.prc,,ir~iorio/is) of Wenman Island/Galapagos. The stimulus value of the eye-less owl is not significantly less than for the unaltered owl. (Redrawn from Curio, 1969; courtesy of Parey, Berlin, Hamburg.)
0
156
E. CURIO
the eyes with the rest of the owl pattern is perhaps different in the two cases. One might propose that the amount of stimulation by a diffuse key stimulus surrounding the eyes of Asio is the key for both an understanding of their different effect when on the owl as opposed to only on its head and their different effects in the two species. The greater the quantity of a hypothetical diffuse stimulus (e.g., the mottled plumage pattern) surrounding the eyes, the less the finch attends to them. Accordingly, key stimuli would compete for attention and the more there is of one the less effective is another. In this view, the eyes would be indispensable in Ficedula because the surface area of the pygmy owl is absolutely smaller than that of Asio and comparable to the latter’s head. To test this idea, different amounts of mottled plumage were presented to a Darwin’s finch species on Genovesa (Fig. 9). Although the models tested also differed in other details from one another, the resulting stimulus values appear to confirm the prediction: The strength of response increases with the amount of a diffuse key stimulus, in this case, the amount of mottled owl pattern seen. This then would support the competition-forattention hypothesis of compound stimuli put forward above. If true, it would furnish another example of stimulus summation in the broad sense.
L
I
1
100 O h FIG. 9. The stimulus effect of three owl (Asio flammeus) dummies differing largely in the amount of mottled plumage visible to sharp-beaked ground finch (Geospiza difJicilis acurirosrris) subjects on Genovesa (Tower Island) Galapagos (from data in Curio, 1969). Eyes were concealed by neck feathers. Stimulus values (arithmetic means) did not differ significantly from dummy on top.
0
50
ASPECTS OF ANTIPREDATOR BEHAVIOR
157
There must be other key stimuli at work (see also Hartley. 1950). The entire, intact enemy Gestalt must encode features above and beyond this size-of-stimulus effect. A pygmy owl, a species not found in the Galapagos, elicits on Genovesa the same response as does the much larger short-eared owl. On Santa Cruz, the pygmy owl is markedly less effective. Even when seeing only the pygmy owl’s back, the finches on Genovesa still respond about as strongly as when seeing its front (Curio, 1969). Although this latter finding would be in line with the minute effect of the owl’s eyes within the intact owl (see Fig. 8) the lack of size dependence in the Genovesa finch, as compared to birds on Santa Cruz. is difficult to explain. Hence, the size-of-stimulus effect does not appear to be a universal explanation of the decoding rule for diffuse key stimuli, but more work is necessary to eliminate possibly confounding features of the owl as a whole. b. Rules of Stimulus Coaction. In no case has the coaction of key stimuli obeyed any simple rule of algebraic summation as was envisaged by the early proponents of the rule of heterogeneous summation. Indeed, such summation seems to be the exception rather than the rule. A neat example is provided by Leong (1969) and Heiligenberg et a / . (1972). but a closer look at one of the two localized key stimuli involved demonstrated the existence of multiplicative processes as well (see below). The analysis of some of the key stimuli involved in the recognition of the perched avian predator follows rules implying multiplicative processes. The eye stripe of the red-backed male shrike yields, when superimposed on the rest of the pattern, the full response. Both stimuli when presented alone on the proper shrike shape are almost ineffective. Hence, their coaction on the natural shrike Gestalt obeys a rule of stimirlus dilation, by which the whole yields more than the sum of its component pattern parts. The same would apply to the owl’s eyes and the rest of the owl (Ficedirla) or that of its head (Geospiza).For a diagrammatic representation see Fig. 10. This effect is so pronounced that it is obvious even without statistical treatment. Yet, Baerends and Drent (1982) contend that the effect is not “proven” rigorously. Unfortunately, they do not give the reasons for their critical stance. They also misquote my paper (Curio, 1975) by calling the opposite effect (see below) response dilation when they mean stimulus compression. By contrast, the opposite type of coaction of key stimuli operates when separate key stimuli are so effective that their combination theoretically exceeds the value of the whole. Therefore a form of stimulus compression must apply (Fig. 10).(The alternative, banal explanation of a “ceiling effect” [= efferent saturation] can be ruled out.) This is the case with parts of the owl and the hawk in Darwin’s finches. In the pied flycatcher it has not been looked for. Both types of coaction can be modeled by various algorithms of
158
E. CURIO
*I.
a
b
C
100 5 L
C m
u
L
In
50 C
0
n
m u
a 0
A
A + B >AB
+ B
A
+ B
=AB
I
A+B*
AB
FIG.10. Coaction of sign stimuli A and B when being combined in a compound stimulus AB: Stimulus dilation (a), stimulus compression (b), and pure algebraic stimulus summation (c), the last being the apparent exception.
weighted summation (Curio, 1975). It is not possible to decide between them as yet. Basically, the same principle of weighted summation was also found to govern the social attack response of a cichlid (Heiligenbert, 1976) and the egg-retrieval response of the herring gull (Larus argentatus) (Baerends and Drent, 1982). In the latter case, the most detailed stimulus analysis to date, three key stimuli, egg shape, color, and speckling all add up in some way to increase stimulus value, but in interaction with egg size. A detailed comparison of the gull study with my work on enemy recognition would be extremely rewarding but transcends the scope of the present review. Heiligenberg (1976) presented a mathematical algorithm describing the coaction of two key stimuli but was cautious enough to point out that the model is valid only in terms of an arbitrarily chosen response score. A basically similar notion of weighted summation was expressed by Margolis et al. (1987) working with the pecking response in laughing gull (Ltrr-its ( i t r k i k i ) chicks, although they apparently overlooked previous work in arrivingat this conclusion. They redefine the rule of heterogeneous summation to encompass "synergistic." that is, multiplicative processes of stimulus interaction, which is exactly what weighted summation means. In doing so, they incorrectly criticize Seitz (1940/ 19411, the originator of the concept of heterogeneous summation, for failing to take account of multiplicative, as opposed to purely additive, processes of perception, for two reasons.' First, Seitz left out synergistic effects of interactions be-
'
Incidentally. Margolis 1'1 d.(1987) reiterated an incorrect year of publication for Seitz's paper (1941). an error that has permeated the literature since an unidentified erroneous quotation.
ASPECTS OF ANTlPREDATOR BEHAVIOR
159
tween stimuli from his rule. However, he had not formulated the rule quantitatively and he emphasized the importance of such effects by stressing the importance of “complex qualities.” Both his recording technique and his nonmathematical formulation of stimuli “summing up” leave room for effects other than pure summation. Because of this, the observation by Margolis et al. that, for pure summation to occur the relationship between stimulus value and response must be linear, is correct, but it offers no critique of Seitz’s rule. Furthermore, their observation is not new (cf. Curio et ul., 1969; Curio, 1969. 1975; Baerends and Drent, 1982). Second, a basal rate of responding in the absence of external stimulation would lead response measurements to be inflated. Because few behavioral acts of animals exhibit this degree of spontaneity (vacuum activities). and the fighting and courtship of cichlids studied by Seitz (1940/1941)are not among these, this critique is rather unimportant. Also, many of the predator models discussed above were found to have a stimulus value of zero (e.g., Figs. 6, 7; Curio, 1975). It is perhaps no coincidence that the rule of stimulus compression has been found when the predator has been split into various component parts. A functional explanation may be that it pays a prey to discharge the (almost) full-blown antipredator response when it perceives merely part of the whole: the latter is always a reliable sign for the presence of the predator. By contrast, if incomplete predator patterns, for example, a black eye stripe which also occurs on an innocuous passerine, were to elicit alarm, many false alarms would occur and energy would be wasted. The encoding of a complex quality, as in stimulus dilation, seems to safeguard the prey against these errors; a complex pattern is hard to mimic (see also Section II,A,6). c. The Unclassijiable Risk Hypothesis. Great tits with nestlings learn to respond by approaching and mobbing an artificial 800 Hz tone patterned like the song of one of their predators, the pygmy owl. For learning to occur the sound is paired with a live pygmy owl and a taped mixed species mobbing chorus including great tits (Curio et al., 1978b). If the owl is omitted during conditioning, significantly fewer birds (47 vs. 79%) approach and mob the speaker in the test. However, there is no difference when approach is the only measure used (73%). Viewed traditionally, the reduced incidence of mobbing with no visual reinforcer might result from the smaller sum of reinforcing stimuli. Alternatively, as mobbing of predators is dangerous (refs. in Curio and Regelmann, 1985), the tits might remember that no predator could be located and identified, introducing an “unclassifiable risk.” That there is a risk can be inferred by the tits from the mobbing chorus signaling some predator. Response scores other than those mentioned support the latter hypothesis. Tits conditioned with the owl average only 4 sec to fly to the speaker,
160
E. CURIO
whereas those that had not seen a predator take significantly longer, namely, a mean of 71 sec. Birds that fail to locate a predator during learning, in the experiment with no visual reinforcer, may remember an unclassifiable risk. As a result, they hesitate before approaching the sound source and mob less. An experiment with a different visual reinforcer (a live cat) and the behavior of birds that did see a predator during learning supports the unclassifiable risk hypothesis (Curio, 1979). Risk is a functional concept. Explanations based on it are necessarily functional too. In the present case, the unclassifiable risk idea inspired experiments to unravel the mechanisms underlying risk assessment and its use in the learned response (E. Curio, unpublished). 5 . Are There Supernormal Predator Key Stimuli? The gradation of certain key stimuli such as the red-backed shrike’s body size, or the shade of its eye stripe (Fig. 6) or head, raises the question of whether they can be exaggerated beyond what is normal. For the shading of the head the answer is no (Section II,A,4,a), and shading of the eye stripe is saturated already. Other results were negative, too. For example, a red-backed shrike model has been fitted, to no effect, with a black beak resembling a snipe’s, thereby extending the eye stripe substantially in length (Curio, 1975: Fig. 35). However, the stimulus change may have had another effect, interfering with shrike recognition rather than enhancing it. Body size is another possibility but the range of dangerous predator sizes is limited for each prey size class. For reasons of prey profitability to predators, small prey should not fear the largest predators; there is evidence for this in birds (Curio, 1963). In general, releasing mechanisms underlying enemy recognition should have an upper bound for all key stimuli; above this responses would be too costly because of a net benefit of zero. For this reason, supernormality of predator stimuli should be rare as compared to the many supernormal releasers in the social domain (Tinbergen, 1951; refs. in Baerends and Drent, 1982; Inglis and Isaacson, 1984). Perceptual correlates of stimuli from conspecifics need no precise upper bound. Here, many constraints would appear to obstruct the evolution of stimulus exaggeration. The same reasoning may apply to brood parasites as well, since they are constrained in their body size for reasons of successfully victimizing their hosts. Hence, it would be rewarding to see if the recognition of brood parasites could be fooled by supernormal key stimuli. 6 . The Multichannel Organization of Enemy Recognition a . Znfroducrion. In the pied flycatcher, shrikes and small owls stimulate about an equally large part of the retina when seen from the same distance
161
ASPECTS OF ANTIPREDATOR BEHAVIOR
as in the dummy experiments. In both cases, shape, spatial orientation, and intrinsic patterning are important for the protective response to occur, while movement is not (Section II,A,4). Yet, the particular nature of the compound patterns requires different decoding processes subserving the underlying releasing mechanisms (RMs). In either predator, the lack of key stimuli from the other could be compensated for by the presence of its own stimuli, as predicted by the “law of heterogeneous summation.” According to this view, both enemies would be decoded by one very general RM (Fig. 1 l ) , triggering an identical motor pattern system. However, several observations tend to cast doubt on such a view. (a) The many harmless species cooccurring with the pied flycatcher on its breeding grounds do not elicit the response, despite the fact that some of these species share external features with shrikes or owls (e.g., Certhia, Sitra). (b) Similarly, the red-backed shrike female that combines an owl-like mottled color pattern with genuine shrike stimuli elicits only one-third of the response given to the male (Curio, 1975). Points a and b are best explained by some interaction of predator key stimuli (Section II,A,4,b), and this in turn would seem to restrict the free interchangeability of sign stimuli suggested by model I. (c) Only when painted on a generalized
shYl‘ Shrike
or
Owl
rhrlk., owl
Mobbing response
I
Mobbing response
n
FIG. 11. Flow diagram representing two hypotheses about the decoding of a shrike or an owl by one general releasing mechanism (RM) (model I ) as opposed to two specialized RMs (model 11) in the pied flycatcher. The geometrical relations of and between control units are arbitrary. E’, E , E”‘, The effectors used in the mobbing response. (From Curio, 1975; courtesy of Academic Press, London.)
162
E. CURIO
non-owl bird shape, encompassing the shrike but not the owl, could novel, non-shrike color patterns lead t o moderate mobbing (e.g., Figs. 3, 4). As an alternative to model I, one can suppose that each predator is decoded by a separate RM (Fig. 1 1, model 11). Only after decoding has taken place will afferent pathways of the two RMs converge at a common control unit where the motor command for mobbing is activated. Model 11, henceforth called the “two-channel hypothesis,” would be banal if both the shrike and the owl stimulus were conditioned stimuli. However, both stimuli are recognized independent of individual experience with these enemies (Section III,A,2). Therefore model I1 must now be carefully examined. b. Mixtures of Heterospec$c K e y Stimuli a s Stimulus Situations. All key stimuli identified so far do enhance the releasing value of the respective enemy models. The rationale behind mixing heterospecific sign stimuli therefore is that if one general predator RM were operating (model I), stimulus combinations should be found that provoke more response than either of the two “donors,” that is, owl or shrike. These hybrid stimuli should sum up heterogeneously. Such stimulus mixtures would lead to no gain of response strength, or even to a loss of the original releasing valuejf more than just one RM would have to be invoked (model 11). The failure of the female red-backed shrike to elicit the (full) shrike response (see above) may serve as a natural experiment that will now be more fully explored. To this end “owl-shrikes’’ and “shrike-owls’’ were designed, that is, models of one predator type were given highly effective key stimuli of the other. In one experiment, the male red-backed shrike pattern was provided with the extremely potent pygmy owl eyes in a place where the live shrike has its inconspicuous (hidden) eyes. This rather obvious change leaves the stimulus value of the shrike model completely unchanged (Fig. 12 a,b). This result would seem to challenge model I, as this would have predicted summation to occur. However, before this experiment is accepted a s support of the two-channel hypothesis (model 11) two objections must be dealt with. First, the stimulus value of the shrike “host” may not permit the owl eyes to exert their effect because it is already approaching the range of efferent saturation and this may prevent any potential gain of response strength. Therefore, a shrike model of less stimulus efficacy, one with a reduced facial mask contrast, was enriched with the owl’s eyes (Fig. 12c,d). Again, the owl’s eyes leave the effectiveness of the original shrike model unchanged, thus doing away with the explanation in terms of efferent saturation; the difference between the less effective shrike model and the effect of the most potent stimuli amounts to 33% and would thus have left room for the response to increase. Second, a bird harassing the owl-shrike will have a view of both owl
I63
ASPECTS OF ANTIPREDATOR BEHAVIOR 0
I
20 I
40
60
80
1
I
1
100 *f.
1
FIG. 12. Stimulus values of stimulus mixtures obtained by variously adding the pygmy owl’s eyes to the male red-backed shrike pattern: only heads are shown. Pied flycatchers with nestlings were subjects (conventions as in Fig. 4). (a) Standard male red-backed shrike model; (b) like a but with bilateral insertion of owl’s eyes; (c) like a with shade of the eye stripe reduced (Ostwald k); (d) like c but with owl’s eyes as in b: (e) like b but with owl’s eyes inserted into only one side of the shrike facial mask: ( f ) like e with reduced shade of the eye stripe as in c. Conventions as in Figs. 4 and 5 . (Modified from Curio, 1975.)
eyes at the same time in only two positions, that is, when looking at the model from the front or from the rear. In order to mimic properly the twoeye feature of an owl’s face (Fig. 7), the two eyes were inserted into a slightly lengthened eye stripe on one side of the optimal model, with their horizontal alignment maintained (Fig. 12e). Because of the first objection, that is, efferent saturation, this experiment was repeated with the reduced facial mask model (Fig. 12f). Like experiments c and d with bilateral eyes, the outcome of both experiments tends to support the two-channel hypothesis of model I1 in that the owl eyes are not evaluated in a donorrelated way; if anything, they tend to disrupt the effect of the shrike pattern (Fig. 12f). The same overall conclusion is attained when shrike models are employed in which the owl eyes do not disrupt the eye stripe. In all
164
E. CURIO
cases, the owl eyes interfere with the shrike pattern as a whole (Curio, 1975). They only seem to enhance the releasing value of otherwise ineffective dummies, and then merely up to a level typical of novel birds as defined above (Section II,A,3,b). Further experiments in which shrike-owls were employed, that is, owl models which were painted to look like a red-backed shrike male, yielded basically the same results. The key stimuli of both enemies interfered with one another throughout these tests, thereby supporting again the twochannel hypothesis to the exclusion of model I. It was also found that otherwise ineffective owl dummies gained in stimulus value up to the level of intermediate responses typical of those to novel birds. Since there is no hint that the response to novel bird dummies entails decoding processes called forth by either predator, a separate afferent channel from the ones envisaged so far is postulated. This “novel-bird RM” is not only characterized by its decidedly low level of response but also by the way in which it is affected by the presence of eyes. While a shrike model like the one in Fig. 12d and f is not enhanced by the presence of owl eyes and is therefore best regarded as an “incomplete shrike,” the eyes do enhance other models of the songbird type and the owl type that otherwise have a value near zero (Curio, 1975). In this way, novel birds can be operationally distinguished from either of the two predators. On the basis of these conclusions an explanation can now be advanced for the failure of the red-backed shrike female to elicit the full shrike response. Since features of both predators do not effectively mix and the shrike female combines some of both (see above), it functions as a novel bird as do various owl-shrikes. The functional independence of a shrike channel and a novel-bird channel is also supported by a lack of intraindividual correlation of responses to the male and female red-backed shrikes. The failure of hybrid stimuli to elicit a response, because there is no effective stimulus mixing, seems a logical consequence of the earlier result that there is tight interaction of the key stimuli of each predator (Section II,A,4,b). This failure corroborates the prevalence of stimulus interaction. In functional terms, the tight interaction safeguards the prey bird against confusing a harmless bird with either predator. A linear summation of key stimuli would fail to do this. c. The Identical Change of the Sume Key Stimuli in Both Predutors. The differential evaluation of one and the same physical property in novel birds and in predators inspired an experiment in which a feature shared by both owls and shrikes was altered. Defeathering of either enemy shows that feathers are not a detectable key stimulus in the shrike male but are an indispensable one in the pygmy owl (Fig. 13). Provided that exactly the “same” structure was changed in both cases, the result again
165
ASPECTS OF ANTIPREDATOR BEHAVIOR
0
50
r
1
100 *I.
1
48
I
38
FIG. 13. The influence of the presence of plumage on the recognition by pied flycatchers of the male red-backed shrike as opposed to the pygmy owl. The figures under the bars are numbers of individuals; conventions as in Fig. 4. The only significant difference is that between the two owl models. (From Curio, 1975; courtesy of Academic Press, London.)
supports the two-channel hypothesis. Sameness is judged here in physical terms, not in terms of perception; otherwise the argument would be circular. Stimuli external to the model they are intended to alter are a better means of manipulation. A red ball closely juxtaposed beside either of the enemies leads to a deterioration of the effect of the owl but leaves the effect of the shrike unchanged. This again appears to support the twochannel hypothesis of owllshrike recognition (Curio, 1975). Interestingly, von St. Paul (1948) could, by this method, differentiate between the recognition of Accipiter hawks and owls by hand-raised red-backed shrikes. The attachment of a “snipe beak” impaired recognition of hawks but not owls, suggesting two respective channels tuned analogously to these types of predators.
166
E. CURIO
d . The Stimulus-Specijic Habituation of the Responses to Both PredaThe functional independence of the two envisaged predator channels predicts that habituation to either of the twa enemies should leave decoding of the other intact. To remove the potentially confounding influence upon such channel-specific habituation of the consequences of responding per se, habituation of the mobbing response without eliciting it was possible. Since a substantial proportion of the pied flycatchers tested (up to 69.7%)did not sound a single call when presented with ineffective stimuli, though ones they habituated to, the habituation obtained was dubbed “response-free’’ (Curio, 1975). By first showing experimentally naive birds the ineffective “crownstripe” shrike model, the standard red-backed shrike male is rendered virtually ineffective (Fig. 14a,b). In a parallel experiment with other subjects, a similarly ineffective owl also impairs shrike recognition, yet to a much smaller degree (Fig. 14c). This demonstrates that the response-free habituation of shrike recognition depends on the similarity between the two consecutive stimuli. A similar conclusion holds for the corresponding impairment of owl recognition (not illustrated here; see Curio, 1975). In tors.
loo1
I
..? a .:
I I I
Y
: 20 -
I
I I I I I I I I I
:
I 1
I I
;
80-
I a 1
nil6
b
I
D Y
i
I
60-
I
r
P 0
0-
Too
P2= ,005
I n .13
5.5%
44.0%
=
10.0%
n. 20
C
-
00
-
60
-40
- 20
=
44.05
10.0%
FIG.14. Habituation of response by pied flycatchers to male red-backed shrike (a) following (b) imaginary model, (c) wooden pygmy owl model without eyes. 1.2, denote stimulus sequence. Percentage figures beside bars show how often birds remained completely silent. PIfrom two-tailed Mann Whitney U-test. (From Curio, 1975; courtesy of Academic Press, London .)
I67
ASPECTS OF ANTIPREDATOR BEHAVIOR
terms of the two-channel-hypothesis, these results mean that both the shrike channel and the owl channel can be impaired by decoding of stimuli that probably enter the same channel, though an influence of the hypothetical novel-bird channel cannot be excluded. The impairment concerns perceptual processes in that (a) an ineffective owl model renders the owl completely ineffective but not the shrike; (b) there is no intraindividual correlation between the responses in first and second trials. To examine the functional independence of the two predator channels in more depth, impairment of the shrike channel by an ineffective redbacked shrike was not immediately followed by the test with the standard shrike (Fig. 15). Rather, an interpolated response to the standard owl prior to that test demonstrates that (a) habituation of the shrike response leaves the owl channel completely intact, (b) a full-blown interpolated response to an owl does not cause dishabituation, and (c) at the same time the result corroborates the above conclusion that the observed response decrement is entirely stimulus-specific. The experiment again supports strongly the two-channel hypothesis, and the notion that the envisaged channels are truely afferent units. 100-
c
i
80-
5
-
LO
-
I I I I I I I I I I
I I I
c ? 40:
I
I I
Y
g
I
I I
Y
20-
z a
83
- I00
I I
I I I I
I I I
-
80
-
60
-
40
- 10
I 73
I
I7
I9
I7 10
0
I
I I
I
I I
I
2
3
FIG.15. Selective habituation of the mobbing response by pied flycatchers to the male red-backed shrike (3) following an imaginary model remains unaffected by the full response to the pygmy owl between presentations (2)(compare with Fig. 14). 1. Stimulus values from experimentally naive pied flycatchers. 1 through 3 shows stimulus sequence. (From Curio, 1975; courtesy of Academic Press, London.)
168
E. CUR10
The potential susceptibility of both channels to partial occlusion by novel-bird models is difficult to explain on the premise that novel birds enter a channel of their own (see Section II,A,6,b above). One way out of this dilemma is to assume that channels are arranged in parallel and that both predator channels are rather well isolated from each other but not from the still hypothetical novel-bird channel. Alternatively, decoding may proceed sequentially with a hierarchy of decoding steps starting from general properties (animate vs. inanimate) and leading on to those of increasing specificity (see Section II,A,3,b). The ultimate step would involve the classification of the predator type (e.g., owl, shrike, raptor). For this to occur, the filtering out of nonpredators, for example, novel, harmless birds, would precede the identification of avian predators; before predator-specific key stimuli are decoded, the respective objects would have been classified as avian. This could explain why, in the habituation experiments, perception of novel birds partly occludes the predatorspecific decoding units further “downstream.” A sequentially ordered decoding would also explain why the occlusion of channels is a function of similarity between the habituating and the test stimulus. A crown-stripe red-backed shrike may pass-and block-a peripheral filter before another filter located more downstream that requires not only a black bar on the head but a black bar that is horizontal is activated. The idea of sequential filtering would also successfully explain the finding, not illustrated here, that the shrike male channel is more vulnerable to habituation by novel birds than is the owl channel: Shrikes are of a more generalized bird nature and, hence, resemble more other birds than do owls. The hierarchical nature of sequential filtering assumed above may, however, be too simple. Pigeons and monkeys (Saimiri sciureus) learned to discriminate between a kingfisher and non-kingfisher species correctly. Both test species also showed the most abstract concept formation by discriminating between animal and non-animal. Surprisingly, subjects failed to conceptualize bird versus non-avian species, though this task required an intermediate, more concrete level of concept formation. The rules governing such concept formation are unknown but are different from those used by humans (Roberts and Mazmanian, 1988). The picture developed is still hypothetical and more experimentation is needed, with the functional independence of predator channels being the strongest pillar on which to build. e. Selective Priming through Predator Experience. If the envisaged predator channels are broadly independent from one another, perception of the full standard stimulus might prime (sensu Hinde, 1970) the recognition of an incomplete stimulus that is classified by the same channel, yet normally remains ineffective. If the pygmy owl iffollowed by an ineffective
169
ASPECTS OF ANTIPREDATOR BEHAVIOR
loor
I
I I I I I
I I I I I I I
100
I
b
00
60
40
20
I I -
0
I
I I I
FIG.16. Selective priming by response to pygmy owl of (a) an imaginary model, (b) of the most natural wooden pygmy owl model. Surface texture, that is, "naked" versus feathered, is indicated below the owl models. 1,2 is stimulus sequence. (From Curio, 1975; courtesy of Academic Press, London.)
shrike model, that is, the crown-stripe red-backed shrike, the latter remains ineffective (Fig. 16a). If, however, the same primary stimulus is followed by the naked pygmy owl, it enhances considerably the stimulus value of this otherwise completely ineffective though most natural of all crafted owl models (Fig. 16b). The priming effect is specific to the strengthened stimulus and cannot be accounted for in terms of motor output. Moreover, this experiment gives weight to the last one described above (Fig. 15): The shrike must have been rendered ineffective by its ineffective replica and not by the intervening response to the owl, which now proves to be response-augmenting, thereby stressing again the distinctiveness of the hypothesized channels. Rendering the naked owl dummy a potent stimulus via the perception of the normal standard owl stimulus has potentially far-reaching implications. The ineffectiveness of the naked owl found otherwise (Figs. 13, 16) may stem from the majority of pied flycatchers not having encountered a live owl when first confronted with that wooden dummy; among all owl dummies used, the taxidermic mount resembles a live owl most, and might therefore have brought about the increment in response to the wooden
170
E. CURIO
owl (see priming by a live owl, Section III,D,2). If this is true, the majority of the wild birds tested would qualify as owl-naive. f. Responses to both Predators Differentially Affected by Territorial Context. Among 15 unmated male floaters and neighboring pied flycatchers intruding onto a foreign territory during dummy tests, all mobbed the owl whereas a significantly smaller fraction mobbed the shrike male (17.4%, n = 23) and various novel bird dummies (20.7%, n = 15). Accordingly, the outcome of this natural experiment lends yet more support to the distinction of an owl channel from a shrike channel (and, for that matter, that for novel birds)(Curio, 1975). g . The Generality of the Multichannel Organization of Enemy Recognition. Six independent facts unanimously suggest the existence in the pied flycatcher of two separate perceptual channels each tuned to a different predator, that is, owl and shrike (Fig. 11). The most direct evidence is provided by habituation and priming, both of which are specific for the predator used. The existence of a novel-bird channel coping with harmless birds is indicated by various facts, though of a less direct nature (but see below). Its validity can only be fully appreciated once more evidence concerning the liability of the novel-bird channel to habituation is put forward (Section III,C,2). This channel may, furthermore, differ from the other two in its degree of sequential versus parallel filtering of stimuli. The multichannel organization of enemy recognition appears to be an economic way of coping with the multitude of predators; it safeguards the prey against wasteful errors of misidentification which a general RM dealing with all potential key stimuli piecemeal could not. Such errors seem to occur in the rare cases where an innocuous animal happens to combine a number of potent key stimuli (MacDonald, 1973; Aegothelidae; Nash and Nash, 1985; Batrachostomus auritus). The apparent optimality of such an organization raises several questions: ( I ) How general is it? (2) If it is more widespread, is there an upper limit to the number of predator-specific channels? (3) How do learning processes change preexisting channels, expecially as a function of experience with predators? Discussion of this last question is deferred to Section II1,D. Question 1 can be answered by pointing to several animals apparently possessing predator-specific channels, though this has nowhere been examined by more than one criterion, for example, along the lines discussed above (Sections II,A,6,b-f). Relying on the method of identically changing the same key stimulus (Section II,A,6,c). Accipiter hawks and owls were shown to enter different channels in hand-raised shrikes (von St. Paul, 1948). Furthermore, while mobbers of many species treat owls and these
ASPECTS OF ANTIPREDATOR BEHAVIOR
171
hawks in qualitatively the same way while perched, they silently dive into cover as soon as the hawk takes wing, whereas they intensify harassment of the owl when it flies (G. M. Klump, personal communication). Differences in ontogeny permit differentiation between two olfactory channels in a snail, each tuned to a different species of turtle predator (Snyder and Snyder, 1971). Further, a different annual time course suggests at least two channels in the ground squirrel (Spermophilus fereficaudus). While alarm calls are given year round to coyotes (Canis latrans), dogs ( C .familiaris), and cats (Felis siluestris), they are restricted to the summer season for roadrunners (Geococcyx californianus), which threaten only weanling ground squirrels when these appear above ground during the summer season (Sherman, 1980, after data of C. J. Dunford). Apart from the shrikes studied by von St. Paul (l948), it is not known for sure whether the respective predators are recognized innately, or whether the channels are simply due to classical conditioning. An answer to question 2 needs qualification of the relationship between the number of channels and the number of predators decoded by them. It is likely that predators of one multispecies taxon share a channel tuned to it, so that the number of channels is smaller than that of sympatric predator species. For example, a hand-raised red-backed shrike that had been rendered “owl-blind” by exposing it for 72 days to a tawny owl mount failed to recognize other owl species thereafter. Habituation apparently encompassed all owls (von St. Paul, 1948), thus supporting the idea of an owl channel in shrikes (see above) coping with all owls. The argument will hold only as long as habituation to one class of objects, for example, owls, is significantly stronger than any concomitant habituation, or the lack thereof, to other classes of objects. This is what happened in the shrike rendered owl-blind; it responded perfectly well to hawks. Similarly, jays generalize from a tawny owl to a long-eared owl (Asio ofus);Lohrl(l980) heard them give the tawny owl’s hoot, usually emitted at a tawny owl’s roost, to a long-eared owl. Yet there is also differentiation among owls according to body size and, hence, the risk imposed by them; owls (Curio, 1963; Goodwin, 1976; Kerlinger and Lehrer, 1982; see also Richardson, 1942; Markgren, 1960) or Accipiter hawks (Lohrl, 1950a) too small to kill a given prey bird are not responded to. This conclusion ties in with Lohrl’s (1980) observation, since the two owls concerned are about the same size. A further test would be of reciprocal habituation. In a Darwin’s finch (Geospiza difjcilis) conventional habituation to an owl left the response to a hawk intact, yet habituation to the hawk entailed habituation to the owl. By contrast, habituation to the hawk did not encompass habituation to a feral pigeon and, conversely, habituation to the latter did not affect
172
E. CURIO
the stimulus value of the hawk. From these four experiments it follows first, that hawk and owl may not enter separate channels but just one and, second, that there exists a distinct channel decoding novel birds, thus furnishing the most direct evidence for the existence of such a perceptual device (Curio, 1969). It can no longer be objected that the feral pigeon functions as an imperfect raptor stimulus, a question not unequivocally settled for novel bird recognition by the pied flycatcher (see Section I1,A ,6,d). The failure of a Darwin’s finch to differentiate between hawk and owl permits an important evolutionary perspective. It provides the only case analyzed so far in which two prey taxa, that is, Darwin’s finches and shrikes, can be compared in their response to the same two classes of predators. Both enemy-specific habituation and alteration of an identical key stimulus had permitted the conclusion that, in shrikes, owls and hawks enter distinct channels (see above). A caution, however, seems in place. So far “class” was meant to refer to a classificatory, that is, proximate, criterion. Functionally, the “same class’ of predator may hold for most owls but possibly not for hawks. The latter group comprises species of extremely diverse predatory threat, for example, the accipitrine and the buteonine assemblages of species; no stimulus analysis performed so far has broken down the hawk class of raptors into these functionally highly diverse taxa. Like habituation, generalization from one Gestalt to another may assist in the discrimination between enemy-specific channels. If experience with one stimulus is generalized only to similar ones, these may be collapsed into one class. For example, on being chased with an exotic kingfisher, hand-raised bullfinches generalized their acquired fear to several other kingfisher species but not to non-kingfisher objects (Kramer and von St. Paul, 1951). Roberts and Mazmanian (1988) duplicated this experiment with pigeons and monkeys (Sairniri sciureus) by use of a rewardnonreward discrimination technique. They showed that subjects generalized from one kingfisher species to others, as compared to birds of other families. The number of “channels” engendered by learning may be extremely large. But broadening the channel concept to all learned situations would deprive it of its evolutionary connotation, unless the existence of particular learning dispositions could be demonstrated. Accordingly, a channel should be invoked only if it represents a perceptual mechanism coping with a class of predators innately. The concept would thereby also encompass preexisting RMs that need priming for their complete functioning (Section II,A,6,e). Novel-bird channels may require a different input to achieve this end (Section 111,D).
ASPECTS OF ANTIPREDATOR BEHAVIOR
173
B. THEEFFECTOF CONTEXT ON ANTIPREDATOR BEHAVIOR
Over the past two decades, it has become obvious that the context of an encounter with a predator is a powerful and sometimes indispensable determinant of antipredator behavior. One and the same predator species or individual elicits different responses, or no response, dependent on the context of the encounter. To explain this dependence, two hypotheses will be examined here. The “stimulus hypothesis” holds that it is due to some stimulus filtering which differs from the decoding of the predator Gestalt only by its greater complexity. The “risk hypothesis” assumes that the subject assesses the risk to itself or to something of value to it, for example, offspring, imposed by the encounter. Though risk is a functional concept, risk assessment is defined here as a causal process. This process will be invoked when there is context dependence of recognition so that an explanation implying a mere filtering of predator key stimuli would be inadequate (see already Section II,A,6,f). The risk hypothesis predicts that the subject behaves as if it were monitoring the degree of its own endangeredness or that of other potential prey. 1 . Spatial Context
Pied flycatchers use “snarling attacks” to fend off a great spotted woodpecker (Dendrocopus major) that has landed on the trunk of their nest tree or of a tree close by. When a dummy woodpecker is placed visibly on branches in front of the nest hole, instead of on the trunk, it fails to elicit attacks, even when moved (Curio, 1975). (Tits and starlings tend to elicit snarling attacks while moving along these branches.) For a subtler effect of territory ownership differentially affecting the response to owls and shrikes by pied flycatchers, see Section II,a,6,f. While predator-specific risk assessment cannnot be dismissed in the latter case, it can in the case of the woodpecker, since any risk implied by its presence should not depend on the interloper’s perch site: the result thus supports the stimulus hypothesis. In many cases, aerial predators and mammalian ground ones provide different behaviors. Carrion crows classify an aerial predator, a flying goshawk (Accipiter gentilis), as a ground predator as soon as it lands (Lohrl, 1950a; see also Melchior, 1971; Buitron, 1983; Seyfarth and Cheney, 1990;Walters, 1990).Though a bird that flies differs from one that walks, mere stimulus decoding appears not to explain the discrimination, especially in view of the fact that pigeons are able to form a highly abstract concept, for example, of a human, regardless of the concomitant context (Herrnstein and Loveland, 1964). Risk assessment seems a more likely answer in that the flying raptor poses a much more urgent threat than any
174
E. CURIO
predator, avian or mammalian, moving on the ground. Further, Gyger et al. (1987) found that distance of a flying object, and thus imminence of threat, was an important determinant of the “aerial” and the “ground predator” call of the domestic cockerel (see also Nice, 1943; Melchior, 1971); the threat varying along a continuum translates into categorically distinct calls. This imminence of threat idea receives support in yet another way. A perched eagle owl (Bubo bubo) elicits ground predator calls from carrion crows, whereas one near an active nest provokes the flying raptor call signaling maximal threat (Lohrl, 1950a). Here then, one context (being on the ground = lesser threat) is overridden by another context (conspecifics in danger) with the stimulus situation remaining the same. This supports the risk hypothesis most forcefully. The referential signaling hypothesis holds that different vocal signals denote different classes of predator, as suggested in a classic paper by Seyfarth e t a / .(1980). While foreshadowed by the observations of Heinroth and Heinroth (1924-1934), Seyfarth e t a / .(1980) extended the idea to entail an adaptive responding of the receivers of the calls in the absence of the predator eliciting those signals, thus implying communication about an external referent. Though verified for vervet monkeys (Cercopithecus aethiops) by Seyfarth et a / ., the referential signaling hypothesis remained somewhat ambiguous since context due to imminence of threat had not been controlled for. To remedy this situation, Pereira and Macedonia (1991) exposed ring-tailed lemurs (Lemur catta) to two nonnatural (allopatric) predators (raptor, dog) at two levels of threat, but the authors drew the wrong conclusion. While the two predators provoked different vocalizations, thus supporting part of the referential signaling hypothesis, Pereira and Macedonia erroneously dismissed the imminence of threat (“response urgency”) hypothesis. First, during their percipitous flight into trees from a charging dog.the lemurs had remained silent. Only after being in safety did they emit calls of a type denoting the less threatening context (walking dog). Second, one of several signals provoked by the raptor at /ow urgency (“gulp”) was also given to the carnivore when presented at the low level threat. Hence, there is clear support for the response urgency, that is, risk hypothesis. By contrast, referential signaling was not shown to operate, as claimed by Pereira and Macedonia (1991), since their subjects could see the external referent and may therefore have responded to it rather than to the calls provoked by it. To exclude imminence of threat as a contextual determinant, as asserted by Seyfarth et a/. (1980), one would have to manipulate context. For example, one would need to know how a terrestrial carnivore would be treated when encountered in a tree, or an eagle on the ground. (Context had only been looked at in terms of age/sex/motivational factors of the caller.) Pending such manipulative
ASPECTS OF ANTIPREDATOR BEHAVIOR
175
experiments, context in terms of imminence of threat is best regarded as a powerful determinant of antipredator responses, in line with the varied evidence reported above. The risk hypothesis receives yet another line of support. Wariness against surprise attacks or avoidance responses may be site-specific. Thus, minnows (Phoxinus phoxinrrs) avoid a place where they have been attacked by a piscivore previously (von Frisch, 1941; see also refs. in Curio, 1963; Klopfer, 1957; Altmann and Altmann, 1970; Galef and Nord, 1975). Mere perception of the predator (Fraser and Mottolese, 1984) or alarm provoked by it (Richardson, 1942) may suffice to bring about this sitedependent avoidance. The most parsimonious explanation for such cases is to assume conditioning to the circumstances of the predatory encounter. A similar explanation may apply to white storks (Ciconia ciconia), which are shy of humans in their African winter quarters, where they are persecuted, as compared to their European breeding grounds (Sielmann, 1971, television film). It is not known whether the same individuals are involved. Shyness may be area-specific, yet a critical test would be to confront storks with black and white humans in the wrong places to see to what extent the response is predator-specific. However, ducks have been found to become tame toward humans only in places where they were fed (Meinertzhagen, 1950). Some mechanism of risk assessment seems to be required in other cases of context evaluation. Moose (Alces alces) foraging in water have a longer flight distance than when feeding on land (Altmann, 1958; see also van Lawick-Goodall and van Lawick-Goodall, 1970). In the only systematic study of spatial context that has been carried out, great tits were found to sound their warning aerial predator call when the hawk (Accipiter nisus) eliciting it was approaching the caller, or when it had passed overhead, not when moving in any other direction at the same distance (Fig. 17; see also Vogel, 1975: Presbytis entellus; Kruuk, 1972: Crocuta crocuta). The intricate spatial relationship reported seems to rule out the stimulus hypothesis as an explanation. Subtle relationships between predator behavior and the targeted prey forcefully support the risk hypothesis as well. The gaze at or the binocular fixation of the prey is the necessary prelude of the final phase of attack and thus informs the prey that it is targeted. Significantly, prey fish (Sregastes planifrotis) display more predator fear when directly looked at by a large piscivore (Aulosromus maculatus) than when not, and when they are smaller than other prey present in relation to the much larger predator. These findings suggest that what Helfman (1989) calls “threat sensitivity” and Fraser and Huntingford (1986), in a similar situation, call “risk adjustment” behavior is operating.
176
E. CURIO Great lit in front o f
behind Sparrow h a w k
FIG.17. Incidence of aerial predator calls depending on the spatial relationship of the sparrowhawk eliciting them and the calling great tit. Stippling reflects percent callers, with zero callers on either side of hawk’s flight path. Figures denote numbers of tits. (Modified from Klump, 1984; courtesy of G. Klump.)
2. Social Context Social context usually involves spatial context as well, but with the defender’s offspring rather than the defender itself being the target of predation. Depending on the species of predator, risk entails that of loss of the brood and/or of the defender itself.* With a brood at stake, many parent animals fend off predators at distances in proportion to the threat they pose (Myrberg and Thresher, 1974; Thresher, 1976; Neil, 1984; Root, 1969; refs. in Perrone, 1978), or to the value of the resource defended (Itzkowitz, 1979). Significantly, the longest distance from the resource may correlate positively with the fiercest attacks directed at the most Optimality models make predictions on how the parent’s defense intensity should vary with the value (age, number, health of offspring) of the brood (Montgomerie and Weatherhead, 1988). McLean and Rhodes (1991) criticized this functional approach by asserting that parent birds cannot possibly have command of the decision rules necessary for each context. Rather, “proximate factors” giving information on that context would govern defense intensity. This view confuses functional and causal explanation. To evaluate “proximate factors” correctly (i.e. adaptively), parents must have the machinery at their disposal to do so. This machinery, even if it includes learned decision rules. may well be the product of natural selection that, in turn, can work on a host of proximate factors and how they come to be perceived.
ASPECTS OF ANTIPREDATOR BEHAVIOR
I77
dangerous predator (Anderson, 1971). Similarly, with one predator species, that the threat perceived is a function of distance from the nest is suggested by the vocal behavior of three American finches (Spinus sp.). With increasing proximity to the nest an approaching person elicits three different vocalizations in succession. The most alarmed one, with the threat closest to the nest, is also (almost) the same as the one provoked by an Accipiter hawk, the most feared predator, in any location (Coutlee, 1971; see also Collias, 1960; Verbeek, 1972a). If the approach culminates with the would-be victim being seized by the predator, social defense may be triggered (Section II,B,3,b), providing at the same time to attendant prey individuals contextual information instrumental in modifying the response to a predator (Section III,D,4). Furthermore, the more directly (i.e., nontangentially) a human approaches an incubating gull (Larus marinus, L. argentatus; Burger and Gochfeld, 1981), or looks at an active nest (Knight and Temple, 1986a: Agelaius phoeniceus), the more prompt or stronger becomes the defense. Similarly, one of two call types given by parent stonechats (Saxicola torquafa)became more prominent when a human headed away from the nest that was at stake (Greig-Smith, 1980).Carried to an extreme, direction of movement alone may become a sufficient cause for an avoidance response to occur. The common toad (Bufo bufo) flees from a large ant (Camponorus herculeanus) that is heading toward it, whereas it strikes at it as food when it moves tangentially around it (Ewert and Traud, 1979). Since the defender might continually be monitoring the spatial relationship between the brood that is at stake and the predator (see also Karplus, 1979; Karplus and Bentuvia, 1979),a “stimulus”-based explanation may still apply. When such a continual monitoring is of little or no avail, risk assessment must be invoked. For example, wildebeest (Connochaetus taurinus) with calves flee from predators at a distance of 200 m as compared to 50 m when they are alone (Schaller, 1972, p. 341); either of the two stimuli, the calf or the predator, is certainly not in sight continually. This applies even more forcefully to all studies where defense increases with the value of the defended item, but the item is not (always) in sight; age and number of nestling birds hidden from a distant parent observer are cases in point (review by Montgomerie and Weatherhead, 1988). Risk assessment also certainly operates in vigilance in general, that is, when predation risk was manipulated by distance from cover or recent experience with a currently unseen predator (Section II,A,2). Risk assessment may vary with the species of the unseen predator (Lorenz, 1935; Seyfarth et al., 1980). Risk assessment may involve other would-be victims. Such a “social” influence may be exerted by other species in the same area. Their mere
178
E. CURIO
presence as indicated by a taped mobbing chorus (Fig. 181, or the number of other individuals partaking in a mob (Volkel and Zell, 1980; Robinson, 1985), can enhance the response to a predator. (Robinson [ 19851 showed that more mobbers in a flock of yellow-rumped caciques [Cacicus cela] chase away avian predators raiding a colony’s nests more effectively [see also Robertson and Norman, 19761.) Though both parties, the predator and the flock, may be continually monitored by flock members the assumption of a risk dilution effect (Hamilton, 1971), and hence risk assessment. appears the most plausible explanation.
3 . The Distressed and the Dead ConspeciJic Since both dead and distressed conspecifics release versions of antipredator behavior, it may be asked to what extent they represent situations of predatory threat or genuine predation. a . The Distressed ConspeciJic. There are considerable species differences in the propensity to attack or mob a predator that is threatening or has seized a conspecific. Augst (1975-1976) first demonstrated quantitatively that a great tit instantaneously increases its harassment of a little owl when a live great tit is made to dangle from the owl’s talons (for Mobbing I
I
n = 11
IF
I
I
1
1
0 1000 2000 2600 FIG.18. The latency of great tit parents with young to mob a live pygmy owl in front of their nest is dependent on the simulated presence of other mobbers. The latter are represented by a multispecies mobbing chorus including great tits. Latencies: median, SD and ranges: n = numbers of individuals. p2 two-tailed Mann Whitney U-test. Black bar (F) on bottom line shows the mean time interval after which parents turn up near nest to feed young when the birds are undisturbed. Latency Is1
*
ASPECTS OF ANTIPREDATOR BEHAVIOR
179
anecdotal reports, see refs. in Curio, 1963; Scherzinger, 1970; Denson, 1979). Conover and Perito (1981) found the same effect with starlings, as measured by “wariness,” leading to an enhancement of the response to the owl (Section III,D,4,a). While starlings respond less to a dead conspecific held by an owl (Conover and Perito, 1981),jackdaws (Coruus monedula) reflexly attack with specific vocalizations as a group a person carrying a conspecific, dead or alive, when well feathered, that is, not being a naked nestling (Lorenz, 1931), European jays do so only when they are not socially bonded to humans, that is, when they are parent-raised (Goodwin, 1952, 1976; see also Booth, 1962: Cercopithecus aethiops, C. neglectus; Kruuk, 1964; Larus ridibundus). Barash (1976) found both a crow dummy and a black, same-sized cloth lying in front of a great horned owl (Bubo uirginianus) mount to increase mobbing by common crows (Coruus bruchyrhynchos) equally strongly. However, since the crow dummy was an unfeathered plastic replica, the lack of differentiation may have been an artifact of the fact that an incomplete stimulus was used. Ravens (Coruus corax) socially defend only a conspecific, or even a human, that is closely bonded to them but otherwise help the predator to kill the seized victim (Lorenz, 1931). In some cases, this helping to kill behavior is not sufficiently differentiated to tell it apart from social defense. In carrion crows it is clearly distinct but, at the same time, they do not discriminate between a conspecific in distress and a tame one carried on the arm, that is, in both situations they harass the threatening human (Kramer, 1941). Thus, the stimuli characterizing a seized conspecific may vary widely among specie^.^ Spatial proximity of a potential predator to another would-be victim, including conspecifics, may be a necessary and sufficient condition for social defense to occur. Augst (1977) first demonstrated that mobbing by three species of tits is elicited at successively higher levels as the wouldbe predator approaches and finally seizes a freshly captured bird of any of four species; results are most complete for the great tit (Fig. 19, situations 1 through 3). The protocol ensured that the response was not contagiously triggered by that of the primary mobbers, yet these were soon joined by secondary mobbers. Neither the captive bird, even if made nervous, nor the empty cage alone suffices. In general, the free tits even perched on the cage, some with mild alarm, as long as there was no threat to the caged tit. Some inconsistency in Lorenz’s (1931) account remains unresolved. Whereas jackdaws are said to attack both a person carrying a black cloth and ajackdaw carrying a black feather, or moving another’s corpse, they do not respond with attack to a black domestic pigeon held in the hand the same way as to a conspecific.
180
E. CURIO
I5 m
E!
*I.
-n*I. 60
0
-
LO-
20 o
0
A
I_
p=.06
0 1
'I.
n 0 "
-LO
55
-20
0
FIG. 19. The incidence of vocal mobbing by free great tits as a function of increasing threat (1 through 3) by the same person carrying a captured tit (Parus major, Parus caeruleus, Parus montanus) or nuthatch (Sirra europaea).Top: control with empty cage; middle: control with captive but no human nearby; bottom: various degrees of objective threat to captive. Figures beside columns indicate numbers of individuals. (After data in Augst, 1977.)
The question whether the distress of the captive per se, the predator approaching it, or a combination of the two are the crucial factors involved cannot be definitely answered yet. Voluntary fluttering of the captive enhanced mobbing in all three tit species, but not up to the level observed in situation 3 (25.7 vs. 68.5%). The crucial experiment would be to shield the captive from the approaching human. The hypothesis of a coaction of both stimuli would predict that the level and course of response remain the same as in Fig. 19 (bottom). The slight mobbing observed in one control (Fig. 19, top), which is certainly conditioned through previous captures, offers a preliminary answer. Furthermore, wild carrion crows immediately harassed Kramer (1941) and intensified the response as he approached his tame young. In this case, the reaction was solely due to the changing distance between the endangered conspecific and the threatening enemy, thus controlling for the behavior of the threatened young at stake. Species vary in their responsiveness to the movements of distress of a captured conspecific from being unresponsive to being alarmed (refs. in
ASPECTS OF ANTIPREDATOR BEHAVIOR
181
Augst, 1977), even including the rescue of a group member through physical attack (Rood, 1983). Responses to distress calls vary from mobbing/ attacks to being deterred (review in Klump and Shaker, 1984). These signals are emitted by a bird (or an insect) once it has been seized by a predator and is still struggling. A discussion of their releasing value is beyond the scope of the present review. Vulnerability of offspring may affect the vigor of defense, all other things being equal. Thus, magpies (Pica pica) harass a crow near their nest more vigorously when the nest is unroofed, instead of being roofed as is normal (Roell and Bossema, 1982; see also McLean et al., 1986; Hobson et al., 1988). Unfortunately, the relationship is confounded by parent age in that younger magpies build unroofed nests more often (and these are also disturbed by crows more often). As correctly observed by Montgomerie and Weatherhead (1988), parents that are more vicious defenders may build more exposed nests, a causal link that is, however, unlikely in the magpies mentioned since, as a rule, defense if anything increases with age (Curio, 1988a). Great tit parents, whose nests had been experimentally rendered more vulnerable by enlarging the entrance hole, defended their brood against a woodpecker (a nestling predator) less than did a control group. From this one may conclude that parents may translate an increased vulnerability into decreased reproductive value (or some more suitable cohortal measure of reproductive prospects) of their offspring. This is just the opposite of what the vulnerability hypothesis originally suggested (Harvey and Greenwood, 1978), though the latter is partly flawed in a number of ways (Onnebrink and Curio, 1991). More experimental work with manipulation of the vulnerability of broods is clearly needed. b . The Dead Conspecific. When found by itself, a dead conspecific elicits cautious inspection (Kramer, 1941) and/or some mobbing (e.g., Kramer, 1941; Moholt, 1989; Stone and Trost, 1991). Does the dead conspecific fall into a known class of objects eliciting mobbing, or does it constitute a category of its own? Since afresh corpse carries many features of an animate object, and since it displays a posture not normally exhibited by live conspecifics, novelty could be implicated. Since, in terms of species recognition, this novelty is slight as compared to truly novel creatures, that is other species, a Gespenst reaction (Section II,A,I) could operate, that is, a special type of novelty. Since a dead animal is, by itself, no deadly menace, the only benefit in responding to it with behavior akin to protection might be to forestall an imminent attack. This functional explanation turns into a hypothetical causal one: The corpse may be taken as a sign of a nearby predator (see also Moholt, 1989). If true, this idea predicts that a similar-sized corpse of an alien (yet familiar?) species should
182
E. CUR10
elicit the same cautionary behavior. There is no systematic information on this point, yet Toenhardt (1935) saw woodland songbirds mob a dead, prostrate tawny owl more than a live one nearby (see also Kramer, 1941). A second prediction springing from the sign-of-predator idea is that a taxidermic lifelike mount of a conspecific should not elicit a Gespenst reaction; subjectively it is alive. In support of this, Strauss (1939) found jackdaws responding almost calmly to such a mount while being enormously scared by comparable mounts of a hawk or an owl (cf. also footnote 3). Also a familiar, harmless species, when stuffed, elicits little fear (Section II,A,I). In the most detailed study examining the effect of a dead companion, Inglis and Isaacson (1984) used stuffed wood pigeons (Columba palumbus). With specimens in various postures simulating a fresh corpse, one with spread wings was found to deter wild conspecifics most effectively. Strangely, the open-winged decoys were only effective when displaying the species’ white wing marks that are normally visible only in flight. A pair of wings alone did not work. Functionally, this may signal a decomposed corpse. This latter result, together with a similar observation in jays by Goodwin (l952), hints again at the sign-of-predator hypothesis. However, Kramer (1941; see also Verbeek, 1972b; Moholt, 1989) found an isolated wing or tail of a conspecific to elicit in carrion crows strong harassment, as did a pile of pluckings from a pheasant (Phasiunus colchicus).Similarly, common crows (Corvus brachyrhynchos) and a red-shouldered hawk (Bureo lineatus) were seen to mob at a pile of turkey feathers (Kilham, 1982). Further experiments on this point are badly needed. This issue is complicated by the fact that, in many social species, including corvids, there is a tendency to attack and even kill a sick or mutilated bird, including conspecifics (Geyr von Schweppenburg, 1958; refs. in Curio, 1976). Mobbing of a dead conspecific by black-billed magpies (Pica pica hudsonia) induces others to join in the chorus; the calls used differ somewhat from those used when mobbing a goshawk. As suggested by Moholt (1989), the attraction of others may protect those seeking the predator by way of the selfish herd or the confusion effect. The gathering itself may be beneficial if the information gained about the predator outweighs the cost of staying near danger. The tendency to kill odd individuals in a group may be in itself a further means to preempt an attack; a disabled prey may impart hunting success on a nearby predator and thereby condition it to the place where it was successful. Killing of the odd removes a most potent attack stimulus from the killer’s home area and, thus, denies the predator sustenance. This functional interpretation of nonpredatory killing receives support from an extraordinary observation that, at the same time, broadens the range of
ASPECTS OF ANTIPREDATOR BEHAVIOR
183
stimuli known to elicit mobbing. According to Root (1969). blue-gray gnatcatchers (Polioptila caerulea) drive away, with unfailing success. nonpredatory animals from the vicinity of their nest. By contrast, they harass, with less success, predatory species. In one exceptional case, they harassed for 2 hr a fledgling western bluebird (Sialia mexicrrna) unable to fly well. Incessant harassment was probably provoked because the otherwise successful supplanting attacks directed at nonpredatory species, including adult bluebirds, had failed. The perseverence of this response is on a par with the strongest mobbing of predators (Curio, 1975). though the stimulus situations differ vastly. In both cases, moving on the intruder may be the driving force behind harassment (Curio, 1978; best evidence in Pettifor. 1990). This interpretation of aggression/mobbing has in common with both the sign-of-predator hypothesis and the unclassifiable risk hypothesis (Section lI,A,4,c) that the potential prey birds take preemptive action against being killed in the absence of any predator. These two hypotheses share the premise that vigilance is engendered by clues indicative of a predator that is itself unseen. The perceptual mechanisms at work in the three cases are certainly different but they would seem to converge on a common mental construct, an unseen and therefore unclassified predator. Given enough information on a predator, this mental representation may turn into ‘‘naming’. it: a wild jay that used to mob a tawny owl in a hollow tree sounded the owl’s hoot calls when the owl was out (Lohrl. 1980). Though involving an unseen predator, the wariness engendered in carrion crows that keep under surveillance a site where a goshawk has disappeared is certainly governed by a mechanism different from the sign-ofpredator one. The crows either wait until the raptor has moved on or they fly off so that no surprise attack threatens them where they go (Lohrl. 1950a). In this case, memory of where a real predator was last seen is causative in bringing about the increased vigilance and alarm. There are marked species differences: tits, emberizines, and sparrows calm down immediately the goshawk is out of sight (see also Curio, 1976: discussion of “object permanence” of prey for the hunting predator). 4. Staying Put-A Simple Yer Potent Key Stimulus
Predators may utilize the harassment they draw upon themselves to track down the nest of the harasser (Curio, 1976; Hennessy and Owings, 1988). Accordingly, parents might refrain from engaging a predator in an encounter and remain in seclusion or simply do nothing; even feeding visits to a nest might betray its locale to observant predators such as magpies (Piccrpiccr; E. Curio, unpublished observations). A small fraction of pied flycatcher parents remain completely inactive when confronting a
184
E. CURIO
shrike (5.5%; see Fig. 14) or an owl (8.2%) near their nest hole (Curio, 1975). Accordingly, parents might strive toward nest concealment instead of active defense. The idea of nest concealment was strengthened by the finding, among others, that great tit parents respond to a danger more strongly at a greater distance from their nest hole (Zimmermannand Curio, 1988). As discovered by chance, an exotic species, a live Java sparrow (Padda oryziuora), inhibited mobbing at great tit nests under the same conditions as an owl elicited it (Curio et al., 1978b). This finding, together with the idea of nest concealment, instigated research into the effect of that novel, harmless bird on cautious behavior. The typical response of a great tit finding, near its nest containing young, a live Java sparrow is “freezing” with the prey items it has gathered. These will eventually be eaten. Or, after a prolonged inhibition to feed the nestlings, the tit inspects the stimulus bird at close range without signs of fear, andlor visits the nest to deliver its food. The time from discovery of the bird till actual feeding, the “feeding latency,” may exceed the usual nest visitation interval by many times (Fig. 20). The duration of the feeding latency can be thought of as striking a balance between the need for nest concealment and the possibility of damaging the brood through starvation. The Java sparrow may elicit cautious behavior either because it is novel or because it is stationary, not moving on as do other birds that happen to perch in the nest environs and have no interest in the brood/nest hole. Being stationary per se may make a bird appear dangerous since time is limited and if extended for any length of time any behavior must have clear benefits. To a vigilant parent, time invested at its nest by a strange intruder may therefore mean a vested interest in its contents. Hence, the parent may be secretive about the nest because this forestalls its discovery. (This explanation is not meant to imply any reasoning on the part of the tit. Rather it suggests the mechanism on which selection could have built this form of brood protection.) In order to separate out the effect of novelty from that of staying put on the part of the Java sparrow, a maximally familiar and harmless bird, a live male chaffinch (Fringillu coelebs), was chosen for a control experiment (Fig. 20). From the observed differences in feeding latencies two things follow. First, the Java sparrow elicits concealment behavior because of both attributes. Being stationary per se can render both a novel, objectively harmless bird and a familiar harmless bird (subjectively) dangerous; note that the chaffinch elicits more concern than does the cage alone. Second, novelty per se is a potentiationg factor, implying that the great tit has stored in its memory all common species present in its habitat (Curio, 1979). This forcefully supports the notion that an initially fear-
ASPECTS OF ANTIPREDATOR BEHAVIOR
185
700) .
6000,
2
500-
E
400-
-I
0
300LL
c
200-
0
: 100I 0-
Novel
Familiar
Novel
Animate
Animate
Inanimate
FIG.20. The inhibition of feeding of nestlings by parent great tits as a function of novelty of a stationary caged live bird as opposed to an "inanimate" cage presented in front of nest. Figures in bars indicate number of parents tested. Differences among latencies (paired tests) are highly significant (two-tailed P < . O I L Inset figure: freezinggreat tit. (From data in Curio. 1989.)
ful response to harmless species abates as familiarization with them progresses (see Fig. 24). The question of why the tits did not attempt to drive away any of the stimulus birds must at present remain unsettled. Given that great tits, like other birds, are dominant at their nest hole over other species, moving on an intruder with a supplanting attack should be cheaper than remaining motionless. Concealment of refuges appears to be widespread. There is inhibition in red-bellied tamarins (Saguinus labiatus) to enter their communal roost in the presence of a human observer, even though they are habituated to the observer (Caine, 1990). Further, from their detailed yet nonexperimental accounts of encounters between California ground squirrels (Spermophilus beecheyi) and free-living rattlesnakes (Crotalus uiridis), Hennessy and Owings (1988) have independently arrived at similar conclusions con-
186
E. CURIO
cerning concealment behavior. A rattlesnake, being a threat especially to young squirrels underground, strives to locate a nursery burrow. For this, it uses the mother’s location “as the hub of a radial search pattern” (Hennessy and Owings, 1988, p. 317). To forestall discovery of the nursery burrow, the mother in turn often does not move in the face of the snake’s advance, as if to withhold from the snake information about the burrow location. Harassment of the snake, for years the focus of research of Owings and his co-workers, is but one of four possibilities of protective behavior of the squirrels. The nest concealment hypothesis predicts that, in the final phase of a successful search, the predator should be attacked uncompromisingly since concealment is then no longer profitable. To test this, the Java sparrow was presented to great tits with nestlings, but now placed in its cage directly beside the nest box (Fig. 21). In line with the prediction, the tits now mobbed the interloper moderately and one male displayed distraction behavior (as is sometimes elicited by a live owl, in conjunction with the most vigorous mobbing). Why the tits initially still froze remains as enigmatic as their associated feeding inhibition when, in another experiment, a woodpecker dummy peered into the hole, thereby indicating to the parents that the nest had been discovered (Onnebrink and Curio, 1991). Pied flycatchers conformed more clearly to the prediction. Their behavior switched from concealment to the most vigorous harassment and aggres-
FIG.21. A test of the nest concealment hypothesis of brood protection with great tits. A live Java sparrow when presented immediately beside the nest box containing young great tits elicits more mobbing and, in addition, distraction display (after unpublished data).
ASPECTS OF ANTIPREDATOR BEHAVIOR
187
sion when the Java sparrow was swapped between the far and near sites, with each site being tested on different pairs (E. Curio, unpublished observations; see also Goodwin. 1953: Tirrdirs merula; Duckworth, 1991: Acrocepphalus scirpaceus). Yet, there is conflicting evidence. For example, fieldfares (Turdus pilaris) and great grey shrikes (Laniirs excubitor) go almost into paralysis once a live predator (cat, red squirrel, carrion crow, magpie) has reached the nest but start to harass it again when it moves off (Hohlt, 1957).The discrepancy may be resolved by looking at the risk for the defending parent. In the two latter species the predator implied a threat to the parent too, not only the brood, as compared to the great tit and flycatcher experiments mentioned previously. Assuming that the nest predator is stationary and thus better able to retaliate, the greater caution of the parents may become explicable. Likewise, European blackbirds mobbing an owl from a distance continue mobbing at close quarters once the owl takes wing (E. Curio, personal observation). However, other explanations may well apply (Goodwin, 1976). The experiments by Duckworth (1991) do not seem to fit the risk assessment idea. However, he worked with mounts of predators (sparrowhawk, jay) that may have been less intimidating than the real thing (see also Goodwin, 1952, 1976). The decision for nest concealment as opposed to nest defense must depend on many factors. The staying put principle may be widespread, as indicated by observations of Perrone (1978) in a cichlid (Cichlusoma muculicauda). It may possibly explain why humans have so often been successfully used as predator stimuli, though for many of the species concerned humans have never played any predator role in the past. Significantly, stationary behavior signals danger not only to the owner of a nest. Even stopping during a walk, or looking at birds closely, irritates them because they perceive this as being targeted (e.g., Hamerstrom et al., 1965; see also Knight and Temple, 1986a). The implications of the staying put principle are potentially far-reaching. The conclusions on the stimulus values of predator and other dummies, as scored by active defense, remain valid only if dummies influence the conflicting needs of alarming and concealment in the same way. This is not necessarily true.
111. DEVELOPMENTAL ASPECTSOF ENEMYRECOGNITION A. INNATE INFORMATION ON PREDATORS
I. An Operational Definition In the following discussion a predator is said to be recognized innately if the response typically given to it requires no individual experience with
188
E. CURIO
and attack by the predator. The underlying perceptual performance is ascribed to an IRM (sensu Schleidt, 1962, 1964) or an innate coding mechanism (sensu Hailman, 1970). The definition is potentially up against two difficulties. 1. The response typically given may require some experience with the predator in question but this experience is channeled by some innate predisposition for acquiring it. The innate predisposition merely furnishes a baseline of response strength on which experience of the predator can then build further, to change an IRM into an IRME (sensu Schleidt, 1962), that is, an IRM altered by e~perience.~ That predisposition must be stimulus-specific because objects other than the predator cannot bring about the full response. Jacobsson and Jarvi (1977) found in Atlantic salmon (Salmo salar) that the full avoidance response to pike (Esoxfucius), a specialist piscivore, required inspection from a distance. An equivalent experience with a live burbot (Lota lota), a predator of lesser threat, did not raise response strength at all; response strength remained as low as that given initially to pike. Unfortunately, it remains unknown whether the response to the burbot exceeds responses given to other, harmless fish species, that is, would qualify as genuine antipredator behavior. Significantly, development of the full pike response requires no attack from pike. Further, avoidance of pike by minnows (Phoxinus phoxinus) is likewise enhanced more effectively via the unlearned “Schreckstoffreaktion” as compared to the identically conditioned avoidance of Tilapia (Magurran, 1989; see also Magurran, 1990). Similarly, various cultural transmission effects reveal predispositions to acquire biologically relevant stimuli without prior experience with them (Section 11I,D14,a).The ways by which this acquisition takes place are diverse. That predator avoidance can function independently of any attack does not, of course, rule out the possibility that the response observed might be enhanced or otherwise changed by an attack (see Section III,D,3). Therefore what has been termed above “full response” is not necessarily the maximal response of which the prey animal is eventually capable. A full response is simply that sufficient to prevent the animal from blundering into the danger zone surrounding a predator. The movements preparatory to a hunt may merge imperceptibly into the final predatory attack. Should a prey, during its first encounter with
The postulate by Schleidt (1962) that, for an IRME to operate, the response should still be released via the original IRM is perhaps unrealistic in all those cases where (a) the IRM has been changed permanently (e.g., Hailman. 1967). or (b) the response has become changed permanently (see below).
ASPECTS OF ANTIPREDATOR BEHAVIOR
189
its predator, be sophisticated enough to decipher those incipient, preparatory (or intention) movements (e.g., Neil1 and Cullen, 1974) as signs of imminent attack, the distinction between attack-related experience and any other predator-related experience becomes blurred. However, the operational definition of innateness given above remains useful in that it captures the essence of a decoding process that is stimulus-specific enough to be termed enemy recognition prior to any genuine predatory experience. To unravel what other predator-unrelated factors during ontogeny have contributed to the maturation of the underlying IRM is a legitimate goal of research. This goal, however, cannot with any logic be used to abandon the concept innate, provided it is carefully defined, as has been suggested by some authors (e.g., Hinde, 1970; Baerends and Drent, 1982). 2. The animal under scrutiny can be deprived readily of the very predator whose innate recognition is going to be tested, such that apredator-related experience is excluded. Yet, there may be stimulus objects that share stimulus properties with the predator under study that cannot be withheld equally well during ontogeny. For example, three-spined sticklebacks (Gasterosteus aculeatus) from a population hunted by pike develop a typical pike avoidance response when raised by their father, though in total isolation from pike. “Orphan” sticklebacks raised by hand fail to develop proper pike recognition as do young from a predator-free population that are raised under either regime (Tulley and Huntingford, 1987a; see also Bruckner, 1933). It remains unknown which factor(s) associated with paternal care renders the response functional. One may speculate that the fry, after frequently being chased and retrieved to their safe nest by their father, generalize from the latter to a pike. In guppies, it is probably the escape response itself that is improved by conspecific chasing of fry, but high-speed cinematography would be needed to confirm this (Goodey and Liley, 1986). In the stickleback, the difference between the fry from the two populations in their liability to develop the avoidance response must bear out a preexisting difference in the IRM coping with pike (assuming that the paternal care in both cases is the same). It remains to be demonstrated in each Kaspar Hauser experiment how successful the deprivation of enemy-specific stimuli has been, and this is not always obvious.
2. The Evidence for Innate Enemy Recognition a. The Stimulus Pattern as a Whole. In the Kaspar Hauser experiment, the prey animal is deprived only of that enemy whose innate decoding is going to be examined. A positive outcome permits the conclusion that some innate decoding of the enemy under study is taking place. In the
190
E. CURIO
case of a negative outcome, that is, a failure of the Kaspar Hauser animal to display the antipredator response under scrutiny, the need for individual experience cannot be invoked to explain its existence as has been done repeatedly (Nice, 1943; Hirsch et a / . , 1955; and rebuttal by Tinbergen, 1957; Montevecchi and Maccarone, 1987). Likewise of limited value are studies in which the naturalness of the predator tested must be called into question (e.g., Csanyi, 1985; Pereira and Macedonia, 1991). As has been made abundantly clear by Schleidt (1964) there are many pitfalls to be avoided. The least appreciated are slight deficiencies in the health of the Kaspar Hausers that may go unnoticed by the eyes of even the skilled researcher. They become fully evident if they can be remedied. For example, the shrikes (Lanius collurio) hand-raised by U. von St. Paul (personal communication) in one year failed to recognize owls at the proper age. By contrast, shrikes hand-raised in another year, whose diet was supplemented with silkmoth (Bornbyx rnori) caterpillars, displayed the proper owl recognition. There was no recognizable difference in the appearance of the two groups of birds (see also Section IIl.D.4,b). Inadequacies of raising and/or housing Kaspar Hausers are the sword of Damocles that emperils every deprivation experiment. It can be safely assumed to be absent when working with “natural Kaspar Hausers.” Thus, the sharp-beaked ground finch (Geospiza dfjcilis septentrionalis) on predator-free Wenman Island in the Galapagos has a pronounced fear, comparable to that of geospizines on predator-inhabited islands, of owls and hawks. That fear must be due to some IRM since any predator-related experience is denied to that population (Curio, 1969). A negative outcome of the experiment on Wenman Island would have been a strong indication that loss of the IRM had occurred due to a relaxation of selection. Similar considerations apply to the snake response of geospizines on snake-free Galapagos Islands (Curio, 1965). The enemy recognition of a number of songbirds was shown to be innate three decades ago (Curio, 1963), and more cases from among the vertebrates have come to light since (Table I). Except for amphibians, the list contains examples from all classes. It may mean that innate performance is the rule, but one does not know what negative evidence has gone unpublished, though such evidence is equivocal for the methodological reasons discussed above. Since the list is a random selection of Kaspar Hauser experiments, it has not omitted negative evidence when this is known. Nonetheless, the list in Table I needs some qualification. 1. Only part of the studies have controlled for the stimulus-specificity of the assumed IRM. Where control objects used were inanimate, novelty alone can by no means be ruled out to be the causal agent. In one such
TABLE I INNATEENEMY RECOGNITION AS DEMONSTRATED BY DEPRIVATION EXPERIMENTS ON VERTEBRATES S I N C E THE LASTREVIEW"I N BIRDS
No.
Kaspar Hauser species
I
Poecilia reticulata
2 3
Predator stimuli and ranking where known"
Stimulus specificity controlled for by a or i' a
Gasterosteus aculeatus Salmo salar
Rivulus hartii, Hoplias malabaricus, Crenicichla alta Esox hrcius Esox Iucius > Lota Iota
4
Hemichromis bimaculatus
2 staring eyes > 3 staring eyes
a. i
5
Heterodon platirhinos
a. i
6
Geospiza sp.
Otus asio D; human with stare > human with eyes averted Dromicus sp. + D
a
7 8
Ceospiza sp. Taeniopygia guttata
Asio D, Buteo D Glaucidium brasilianum
a(D). i a
9
Ficedula hypoleuca
Strix D, Athene, Lanius excubitor Staring eyes D, human face
a. i
10
Callus gallus bankiva
-
I
Comment
Source
Adaptive geographic variation
Seghers (1973. 1974)
Adaptive geographic variation Avoidance of Esox only increases on perceiving it Serves avoidance of piscivores + dominant conspecifics Recovery time from cataleptic response
Tulley and Huntingford (1987a) Jacobsson and Jarvi (1977)
Natural Kaspar Hausers on snake-free islands. Adaptive geographic variation Adaptive geographic variation Presence of pair mate andlor open view of landscape required. Dummies fail Lanius: adaptive geographic variation Recovery time from tonic immobility. Domestic fowl, human-experienced
Curio (I%% E. Curio, unpublished
Coss (1978a) Burghardt and Greene (1988)
Curio ( 1%9) Hoffmann (1979). Lombardi and Curio (1985a) Curio (1975) Gallup et al. (1971. 1972)
(continues
TABLE 1 (Continued)
No. II
Kaspar Hauser species Gallus gallus bankiva
Predator stimuli and ranking where knownb Falco tinnunculus D, staring
eyes D 12
Gallus gallus bankiva
Human
13
Bubo virginianus
14
Aphelocoma coerulescens, Aphelocoma ultramarina Alectoris rufa
I5 16
Neotoma albigula Rattus norvegicus, 5
Pit uophis catenifer Felis catus
Stimulus specificity controlled for by a or i' aD aD
-
r\o 4
Human
laboratory strains 17
Mesocricetus auratus
18
Mesocricetus auratus
19
Peromyscus maniculatus
20
Spermophilus beecheyi
Odor of Mustela putorius, +D Mustela putorius f. furo. + D Dog, odor of dog, +D Mustela, Felis , Coluber , Pituophis Crotalus viridis > Pituophis melanoleucus
Comment Fear increases on stare of eyes following chick. Domestic fowl Avoidance differs among two stocks; modifiable more by reward/habituation in birds of tame stock Response matures earlier in less social A. coerulescens Only if not familiarized with man within 48 hr of hatching
a
a, i
Response most pronounced in least selected strain. Strain differences Freezing, threat, attack, occlusion of burrow Flight into burrow; freezing rarely Adaptive geographic variation Adaptive (?) geographic variation
Source Scaife (1976a.b) Murphy and Duncan (1977, 1978) Cully and Ligon (1976) Csemely et al. (1983, 1984) Richardson (1942) Satinder (1976)
Dieterlen (1959) Dieterlen (1959) Hirsch and Bolles (1980) Owings and Coss (1977);
s
21
Spermophilus beecheyi
Crotalus viridis = Pituophis melanoleucus
22
Canis lupus
Human
23
Damadama
Human
24
Didelphis virginianus
Human (dog)
a
Kaspar Hausers both snakenaive + burrow-naive dealt appropriately with snake in burow but did not discriminate the two species as they do above ground (see no. 20) Only if not familiarized with humans in early life. Independent of parents' tamenessd Only if not familiarized with humans during first 2 days of life. Independent of mother's tameness Feigning death when grabbed: dependent on rearing by mother and/or housing conditions
Coss and Owings (1978)
Woolpy and Ginsburg (l%7)
Gilbert (1968)
Francq (1%9)
Curio (1%3). . .
* D denotes response to dummy only; + D denotes response to dummy and to live predator.
' a, Animate, denotes either live, taxidermic, or other replica of control stimulus. i, Inanimate, denotes man-made control stimulus of about predator size, or simply test environment (the latter when not specified). There are qualitative interindividual differences among littermates in their response to humans which complicate things (Shaker et al., 1977;see also Fox, 1972).
194
E. CURIO
study (no. 4 in Table I), some work on stimulus analysis appears to make it certain that the performance is specific for the targeting predator/ adversary. However, even here some control for preexposure conducive to positive responses would have been necessary (see point 2 below). The stronger effect of the predator as compared to an animate object would appear to guarantee the stimulus specificity looked for. The importance of the discrimination of predators from innocuous species derives from the popular notion that animals have “to learn what not to fear” (refs. in Nice, 1943; Bronson, 1968). This idea is clearly rejected by the evidence for an innate discrimination between the two classes of objects. It is also rejected by evidence showing that avoidance of particular enemies requires learning (Section III,C,3). The idea is less easily falsified in the case of the discrimination between harmless species and novel inanimate objects (see Section III,B,C). 2. The gaze of two staring eyes is one potential key stimulus that is contained in the human face. It is possible that preexposure during rearing, maintenance, or capture by humans could bias responses to staring eyes, where these have been employed as a stimulus. Apart from one study (no. 7 in Table I ) where experimenters covered their faces with a stocking mask whenever handling the subjects, no study controlled for this potential source of bias (but see Coss, 1978a). A similar caution applies to the effectiveness of a mammal’s pelage (e.g., Kramer and von St. Paul, 1951) and the hair of the experimenter’s head. 3. In some cases (nos. 9 and 13), only some of the Kaspar Hausers tested responded as would be expected from the behavior of wild birds. This may be no serious drawback since in the wild the adults tested had a territory and/or a brood, factors that the Kaspar Hausers were deprived of. Therefore the test must be regarded as highly conservative. It is important to note that the maximum response strength attained a level equivalent to that in the wild (Curio, 1975). 4. Experiments in which dummies (D) were used instead of the real enemy must be regarded as conservative, too; dummies provoke weaker responses (Section II,A,l) and, in one case (no. 8), failed to release any: this had led an earlier investigator to conclude that zebra finches lack any owl response (refs. in Lombardi and Curio, 1985a). This latter case is particularly instructive in that it demonstrates the difficulty of replicating results. The owl response of zebra finches obtained earlier (Hoffmann, 1979)could-for unknown reasons-only be replicated by subtly changing the context of testing (see Comment in Table I, no. 8). There are intriguing sensitive period effects that determine whether an object is appropriately responded to (nos. 14,22,23 in Table I). Discussion
ASPECTS OF ANTIPREDATOR BEHAVIOR
195
of these effects would go beyond the scope of this review. Discussion of responses to flying predators is deferred to Section 1II.C because of the long-standing contention that the underlying IRM is relatively unspecific. An ecological correlation between the antipredator behavior of captiveborn individuals and the predatory threat to the populations they came from has similarly been used to infer innate differences among the groups concerned. It could be argued that the correlations observed are due to some interaction between a hypothetical population-specific susceptibility to captivity and the development of the behavior under study. However, this objection seems farfetched since, without exception, the correlations mirror, on a ranking scale, the population-specific threat from predation in the wild in guppies (Poecilia reticulata),sticklebacks, minnows (Seghers, 1973, 1974; Breden and Stoner, 1987; Stoner and Breden, 1988; McPhail, 1969; Huntingford, 1982; Giles and Huntingford, 1984; Levesley and Magurran, 1988; Tulley and Huntingford, 1987b, 1988), voles (Chlethrionomys glareolus; Alder, 1975). deer mice (Peromyscus maniculatus; Hirsch and Bolles, 1980), and California ground squirrels (Spermophilus beecheyi: Owings and Coss, 1977; Coss and Owings, 1985). A possible exception is in sticklebacks, where population-specific escape responses to simulated attacks from birds differed in the details of the orientation among wildcaptured and laboratory-raised fish (Giles, 1984), perhaps suggesting an influence of maintenance conditions. Work on anti-snake behavior of snake-adapted versus snake-nonadapted populations of black-tailed prairie dogs broadly parallels the results on ground squirrels, but experience with snakes could have contributed to the population differences found (Owings and Owings, 1979; Loughry, 1988). Only for guppies, sticklebacks, voles, and deer mice did the experimental protocol ensure that individual experience with the predator(s) could not have caused the observed avoidance. The adaptiveness of the avoidance involved was most directly demonstrated by Hirsch and Bolles (1980; Table I, no. 19). They showed that deer mice that failed to recognize predators which they had not lived with in sympatry succumbed to their attacks whereas animals from an area of historical sympatry survived. That the differences between predated and unpredated populations are largely due to genetic adaptations is corroborated in some cases by accompanying differences in antipredator devices that are morphological (McPhail, 1969; Giles, 1987; Reist. 1983), physiological (Coss, 1985), behavioral (escape response: McPhail, 1969), or behavioral in other contexts (agonistic: Tulley and Huntingford, 1988; courtship and female choice: Breden and Stoner, 1987; Stoner and Breden, 1988; mate choice: McPhail, 1969). As a cautionary point, one has to consider that part of these correlations, if not shown otherwise, may be
I96
E. CURIO
due to individual differences. Individual sticklebacks with a heavy armor and many spines were found to be bolder against their fish predators (Reist, 1983). b. Dissection of the Stimulus Pattern into Parts. A number of rules governing coaction of predator and novel bird stimuli have been elucidated above (Section II,A,4,b). Do these rules operate on first encounter with a predator or do they result from some experience with it? Some suggestive results have been obtained by comparing populations of Darwin’s finches with different opportunities for acquiring information on predators. In Darwin’s finches, the eyes of an owl interact with the “rest” of the pattern surrounding them. While the presence of eyes is immaterial for the whole of the owl Gestalt, they are of paramount importance when only the owl’s head is perceived (Fig. 8). There are two effects: There is stimulus compression in that the eyes are scarcely, if at all, effectual in the intact owl, but have an extraordinarily great stimulus value in the owl’s isolated head; the eyes are “compressed” but this becomes clear only when their surroundings are reduced. The same effect can be found, though less dramatically, on the islands of Genovesa and Santa Cruz (Curio, 1969, Fig. 48). On these islands the finches can gain experience with owls, though only on Santa Cruz are adults much preyed upon; on Genovesa, their nests are raided and some immatures or adults are taken by owls (Grant and Grant, 1980).It remains unknown whether the differential compression of the eyes is a consequence of experience (with owls) that differs among the populations concerned. What can be safely concluded is that the compression effect operates independently of any experience with owls. Similarly, the great efficacy of the head alone and the rump alone (see Fig. 9) cannot depend on individual experience with the predator in question. The Galapagos hawk’s (Buteo galapagoensis) head displays a stimulus value comparable to the owl’s head in Fig. 8 (Curio, 1969).Again, since this is so on three islands where the finches are hawk-naive (Wenman, Genovesa, Santa Cruz), experience with the hawk cannot be a prerequisite. It could be argued that an experience with the owl might be generalized to perception of the hawk and determine the rules governing decoding of the hawk’s parts in relation to the whole. However, this is an unlikely explanation since on Wenman Island the finches are both owl- and hawknaive, and the same efficacy of the hawk’s head applies. Furthermore, the stimulus compression observed on Santa Cruz Island, where the hawk’s head and the hawk’s rump together yield more stimulus value than the whole of the hawk, cannot be contingent on experiencing a hawk before. It is remarkable that stimulus compression in the human infant, as elucidated by its response to facila features, is also independent of seeing the whole. (Bower, 1966).
ASPECTS OF ANTIPREDATOR BEHAVIOR
197
The epigenetic basis of stimulus dilation, as found in the pied flycatcher (Section II,A,4,b), remains unknown at present. c . The Multichannel Organization of Enemy Recognition. Six lines of evidence suggest that, in pied flycatchers, owls, shrikes, and harmless birds enter perceptual channels specific to each of these object classes (Section II,A,6). Furthermore, as shown by the deprivation experiment (Table I, no. 9), owls and shrikes are recognized innately, and a live harmless bird (Nymphicus hollandicus), the animate control for predator specificity of the underlying IRMs, was responded to much less than were the predators (Curio, 1975). This ranking of responses parallels that found in the wild. Hence, the decoding of the three object classes fulfils the criterion of innateness (for a possible qualification of the novel bird response, see Section 111,C). It remains to be explored whether the multichannel organization itself is innate or requires experience with any of the objects classified by it.
B. NOVELTYAS
AN EPIGENETIC DETERMINANT OF ANTIPREDATOR BEHAVIOR
A number of birds have been shown to respond more strongly to genuine predators than to harmless birds and inanimate objects (Fig. 3, Section II,A,3). Since these results were obtained with birds in the wild, one could argue that the stronger response given to the predator was due to the predator being rarer than are harmless birds (Schleidt, 1961a,b).This idea, the “rarity principle” (Curio, 1969),predicts that all potentially dangerous objects are initially of equal stimulus value. A difficulty with this idea is that the harmless birds tested were, by design, entirely novel whereas the raptor could have been encountered previously, though rarely. Harmless birds should then have provoked at least the same level of response, which was not the case. One might, however, save the idea that the response to the two classes of stimuli is due to differential novelty by assuming that the test birds conceptualized a class “harmless bird” by generalizing from previous and frequent experience with harmless birds to the novel harmless bird presented to them experimentally. As an alternative to the differential rarity idea, a harmless bird might be any bird that is a nonpredator. A basis for such a negatively defined stimulus class would be the sequential stimulus decoding suggested above (Section II,A,6,c). In a first step of identification, an object would be classified as “bird.” In a second step, a harmless species would be identified as “nonraptor” by not entering any of the raptor-specific channels. This not very stimulusspecific mechanism would not require differential encounter frequencies, as does that based on rarity, but it might need experience with stimuli characterizing what is a bird.
198
E. CURIO
The idea of differential novelty underlying enemy recognition received partial support from Schleidt's (1961a,b)experiments with predator-naive domestic turkeys (Meleagris gallopavo). He demonstrated that chicks of 14-16 weeks of age responded by aerial predator calls to various equalsized silhouettes, regardless of whether they mimicked a raptor or any meaningless object (Fig. 22). Stimulus efficacy was inversely proportional
5
Circle
Hawk
' R a p t o r ' 'Goose'
Rectangle
FIG.22. Response strength (aerial predator "prrr" calls) given by turkey chicks to various equal-sized (30 cm2) silhouettes moving overhead on test days (abscissa). From day 3 on. points denote mean values from 10 trials each. After day 5 three stimuli that were only shown on days 1 and 2, or were novel. displayed stimulus values equivalent to those on days I through 3. Apparent sizes correspond to a hawk seen 27 m above ground. (From Schleidt, I%lb; courtesy of author and Springer Verlag, Berlin, Heidelberg, New York.)
ASPECTS OF ANTlPREDATOR BEHAVIOR
199
to frequency of encounter, apparently irrespective of the particular shape involved. It is important to note that on first encounter all stimuli were absolutely novel (at least the one seen first). They were not effective because of being relatively novel, that is, as compared to a stored “background” of innocuous stimuli, to which subjects had become habituated as a consequence of frequent encounters. This falsifies the notion that relative novelty is the exclusive mechanism underlying decoding based on habituation (Bronson, 1968; see also Section 11,A,3). Although only a limited number of stimuli were tested after habituation had occurred, the result seems also to be at variance with Kagan’s (1970) popular notion of the “discrepancy principle,” which holds that stimuli that differ only mildly from remembered ones are more effective than strongly discrepant stimuli. Schleidt’s (196la,b) finding was taken to resolve the controversy concerning the short-necked key stimulusfor avian fear responses (see Hirsch et al., 1955; Tinbergen, 1957), for Lorenz’s and Tinbergen’s turkeys and pheasants had seen flying geese more often than the short-necked raptors (Schleidt, 1961b; see also Markgren, 1960, for Anatidae). While the differential encounter rate may be one reason for the raptor specificity of the response in the wild, a stimulus specificity independent of rarity cannot be dismissed. In fact, birds have been observed to gear their aerial predator response to the species-specific stimuli (visual pattern, flight style?) of the raptor species and to the threat it poses (refs. in Curio, 1963). Similarly, American coots (Fulica americana) show highly adaptive responses when discriminatingbetween planes, hawks, and eagles that cannot be explained by either the short- versus long-neck dichotomy or their abundance (Grubb, 1977; see also Markgren, 1960; Muller, 1961; Martin and Melvin, 1964). Even the same raptor species may provoke different behavior. While flying in nonhunting style, a sparrowhawk provokes mobbing from woodland birds, whereas when hunting it induces aerial predator calls (Klump, 1984) or silence (Hartley, 1950). Experiments with predator-naive mallard (Anus platyrhynchos) ducklings seem to support the view of an innate superiority of the hawk versus the goose silhouette (Green et al., 1966; Mueller and Parker, 1980), and thus do not confirm the rarity principle advocated by Schleidt (1961a,b). Unfortunately, the models used, the manner of their presentation (height, speed, path length), and the behavior measures used all differed from those in Schleidt’s turkey work. Green et al. (1966) were not even aware of the standardized methodology of stimulus presentation pioneered by Schleidt. Furthermore, the measures used are difficult to interpret biologically. In one study (Green et al., 1966), the measure used (running) was not validated at all, in the other (Mueller and Parker, 1980), the measure
200
E. CURIO
(uariance of heart rate) was backed up by pointing to the correlation between it and the threat posed by the stimulus leading to it. If taken at face value, the studies falsify, like others (nos. 1, 5, 6 , 7 , 8 , 9 , 11, 15, 17, 18, 20 in Table I), one prediction of the rarity principle, that is, that all potentially dangerous objects are initially of equal stimulus value. Furthermore, different genuine predators may be treated, from the start, differently according to the threat they pose (nos. 3, 17, 18, 20 in Table I; see also Martin and Melvin, 1964). Evidence that permits the rejection of any explanation based on absolute novelty of harmless animals at the same time falsifies an alternative idea on their correct classification as mentioned above: This idea is based on individual experience with other harmless species from which to generalize. For the pied flycatcher, this can be dismissed (see Section III,A,2,c). Whether (peaceful) experience with conspecifics could shape the response to absolutely novel harmless animals (beware of any nonconspecific!) is unknown. For an animal to be classified as relatively novel familiar ones must be remembered. In species-rich habitats, more than 40 species can be remembered by a fish (Ebersole, 1977), and probably by great tits (Fig. 20), which is not surprising in view of the enormous number of visual patterns that pigeons can store (von Fersen and Delius, 1989). In paradise fish, a 1-min exposure to a goldfish effects an habituation for at least 3 months (Csanyi et al., 1989).
C . HABITUATION AS
A
DETERMINANT OF ANTIPREDATOR BEHAVIOR
Two interrelated questions can be asked: (a) Is the lower alarm behavior directed to harmless animals in the wild the result of habituation to them as a consequence of their higher abundance? (b) If yes, do prey animals habituate to predators in the wild as well and to what extent?
I . The Rarity Principle The habituation hypothesis of enemy recognition predicts that nonconspecifics should provoke protective responses as a function of their abundance; because of their rarity, predators should rank highest (Schleidt, 1961a,b; Curio, 1969). To test this, we manipulated abundance of the harmless Galapagos dove by capitalizing on its different abundance on different islands. When presented as a mount to Geospiza finches on Genovesa and Santa Cruz Island, responses were stronger on the latter where the dove no longer exists; on Genovesa it is extremely common, feeding on the ground next to the finches (Fig. 23). Similarly, great tits fear a novel bird more than a familiar one (Fig. 20). Hence, the results
ASPECTS OF ANTIPREDATOR BEHAVIOR
30
r
20 1
Ge n o v e s a
01
Santa C r u r 0
1
2
FIG.23. Testing the “rarity principle” by comparing the fear responses to the harmless Galapagos dove on two different Galapagos islands where it differs in abundance. Finches tested were Geospiza difficilis ( n = 10) on Genovesa, with a high density of doves; and Geospizaf. fuliginosa ( n = 10) on Santa Cruz, with f zero density of doves. 1, 2 denote sequence of stimuli. (1) To make responses on Genovesa measurable, mounts were shown at half the distance ( I m) from that on Santa Cruz.(2) Since the response measure used might reflect different degrees of fear in different species, the dove was compared with a similarsized yet moderately effective owl head. The difference between stimuli is significant on Genovesa. (Modified from Curio, 1969; courtesy of Parey, Berlin, Hamburg.)
tend to support the rarity principle for harmless species. Pertinent questions remain unanswered: Does habituation differ depending on the nature of these species, the sequence of encountering them, or other circumstances? Attempts to mimic under captive conditions the diverse processes of habituation to an array of syntopic species have been notoriously jeopardized by the fact that even effective predator stimuli rapidly lose their efficacy (Hinde, 1954a,b; Curio, 1969). This loss appears maladaptive in view of the vulnerability that would ensue if it occurred in nature. Since
202
E. CURIO
stimulus presentations have usually involved the same position of appearance in relation to the subject, the rapid onset and long-lasting nature of the habituation was rightly thought to be an artifact. As shown for domestic and wild fowl, pied flycatcher, and angel fish (Pterophyllum eimecki), a waned response was renewed by changing the site of presentation of a fear/predator stimulus to which habituation had occurred (Shalter, 1975, 1978a; Schleidt et al., 1983). This suggests that the (relative) “lack of habituation to recurring predators in nature, is due, in part, to everchanging relationships of the predator relative to the inanimate environment” (Shalter, 1978a, p. 1219). Similarly, habituation has also been avoided by shifting the subject (chaffinch) from one aviary to another between presentations (Hinde, 1954a). In all these experiments renewed mean responsiveness attained, at most, the same level as before. (A higher level later on may result from shifting the stimulus from a ground position to an overhead one, thus perhaps involving two different predator channels [Shalter, 19751.) By contrast, in a cultural transmission experiment with European blackbirds, response level was dramatically increased far beyond the initial level (Curio, 1988b). A novel honeyeater (Philemon corniculatus) mount attained a conditioned stimulus value when presented at the place where it had been seen during cultural transmission. When, after one-trial learning, the honeyeater was presented at the opposite side of the aviary, its stimulus value had trebled. This shows that conditioned enemy stimuli can also gain in stimulus value by a change in locale. Despite overwhelming evidence bearing out the importance of patternspecific recognition of enemies in the widest sense (Sections II,A,4; 11,B; III,A), Schleidt et al. (1983) still maintain that the rarity principle is sufficient to protect prey from their predators. This mechanism, however, may fail (see also Seyfarth and Cheney, 1980) where a predator has become commoner than harmless species (examples in Curio, 1969), or where harmless species are as rare as are many predators, a common situation, especially in species-rich faunas; too many false alarms to innocuous creatures would be energetically prohibitive. 2. Differential Habituation to Predators and Harmless Species? Prey could escape the dilemma posed by the rarity principle if they habituated to predators less, or not at all, as compared to harmless species. Though not systematically fested, there is a sizeable amount of circumstantial evidence in favor of such a view (Fig. 24). The lower stimulus value of nonpredatory species has been found in all deprivation experiments controlling for the stimulus specificity of genuine enemy recognition (Table I). The response elicited by the dummy red-backed shrike male does not seem to abate until after 6-8 presentations to pied flycatchers of this and
ASPECTS OF ANTIPREDATOR BEHAVIOR
Anti -
Predator
203
Predator
I
Age of Prey Bird
FIG. 24. Schematic representation of habituation to predators and to harmless birds dependent on encounter number, or time. Ordinate is arbitrary.
other less effective shrike dummies, whereas the response to mounts of the roller and the red-backed shrike female, another novel bird (see Section II,A,6,b), appears to wane immediately after the first encounter (Curio, 1975, Fig. 18). Similarly, pied flycatchers that had their territories adjacent to red-backed shrike pairs, and birds from populations living syntopically with red-backed shrikes displayed the same level of response to the male shrike model as did pairs and populations, respectively, living unmolested by shrikes. Again, the male shrike appears immune to habituation (Curio, 1975; see also Mineka and Keir, 1983). Furthermore, paradise fish habituate to free-moving goldfish more rapidly than they do to pike under the same conditions, despite an initially identical amount of interest (Cshnyi, 1985; see also Buitron, 1983; Magurran and Girling, 1986). In other cases, waning of the response is more rapid for the more potent predator stimulus (Melvin, 1969; Hinde, 1954b), but this may be an artifact due to massed presentations in the same position. Likewise, “transfer of habituation” (Hinde, 1954b), which entails reduction of predator stimulus value as a consequence of exposure to less effective stimuli before it (Hinde, 1954b; Melvin, 1969; Martin and Melvin, 1964), may be such an artifact. If it occurred in nature, this would clearly be detrimental. Significantly, other dummy experiments have failed to confirm the effect (Fig. 15; Curio, 1969). Furthermore, langurs (Presbytis entellus) in India that had become fully habituated to native Indians still exhibited the full range of fear responses to Europeans; among the latter, novel movements, like lifting a pair of binoculars, enhanced these responses still further (Vogel, 1975). (It is unknown whether the initial fear of humans is innate which, if true, would violate the hypothesis underlying Fig. 24.) Transfer of habituation may follow different rules when experiences are widely spaced in ontogeny and/or the objects habituated to are inanimate.
204
E. CURIO
For example, Rubel (1970)found that quail (Coturnix coturnix) feared such objects as adults less when they had already encountered them much earlier. The circumstances under which transfer of habituation to fearsome stimuli takes place need further study. In other cases, habituation to the predator may have been obviated by seeing it hunt, though this has not been demonstrated. In sociable weavers (Philetairus socius),alarm calls given to pygmy falcons (Polihierax sernitorquatus) breeding in their colony do not wane at all (MacLean, 1973). Similarly, H. Lohrl (personal communication) found that passerines did not cease alarm calling to a sparrowhawk that lived in an adjacent wood and was seen daily. Further, a pair of pygmy owls refrained form nesting for 3 years while being housed adjacent to an eagle owl’s aviary. As soon as the pygmy owls were shifted to an aviary out of its sight they bred (W. Scherzinger, personal communication). Some casual hunters, like gulls nesting in colonies of terns, tend to hunt more away from the “host colony” rather than robbing nests therein. Accordingly, terns attack foreign gulls rather than their “guest” gulls. Such observations led McNicholl(l973) to contend that the host terns had become habituated to their guest gulls while they remained responsive to same species gulls roaming over the colony from afar. An alternative view, however, may be that the “domestic” gulls, being less prone to hunt in the colony, were correctly classified as harmless by the would-be victim terns. Hence, the habituation view is not necessarily at variance with the view advocated here according to which predators under natural conditions are immune against habituation. Things may be very different when birds have the chance to avoid the locale of a predator that cannot move about. Thus W. Scherzinger (personal communication)observed passerines each spring, after their return from the south, to mob his caged owls (Strix nebulosa, Surnia ulula), yet only for a couple of days. This differs strikingly from the behavior of resident jays toward a free owl (Section II,B,3,b). Thus, when danger is permanent there may be no habituation to it at all, which clearly falsifies part of the rarity principle and calls for some higher order process of enemy recognition. The difference in response may be due to simple habituation. Or, the birds confronting the caged owls may have assessed correctly that mobbing was of no avail: Whatever the strength of the response, the raptors could not be made to move on. Similarly, sociable weavers gave up showing alarms to snakes, which plundered nests in the breeding colony with impunity, perhaps because they recognized that alarms were futile (MacLean, 1973).Thus, the reasons for response decrement may be varied, but this has not been analyzed in detail. (Even for turkeys, the birds Schleidt studied, it remains to be shown if some more
ASPECTS OF ANTIPREDATOR BEHAVIOR
205
realistic raptor model [with flapping flight, nonlinear flight path, etc.] would be immune to habituation. Significantly, Martin and Melvin [ 19641 found a clear superiority of a flying hawk as opposed to its moving silhouette. The naive bobwhite quails [Colinusuirginianus] used, however, did habituate to the live hawk, perhaps due to the unvarying conditions of its appearance [see also Murray and King, 19731.) The opposite from habituation, an increase of distraction display with an increase of encounter frequency, has been observed by Hudson and Newborn (1990) in red grouse (Lagopus lagopus scoticus) encountering red foxes (Vulpes uulpes). This incremental process, best ascribed to sensitization, undermines even more forcefully than does the lack of habituation the special reaction to predators among all stimulus objects eliciting avoidance responses. In conclusion: There is evidence that harmless animals lose their moderately alarming properties as the prey species becomes familiar with them. The underlying habituation, or some higher order risk assessment, accentuates the preexisting distinction between them and genuine predators, which is due to inherent properties of both object classes rather than to different encounter frequencies. There is little evidence that prey become habituated to genuine predators under natural conditions.
D. LEARNING ABOUT PREDATORS: CONTENT A N D MODES In view of the substantial evidence of innate information underlying avoidance of predators in vertebrates (Table I), some questions become pertinent: (a) If and to what extent are these responses altered by experience that relates to predators? (b) What characteristics of predators are learned? (c) Can harmless species, that is, nonspecialist hunters or brood parasites, become recognized as harmful through experience? (d) What are the modes of and the constraints on learning?
1.
What Is Learned? Many vertebrate prey modify their antipredator responses in ways that are extraordinarily flexibile, thereby supplementing their rigid framework of IRMs and preprogrammed startle reflexes. The evidence for this is often based only on the reasoning that the observed fine-tuning of responses is too unlikely to result form innate “wiring.” a. Acquired Predator Species Characteristics. There is a dearth of information as to which and how many animal species (“types”) can come to elicit the protective behavior of prey. Seyfarth and Cheney (1980) inferred from their observations and playback experiments with vervet monkeys that they discriminate four different classes of predator, as
206
E. CURIO
judged from the fact that they give acoustically different alarms to leopards, martial eagles, pythons, and baboons. On hearing the alarms, vervets respond adaptively in terms of risk avoidance. When compared to adults, infant vervets give alarm calls to a significantly wider variety of species, that is, give many false alarms. Additionally, they display more “wrong” responses. However, their signaling is not arbitrary; they restrict leopard alarms to terrestrial mammals, eagle alarms to birds, snake alarms to snakes, and baboon alarms to baboons. How infants come to “sharpen” their discriminative abilities over the years till adulthood is not known; social transmission is a likely candidate. For example, during alarm playbacks infants look at their mothers and the responses are more adultlike if their mothers are nearby. The gradual sharpening, that is, narrowing down to the species level, or to a particular spatial context (Section II,B, I), may build on four innate channels tuned to the four classes of predators mentioned (a possibility not discussed by Seyfarth and Cheney [ 19801). Without conducting a deprivation experiment, however, the innateness of such channels remains conjectural; in view of the high sociality of vervets, cultural transmission, even of these baseline channels, remains a viable alternative (see Section III,D,4). A taxon-wide generalization from an adverse experience with one of the taxon’s members has been demonstrated in bullfinches(end of Section II,A,6,g). This need not imply a difference in the underlying learning process between birds and primates. The one-trial learning (pursuit) by which that predator fear was brought about in the bullfinches vastly differs from the gradual improvement observed in the vervets. It would be important to know whether bullfinches are able to separate out particular species from their taxon-wide fear of an avian family as a consequence of further experience with them. It is as yet uncertain whether the decoding of innately recognized predators differs fundamentally from that of acquired recognition. Furthermore, the process(es) underlying the ontogenetic increase of caution in confronting dangerous predators (Owings and Coss, 1977; Coss and Owings, 1978) awaits elucidation. b. Acquired Predator Individual Characteristics. There are numerous reports that the individual human (Nicolai, 1950; von Frisch, 1964; Brown, 1970; Drost, 1971; Stinson, 1976, Merritt, 1984; McLean and Rhodes, 1991), cat (Lendrem, 19801, or gull conspecific committed to cannibalism (Tinbergen, 1958; Veen, 19771, provokes protective behavior from birds. A reinforcing event has been identified as handling of a brood or an adult, thus mimicking predation (Nicolai, 1950; von Frisch, 1964; Drost, 1971; Stinson, 1976; Merritt, 1984), or true predation itself (Tinbergen, 1958). A particular person may also be singled out, for example, by parent red-
ASPECTS OF ANTIPREDATOR BEHAVIOR
207
winged blackbirds (Agelaius phoeniceus), if that person alone repeatedly visits the nest such that only the familiar visitor provokes bolder defense responses. This difference is thought to result either from habituation of the fear system to the familiar person, or from positive reinforcement following its moving on after each encounter (Knight and Temple, 1986a; see also Brown, 1970). Whatever the reason, the finding is in line with the idea developed above (Section 111,C,2)that the response to nonpredators (= harmless species that are potentially dangerous) becomes modified as a result of peaceful encounters. As they are not game birds, blackbirds almost certainly lack any innate avoidance of humans. This raises the important question whether only the low-keyed responsiveness to harmless species is a prerequisite that imparts on prey the flexibility reflected by recognition of individual adversaries. If so, there would be no individual labeling of genuine predators that are decoded innately. Whether such predators may still be partitioned into classes following habituation to one class is uncertain. Thus, langurs discriminating between morphs of humans (Section III,C,2) may or may not fear them innately. The details underlying such adversary learning may differ fundamentally from those involved in the acquisition of fear of species or higher categories: First, there is no generalization from the individual concerned to the whole of that individual’s species, whereas bullfinches generalize from one predator species to the whole family of that species (see above). Second, compared to genuine predator recognition, they seem to forget the individual they were conditioned to previously; for example, the same mockingbirds (Mimus polyglottos) that harassed a person one summer failed to do so the next (Merritt, 1984; see also Drost, 1971). As with acquired species recognition (see above), there is much scope for experimentation. c . The Behavior of the Predator. Much mobbing (Marler and Hamilton, 1966) and inspection behavior (Magurran, 1986) vis-a-vis a predator is thought to be information gathering. There is also active testing of whether an attack is imminent, for example, it may be dependent on the thermal condition of an ectothermic predator (Rowe and Owings, 1990). There is a general belief that the details of the behavior of such a predator have to be acquired because a n y IRM, should it exist, would appear to be overtaxed. Though one can sympathize with this view there is no hard evidence to support it. Prey animals apparently discern a predator in hunting mood from one that is not (Meinertzhagen, 1959; refs. in Curio, 1963; Berger et al., 1963; Kruuk, 1972; Potts, 1980; Robinson, 1980; Buitron, 1983). The extraordinary behavior (termed “baiting” by Brown [1971]) by a Syke’s monkey (Cercopithecus mitis) vis-a-vis its most dangerous enemy, an
208
E. CURIO
incubating/broodingcrowned eagle (Stephanoaerus coronatrrs),is difficult to categorize. In a number of episodes, the male monkey bounded back and forth over the eagle many times, even touching the nest on occasions, just keeping out of reach. The eagle was visibly molested by these maneuvers, which are reminiscent of mobbing, and for which a number of functional explanations can be dreamed up. When analyzing from film the preattack posture of a red-tailed hawk (Buteojarnaicensis),Grier (1971) was unable to find any cues that might be utilized by prey to predict an attack. There were no differences compared to the movements preceding any change of perch. As correctly observed by Grier, a prey that is targeted visually prior to an attack may well infer from the movements involved that an attack is imminent. This point could not be settled since the prey used were laboratory mice that were unaware of the distant hawk. In an attempt to mimic the situation of a predator in different moods, Licht (1989) presented guppies with a choice of a satiated and a hungry piscivore. Guppies almost invariably chose the satiated one, that is, then avoided the one that continually attempted to prey on them. Unfortunately, this experiment does not address the problem of how prey recognize the subtle details differentiatingdifferent states of readiness to attack; rather it demonstrates, not surprisingly,that overt attacks elicit avoidance. We still do not know how prey animals come to decipher, to their advantage, different states of the predator. More specifically, the question of whether an animal can become aversively conditioned to another one as a consequence of the latter being treated (stationary) near a vulnerable possession (Section II,B,4) cannot be answered for any species.
2. The Effect of Perceiving the Predator Perceiving the complete releasing situation for a response may change the range of effective stimuli. By “priming,” a previously ineffective stimulus acquires eliciting properties through association with initially effective ones so that the range of stimulus objects is broadened, given some degree of similarity between them (Hinde, 1970). Could such a process safeguard a prey against its predators even if these occur in a situation not readily decoded by an IRM? Shalter (1978b) found that 42% of parent pied flycatchers did not mob a pygmy owl mount which others vociferously harassed. When the nonmobbers were presented with a live pygmy owl, all of them mobbed it. When one day later these same birds were again given the pygmy owl mount, all responded in a way indistinguishable from those that had reacted during its first presentation (median call rate 85 and 79/min, respectively). Thus, the range of stimulus objects had increased, although proba-
ASPECTS OF ANTIPREDATOR BEHAVIOR
209
bly not that of the constituent key stimuli, since a stuffed owl lacks such features as movement that the live owl presents. In other experiments with great tits overlooking a tawny owl mount, one head turn by 90" sufficed to induce incessant mobbing of the mount (E. Curio, unpublished). Shaker's (1978b) priming experiment revealed a still unsettled enigma. During an experiment 15 years earlier, employing the same owl mount, Curio (1975) had found that only 8% of the pied flycatchers, that is, significantly less ( p < .001), had failed to mob. One possible explanation is that the densities of owls in the pied flycatcher's central-west African winter quarters might have diminished between the two experiments. If true, this would suggest species differences in the ability to decode owl stimuli since both man-made and natural Kaspar Hausers of several species have been found to respond to a stationary model owl without previous priming with a live one (Table I). A similar consideration applies to the ability to recognize part of the predator without having had a chance to see a whole live one previously (Section III,A,2,a). A rather sophisticated mechanism, perhaps entailing priming sensu lato, was reported by Owings and Coss (1981) for California ground squirrels. Young animals that have on first encounter innately avoided a rattlesnake are thereafter, but not before, reluctant to flee from a human into their burrow. Burrows are the habitual place of retreat when thus threatened. Rattlesnakes routinely enter squirrel burrows to escape the heat or search for squirrel pups. Perception of the snake has apparently been generalized to encompass places that a snake habitually visits. During an encounter in a burrow squirrels are at a disadvantage as compared to aboveground. The fear of a burrow upon perceiving a snake nearby is reminiscent of the sign-of-predator hypothesis suggested above for birds (Section II,B,3,b), though the underlying mechanisms may, of course, differ. There is a dearth of information on priming in relation to adversary avoidance. An increase of distraction displays by red grouse due to a rise of encounter rate with red foxes has been onerously explained by Hudson and Newborn (1990). They suggest that more foxes mean a higher proportion of young foxes; young foxes in turn mean, because of their inexperience, more reward for distraction displays. It would be worthwhile to follow up this functional interpretation. It predicts that predators less in need of education by their prey should not, by their increase in numbers, lead to more pronounced defense. 3 . Pursuit of the Subject As a result of being pursued, animals may rapidly develop avoidance behavior that forestalls a successful attack by the pursuer (e.g., Benzie, 1965: stickleback). In a thoroughly studied case (Dill, 1974: Bruchydunio
210
E. CURIO
rerio), the changes were found to concern the R M responding to a looming stimulus rather than the motor pattern of flight. Similarly, Darwin's finches (Geospiza sp.), which initially allow a human to approach to a distance of 0.5 m, hop away on the ground at an increasing distance as slow pursuit continues (E. Curio, personal observation). With cats, the degree of avoidance initially present does not effectively protect the more ground-living finches against an attack (A. Kastdalen, personal communication). How quickly they develop avoidance behavior as a consequence of being stalked is not known. As a consequence of relaxed predator pressure, mainly from carnivores, island birds have apparently developed a reduced ability to recognize them innately and to learn from being pursued by them. Of all avian species that have become extinct through introduced mammalian predators, 90% have lived on oceanic islands (Johnson and Stattersfield, 1990). Yet, even game animals may lack any innate fear of humans. American elk (Ceruirs elaphirs) are not wary where humans are rare (Altmann, 1958). Pursuit may take quite subtle forms. In predator-naive domestic chicks, a pair of artificial staring eyes elicits an initial avoidance that is enhanced if the eyes are made to track the subject with their gaze (Scaife, 1976b). Unfortunately, this tracking movement was not controlled for by applying other modes of eye movement excluding the threatening gaze. Moreover, prior to testing, the chicks were not naive in terms of a human face, thus marring this and many other similar experiments; the experimenter may unwittingly engender fear from staring eyes while picking the subject up prior to a test (see Section III,A,2,a). Staring at animals, or lifting binoculars to look at them, is believed to scare them only after they have been persecuted (shot at) by man (Goodwin, 1976: corvids; Booth, 1962: Ceropithecus). Nevertheless, continually fixating a particular subject may engender an unusually high degree of fear of humans. During a 5-day observation period, a focal Javan mannikin (Lonchura leucogasrroides) in a flock of conspecifics became dramatically afraid by merely being looked at, so that it hid in plants or a nest box once the observer resumed her observation of it (B. Krause. personal communication). From the above, one may conclude that the widespread innate fear of a pair of staring eyes (Section II,A,4,a) may be reinforced by the subject merely being uisucilly targeted, without any other overt signs of imminent attack. Targeting a victim, being a prelude to an attack, seems likewise to be decoded innately and apparently reinforces an initially low level of avoidance. Whether this enhanced avoidance results from the stare only, or includes the whole of the adversary, is presently unknown. The mere proximity or approach of a human may scare naturally raised birds. As is well known for captive birds, talking or whistling relieves this
ASPECTS OF ANTIPREDATOR BEHAVIOR
21 1
tension in different species to various degrees. The reason probably is that stalking predators are always silent, and when they vocalize they apparently pose less of a risk. 4.
Cultural Transmission of Enemy Recognition
a . Learning in the Presence of a Predator. A protective response may become enhanced by perceiving either a (potential) predator chase, kill, or hold of a (would-be) victim, or an animal being mobbed. In both cases, learning takes place only if the adversary is present. Pursuit of would-be victims by a predator offers another potential source of information on how to survive an attack both to the pursued and to onlookers. The best knowledge presently available is in regard of the response of animals that perceive others being pursued. How this experience translates into protective action later on remains unknown. Many prey animals, such as fish (refs. in Dill, 1974; Suboski e t a / . , 1990). birds (Davis, 1975), and mammals (Gerkema and Verhulst, 1990), flee into cover when they notice others flee who are knowledgeable about an imminent threat. This knowledge may derive from earlier experience with that threat (refs. in Dill, 1974). In many situations, information on the direction in which to flee as a result of observing informed prey animals is crucial. Depending on the species and on the circumstances, the observers either flee into the nearest cover, even at the risk that they thereby approach the predator (Tinbergen, 1951), or they flee in the direction they see others take. What happens when the social information about the direction where an attack is expected to come from interferes with information on a real attack? In an experiment testing the “alerting others” hypothesis of mobbing, Frankenberg (1981) pitted these two sources of information against each other. An observer blackbird had a free view of an actor who mobbed a little owl mount, but the actor could not see a rod which was visible to the observer (Fig. 25; curtain shown by solid and dashed lines). As a result of the interaction, the observer mobbed as well and, when startled by sudden movement of the rod startle stimulus [SS], took off with a significantly lower latency than normal. Taking off was invariably directed away from the SS that the actor could not see. With a small delay, the actor took off in the same direction, that is, away from the owl. With a slight modification of the setup, the actor was allowed to see the SS as well (Fig. 25; curtain solid line only), in order to test for an effect of the actor’s mobbing on its own escape performance. When the owl and the SS were in the same direction from the cages, both birds took off away from the SS (Fig. 26: Tl). However, when the SS startled the birds into flight from the opposite direction to the owl (T2), the actor still fled from
212
E. CURIO
/4 I I +1I Actor
1 m
FIG. 25. Experimental setup to unravel the information content an observer blackbird extracts from the mobbing of an owl by the actor blackbird. The owl is visible only to the actor; the startle stimulus is visible only to the observer in one experiment (both solid and dashed line of c curtained), and to both birds in another (solid line of c only curtained). (Modified from Frankenberg, 1981.)
Actor
c1
11
Observer
QQ QQ Owl
12
ss c2
00 ss
FIG.26. Spatial arrangement of predator stimulus (owl) and startle stimulus (SS) to test for directional information encoded in the mobbing of an actor blackbird when seeing the owl and in the startle response of an observer blackbird when scared by SS. Arrows denote the direction of first takeoff upon receiving stimulation from the conspecific's action in a neighboring cage; thin lines denote the SD of takeoff directions (for details of setup see Fig. 25). CI, C2 and TI, T2 denote control trials and test trials, respectively. in order from top to bottom. See text for discussion. (Modified from Frankenberg, 1981; courtesy of author and Parey, Berlin, Hamburg.)
ASPECTS OF ANTIPREDATOR BEHAVIOR
213
the owl; the observer, with the owl barred from its view, largely behaved the same but part of this group compromised by jumping toward the SS or sideways. Hence, with conflicting information about a potential attack (T2), the real predator had precedence over the SS although it did not move, and, even more surprisingly, the observer apparently rated the information extracted from the actor’s behavior higher than what it sees itself when the SS moves. Two control experiments (Cl, C2), with the SS being the only disturbance, ensured that the direction of escape observed in experiments T1 and T2 was not in any way biased by the geometry of the cages and their environs. Directional information about the place of the predator is probably transferred by the actor’s mobbing behavior. The actor’s way of calling may provide a clue: The call rate increases both after each takeoff away from the owl and after each landing close to it (Frankenberg, 1981). The direction of monocular fixation may be another clue. In domesticated zebra finches there is social facilitation of mobbing among pair mates only one of which can see an adversary. Performance of the knowledgeable bird successfully conveys information about the adversary’s position so that harassment of both mates is directed at it (Hoffmann, 1979). Acoustic information from a male suffices to induce the behavior in a female separated visually from it (Lombardi and Curio, 1985b). A distressed or killed conspecijic near an enemy has been shown to elicit antipredator behavior from individuals or groups (Section II,B,3). The strength of the behavior surpasses that given to the predator alone. As a consequence of such behavior, experienced individuals tend to respond more strongly or earlier on any future occasion when they have the same or a similar encounter, or they avoid the site where it has occurred previously. Foreshadowed by the anecdotal observations of Lorenz (193I), Conover and Perito (1981), and Conover (1987) demonstrated that starlings and ring-billed gulls (Larus delawarensis) mob more vigorously at a predator (owl, human) after having experienced it hold a live, adult conspecific. In both these cases and similar ones (Csanyi, 1985), the experienced birds had partaken in mobbing assembliesaround the threatened or dead conspecific. Therefore, it remains unknown whether merely perceiving the threat and/or the commotion around it would suffice to bring about conditioning. Strangely, pairing the owl with a dead starling or the species’ distress calls failed to render the owl more effective later on (Conover and Perito, 1981). From an experiment with domestic ducks on “empathic learning” it would appear that the mere sight of a distressed conspecific leads to an avoidance of the place of danger (Klopfer, 1957), though both the latter and the aversive stimulus used (electric current) were unnatural. To see whether animals can extract information about a predator by
214
E. CURIO
perceiving it in conjunction with a killed victim, Kruuk (1976) presented a dead gull next to a stuffed predator to mixed gull colonies (Larus argentarus, L . fuscus). Incidentally, this combination of stimuli, simulating an act of recent predation, scared the gulls more than did the sum of the releasing values of each one of them. This furnishes yet another example of stimulus dilation (Section II,A,4,b), demonstrating its validity not only for key stimuli of one Gestalt (predator) but also for a combination of two Gestalten (predator, prey). The releasing values of the predators used, that is, hedgehog (Erinac-euseuropaeus), stoat (Mustela erminea),and red fox (Vulpes uulpes), increased in that order, thus reflecting their biological significance to the gulls. Having seen a stoat with a dead gull, the gulls responded to the stoat thereafter, at the same site, with increased avoidance, as measured by alighting distance (Fig. 27) and greater flock size. A habituation experiment with the stoat only verified that the increase was due to some learning effect. In order to examine whether this effect was due to conditioning to the site of the encounter or to the circumstances of presentation, a control
FIG.27. Avoidance by herring gulls and lesser black-backed gulls of a stoat, a stoat plus a dead gull, and a stoat during the 5-min presentations 1 to 3 (-), respectively. versus three trials with the stoat alone (---). Avoidance was measured by the mean alighting distance of a flock circling above the stimulus. Significance level relates to the difference between trials 1 and 3 in the first-mentioned experiment. (From data in Kruuk, 1976.)
ASPECTS OF ANTIPREDATOR BEHAVIOR
215
experiment was run with a hedgehog being shown in trials 1 and 3, while the combined stimulus of the stoat and gull was presented in trial 2 (Fig. 28). Since experiencing the combined stimulus left the releasing value for the hedgehog unaltered, the learning observed must have been specific for the stoat. This stimulus specificity may suggest that the two predators involved enter two distinct channels (see Section 11,A,6). Unfortunately, the reciprocal experiment testing for any reinforcing role of the hedgehog in trial 2 has not been performed. The experiments carried out so far do not yet permit us to conclude whether the predator attraction itself is important in this learning process; birds that fly away immediately, rather than stay and circle above the enemy, might show the same kind of learning process. The increase of avoidance behavior due to this type of social learning is probably adaptive in coping with predators that engage in surplus killing. Stoats and foxes and, to a lesser degree, hedgehogs are known to belong to these species; a predator that has killed one prey in a place is likely to kill others there once the opportunity arises (Kruuk, 1976). Learning by observing others interact with a predator lies at the heart
- 6
E
c u C
0
4
0
FIG. 28. Avoidance by gulls of a hedgehog in trials 1 and 3 to test for the stimulus specificity of seeing and avoiding a stoat plus a dead gull inbetween (trial 2). *denotes the releasing value of the stoat in the conditioning experiment in Fig. 27. (From data in Kruuk, 1976.)
216
E. CURIO
of cultural transmission of enemy recognition and has become an area of active research. This mode of learning about adversaries safeguards the prey when an IRM is of no avail, for example, after invasion of an area by a predator. Knowledge about the new danger in those transmitting it to novices may in this case have come about by more conventional modes of learning (e.g., Section III,D,3). The experimental evidence on cultural transmission of enemy recognition in the European blackbird and the rhesus monkey (Macaca mulatta) has been summarized (Curio, 1988b; Mineka and Cook, 1988), so a brief outline will suffice here. The basic method, pioneered by Curio et al. (1978a),consists of permittingan enemynaive learner (Lr) to perceive a conspecific teacher (Tr) interact with a predator that is invisible to the Lr, while the Lr is looking at the conditioning object to be feared; this latter object is, in turn, not visible to the Tr but is closely juxtaposed to the dangerous object the Tr is interacting with. This ensures that the Lr regards the conditioning object as something feared by the Tr. The criteria for selecting a conditioning object were as follows: (a) it had to be novel; (b) it had to be unlike any predator that is recognized innately; (c) it had to be similar in size to a dangerous predator. A jay-sized Australian honeyeater (Ho) fulfilled the criteria reasonably well. A test for novelty ensured that the Ho elicited mobbing at only a low level (Fig. 3), though at a level that was higher than the previous response to a wooden box used to rotate the Ho into view of the Lr (Fig. 29, trial 2). In a third trial (reinforcement), this response was reinforced by pairing the Ho with a conspecific mobbing a little owl, thereby raising the Lr’s response level about threefold. In a final test for learning (trial 4),the Ho proved to be about as effective a stimulus eliciting mobbing as is the owl. Repeated presentation of the Ho without any social reinforcement brought about habituation of the novelty response (trial 2) so that sensitization (pseudoconditioning)to the Ho could be ruled out as an explanation of the transmitted response in the trial 4 test. Although mobbing is sympathetically induced in the Lr while perceiving the Tr mob the position of the Ho, it is dispensible for full transmission to occur (Curio, 1988b). In order to discover the extent to which transmission of the Ho was natural, whether learning would occur as well when a subject had previously encountered a potentially dangerous animal in the absence of a knowledgeable Tr was examined. To this end, the Ho was first rendered ineffective by habituating blackbirds to it, and they were subsequently subjected to the conditioning procedure outlined above. As a result, transmission took place unimpaired, thus raising confidence in the naturalness of the transmission procedure substantially. Encountering an adversary without any education does not blindfold the prey to successful education
ASPECTS OF ANTIPREDATOR BEHAVIOR
217
3 3
-0
aJ .-N
?
1
0 0 C
0
f
p
0
1
c
d
v)
0
0
0’
12
0
I Novelty Rcsponsc
2
1
Reinforcement
3
1
Test
4
Stimulus Situations FIG.29. Comparison of cultural transmission as shown by recognition of honeyeater (upper curve) and recognition of a multicoloured bottle. Response strength (RS) was standardized by subtracting the empty box RS value in the relevant experiment from each of the mean RS values of the stimuli presented in the box. Figures beside means denote number of blackbirds tested. (From Curio, 1988b; courtesy Lawrence Erlbaum Associates.)
later on. Similarly, switching the site of presentation after conditioning, for the test of learning, enhances the transmission effect threefold (Curio, 1988b). This demonstrates both the naturalness of this test procedure and the marked power of the transmission itself; in the wild, the predator will appear under ever changing circumstances (Section III,C, 1). To explore the possibility that a n y object could become conditioned, a multicolored plastic bottle was used as a conditioning stimulus for comparison (Fig. 29). In all three trials of the transmission procedure, it scored significantly less. This suggests that there are constraints on learning in regard of the array of stimuli effectively transmitted. This seems to support the view expressed above (Section II,A,6,b) that the presumed novel bird channel is something distinct from an even more hypothetical channel tuned to novel inanimate objects. We do not yet know whether experiential
218
E. CURIO
factors shape the novel bird response, for example, experience with conspecifics that might render any nonconspecific somewhat effective. Because of this, it would be premature to conclude from studies using different species that there are species differences in constraints on learning. Mineka and Cook (1988) have found that flowers could not be transmitted socially to attain enemy valence among rhesus monkeys, whereas a toy snake could. Such a wholesale failure was also found in Kaspar Hauser jackdaws socially conditioned to a toy cat as compared to a live cat or rabbit, both of which worked well (W. Windt. personal communication). While these monkeys and the jackdaws were laboratory-raised, the blackbirds had been trapped in the wild. The question of species differences versus maintenance differences as causative agents of constraints on learning presently remains unresolved. Yet, the jackdaw study teaches us an important lesson about the perceptual basis of transmission: A live cat or rabbit can become an alarm stimulus without any baseline fear of novelty of either stimulus in the naive bird (Windt, personal communication). (This lack of fear of both a natural predator and nonpredator may well stem from a generalization from humans, who raised the birds, to many mammalian species.) Do Lrs pass on the information received? To test this, the Lr of one experiment was made the Tr of the next and so on. This was done by exposing both the trained Lr and the naive Lr to the Ho at a new site simultaneously. It turned out that Lrs could pass on the information received to others along a chain of at least six individuals. Surprisingly, there is no decrement of response intensity, thus showing such transmission for the first time as being capable of subserving a long-term tradition across generations. Tutoring others may transcend the species’ limits. The taped mobbing calls of other species have been found to be as effective as the whole of the conspecific mobber. However, the calls alone lack some information that only the latter can provide. When a conspecific’s calls are the only reinforcer, the Ho needs to be novel; the training procedure fails when the birds had become habituated to the Ho previously (Curio, 1988b). The cross-species tutoring again attests to the naturalness of the underlying learning process; mobbing assemblies are typically composed of many species whose interests in predator avoidance are similar. Cultural transmission of enemy recognition has also been found in the wild, by capitalizing on the endangered conspecific as the reinforcer, that is, one that had been seized by an owl (Conover, 1987). A similarly sophisticated acquisition of an alarm response to a conditioned chemosensory stimulus has been demonstrated in zebra danio (Brachydanio rerio) by Suboski et d.(1990). Alarm substance is released by
ASPECTS OF ANTIPREDATOR BEHAVIOR
219
injury to the skin of these fish and sends a whole group into alarm behavior. When this substance is paired with morpholine, a behaviorally neutral stimulus, the fish learn to respond to this as a consequence of responding to alarm substance. Like blackbirds, zebra danio also have an ability to communicate the acquired recognition of morpholine (i.e., a simulated, unseen predator) to a new group of naive observers. This was, however, examined merely along a chain of one link, thereby mimicking transmission across but one generation. In none of the species investigated so far is the response to the predator geared to the presence of or any affiliation with a potential Lr. By contrast, domesticated zebra finches sympathetically induce a conspecific to mob only if it is a pair-mate. A finch allowed to see both an owl (Gluucidiurn brusiliunurn) and its pair-mate in an adjacent cage shielded from the owl displayed a response about as strong as when it experienced its mate in its own cage harassing the owl (Fig. 30). By contrast, a bird (a potential Tr) adjacent to a randomly selected flock member shielded from view of the owl responded as weakly as it did on a control trial with no owl or when isolated from any conspecific. Hence, there must be positive feedback between the harasser and its mate for the response to occur. This feedback is probably the harassment induced in the observer bird which, incidentally, is also aimed in the direction of the unseen owl (see above, Section III,D,4,a). This interaction between conspecifics as a function of the pairbond raises several questions as to the honesty of the information contained in mobbing. While in the blackbird the mobbing calls serve as a (secondary?) reinforcer, the curlew (Nurnenius arquata) chick learns to respond by crouching to its parents’ aerial predator call only by associating it with a flying raptor. Prior to that, the sight of a raptor alone makes the chick crouch. Here, the reinforcer is the predator whereas the call is conditioned (von Frisch, 1958). It remains unknown though whether the parent’s call is necessary to maintain the initially innate response or to imbue it with raptor specificity. b. Learning in the Absence of a Predator. As reported above (Section III,A, 1) sticklebacks develop their normal antipredator behavior in the absence of any predator only when raised by their father. Significantly, only young from an environment with the predator under study develop the response when thus raised. The mechanism by which this education is achieved is presently unknown, yet work on guppies hints at a possible reason: fish that had been chased by adult conspecifics when newborn escaped capture more successfully (Goodey and Liley, 1986; Tulley and Huntingford, 1987a). Little attention has been devoted to the role of imprinting-like phenomena in the development of vital survival behavior in birds. Csermely et al.
220
E. CURIO
6
“Tuck” 5
Contact Calls
L
3
Standard. 2
/’
Empty Cage
FIG. 30. Mobbing an owl by zebra finches as a function of pair bond. The response strength (RS)was measured by “tuck” contact calls/min (4-min presentations) standardized with reference to the RS elicited by an empty cage (dashed line). Filled circles denote model birds (one for each combination of birds) in the presence of the owl. Unfilled circles denote observer birds in the presence of a model in an adjacent cage (owl not visible). 00, Paired; 00,unpaired birds. Inset figure: Sonagam of “tuck” contact call. (From Curio. 1988b; courtesy Lawrence Earlbaum Associates.)
(1983- 1984) claim that red-legged partridge chicks develop no fear of humans if they happen to see them within 48 hr after hatching (Table I). It is unclear to what extent maternal care contributes to the full level of
fear. According to T. Silva (personal communication), young parrots of various species develop a fear of humans only when they are parentraised, regardless of whether their parents are themselves shy of humans or tame. Whether this observation stands quantitative scrutiny remains to be seen. If true, an explanation based on habituation resulting from affiliation with the human caretaker, which would prevent an IRM from developing properly, might be most parsimonious at present.
ASPECTS OF ANTIPREDATOR BEHAVIOR
22 1
There is a dearth of information on how the various risk-assessment mechanisms come to operate. An exception to this is a noteworthy observation by Trost (see Moholt, 1989) on how magpies develop recognition of the dead conspecific and, thus, risk assessment based on the “sign-ofpredator.” A hand-raised magpie failed to mob a dead conspecific. By contrast, another magpie, raised later in the presence of that older individual, readily mobbed a dead one. It appears that experience with a live companion is necessary for the response to a dead one to develop. Interestingly, mobbing episodes by the second, socially less deprived bird in encounters with a deceased magpie increasingly induced the response in the deficient bird. These observations indicate that the possibility of social effects bringing about the typical corvid response to dead conspecifics through an IRM cannot be ruled out: the potential shortcomings of any experimental deprivation are always a problem (Section III,A,l). c. The Conservation Relevance of Cultural Transmission. The message of Sections a and b above for conservationists faced with the problem of releasing captive-bred animals into the wild is clear. Given appropriate techniques of cultural transmission or their substitutes, the success of such releases (Suboski and Templeton, 1989) or relocations (McLean and Rhodes, 1991) may be considerably improved. The question of whether hand-raised chicks of various grouse species really habituate to predators more quickly than parent-raised ones, or whether they do so at all (Dowell, 19861, needs closer study.
IV. CONCLUSIONS A. CAUSAL ASPECTS Evidence keeps accumulating that antipredator behavior is achieved by three rather different ways of stimulus decoding. First, there is abundant evidence that predators are discriminated typologically down to the species level. This mode of stimulus evaluation gives rise to predator-specific defense/escape responses, the adaptive nature of which has been repeatedly established (e.g., Kruuk, 1964; Curio, 1975) but has not been discussed here. Even if the motor pattern of a response does not vary with predator species, even though the latter differ considerably along many stimulus dimensions, predator-specific channels can be shown to exist. Such multichannel organization of stimulus decoding (Section II,A,6) suggests that types of predator are somehow respresented in the receiver as different qualities. Being part of that system, the close relationship between key stimuli often precludes breaking down experi-
222
E. CURIO
mentally the whole of an enemy “Gestalt” into its parts. It is this stimulus interaction that prevents confusion of enemies with similar yet harmless species. Second, predator type recognition is clearly modulated by conrexr (e.g., location, own vs. neighbour’s territory, “endangeredness” of group member). Decoding involves the relationship between the adversary and a complex background and, thus, defies any simple description in terms of separable key stimuli. Context may outweigh the importance of predator type. The interpretation of an experiment negating the importance of context, as compared to the predator’s species per se, was shown to be flawed. Further, for some birds, an aerial predator may turn into a terrestrial one as soon as it lands, as measured by the responses it provokes before and after (Section II,B,l). If one assumes that a flying raptor is more dangerous than a walking one, the prey concerned may be thought of ascribing a particular level ofrisk to each predator that changes with the circumstances under which it is perceived. The attributes of predator type and context may summate heterogeneously so that both together translate into a given level of risk. A less harmful predator may provoke the same response as a more dangerous one if occurring at closer range. The potentially extraordinary power of context is, among other things, born out by the “principle of staying put”: By being experimentally made to stay near a defender’s nest, an innocuous species will assume predator valence (Section 11,B,4). At the same time, the finding demonstrates that staying still can replace enemy-specific stimuli entirely, though it must be appreciated that some minimal stimulus requirements must be met; an inanimate object, though it is stationary, does less well. Neurobiologists are optimistic that the rules of stimulus filtering and stimulus coaction underlying the functioning of RMs at the neural level will be unraveled soon. A word of caution may be justified. First, for such an analysis, localized key stimuli may be eminently suited, yet diffuse key stimuli, so common in enemy recognition (Section II,A,3,a), may not be. Second, the exceedingly complex interrelationship of a compound stimulus and its context, itself often a network of spatial and social, experiential and unlearned factors, may defy any attempt to break it down into discrete operations at the neuronal level. At present, such attempts appear beyond the grasp of even the most sophisticated techniques of neurobiology. Third, prey animals apparently make use of a number of risk-assessment mechanisms that safeguard them even in the absence of any overt predator cues. Though they are diverse, these “hidden-risk” mechanisms have received the least attention. For example, animals attend by antipredator behavior to the following cues: The acoustic signals of others who have perceived a predator (unclassifiable risk; Section
ASPECTS OF ANTIPREDATOR BEHAVIOR
223
II,A,4,c); the remains of a fresh prey (sign-of-predator; Section II.B.3.b); an especially vulnerable (e.g., sick or otherwise odd) individual that is liable to attract an enemy’s attention is preemptively attacked or killed (Section II,B,3,b); the disappearance of an enemy. This latter “object permanence,” resulting in increased vigilance, is likely to forestall surprise attacks from the place of disappearance (Section II,B,3,b). While most vigilance may be relatively unspecific with respect to the adversary involved, as are the risk-assessment mechanisms mentioned above, object permanence and the “hallucination” of a particular, yet unseen predator (Section II,B,3,b) are not; these latter phenomena suggest that some mental representation of a particular predator does exist. The learned avoidance of risky places (Section II,B,I) may belong to this little known category of protective behaviors, too. When well studied, these hiddenrisk-assessment mechanisms may turn out to represent channels in their own right, thus adding to the number of enemy-specific (and harmless animal) channels established already (Section 11,A,6). kt is a challenge to future research to also study the potential relationships of such risk assessment with enemy-specific channels, thereby learning about how specific to particular dangers these assessment mechanisms actually are. While some risk-assessment mechanisms may lend themselves to a feature detector-centered neurobiological analysis (e.g., the sign-ofpredator paradigm), the majority will best be viewed with less optimism. Since most of them operate in the absence of predator stimuli or have to rely on the animal remembering them, an analysis at the neural level seems out of reach at present. Classical key stimulus analysis has thus been supplemented by the still rudimentary analysis of context of encounter and the assessment of hidden risk. While risk, being a common denominator of all antipredator responses, is implicated at all three levels of danger assessment, it should not be forgotten that in no species have all three levels been looked at or are even known to occur. However, the assumption that the identification of danger from enemies will always involve some sort of risk assessment seems a robust one. It is already clear that a strictly causal analysis of that identification process will profit from incorporating the concept of risk assessment in addition to the concepts of classical stimulus analysis. From this it follows that a study of causarion is bound to incorporate aspects of function if it is not to run the risk of remaining rudimentary. B. DEVELOPMENTAL ASPECTS When operationally defined, innate recognition of enemies has been abundantly demonstrated in a large number of prey species (Table I).
224
E. CURIO
Recognition and appropriate risk assessment, are demonstrably accomplished by attending to predator-specific stimuli rather than to novelty. The claim that “appraisal of threat” requires experience with the enemy in question (McLean and Rhodes, 1991) is largely unwarranted. Novel, harmless, yet potentially dangerous species also elicit some antipredator behavior, which, however, is invariably weaker than that released by genuine predators. The “rarity principle” holds that predators are avoided in proportion to and because of their (relative) rarity (Schleidt, 1961a,b). Accordingly, harmless species, being more abundant, are usually feared less following habituation, but can take on predator valence when they are novel or rare. Experimental habituation weakened the effect of predator and nonpredator dummies alike, thereby seemingly supporting the hypothesis. I have argued that habituation to predator dummies was probably due to the standardized, monotonous conditions of stimulus presentation. In the wild, rarity does not successfully explain the discrimination among various aerial predators (Section III,C,2). Instead, the rarity principle may survive in a more refined version. According to this, harmless species are habituated to as they are encountered in the wild while genuine predators may prove immune to habituation (Section 111,C).This contrast in organization needs further examination. While it is known that parts of the compound predator stimulus are recognized prior to any experience with the whole Gestalt (Section 111,A,2,b),much remains to be learned of how experience may alter the coaction of key stimuli. Nevertheless, the multichannel organization of enemy recognition is extremely well founded compared with most ethological theories, as judged by the number of facts supporting it (Section II,A,6). However, though the innate nature of some of the channels has been established by the deprivation technique, it is still unknown whether the functional independence of the proposed channels does or does not also require experiential input from the predators they are tuned to. Similarly, we know next to nothing about how the evaluation of context and hidden risk is affected by experiential factors. The ways in which harmless, yet potentially dangerous species come to function as enemies when perceived are highly diverse. Though the learning processes involved may hold no great surprises, the ways in which the learning mechanisms come to operate need to be studied. Three questions are especially intriguing. First, where an IRM (as defined in Section III,A,l) has been shown to safeguard an animal, individual experience with the predator concerned seems to improve recognition very little. California ground squirrels may be an interesting exception to this rule. It seems that learning changes
ASPECTS OF ANTIPREDATOR BEHAVIOR
225
markedly the responsiveness to harmless species that initially elicit only moderate levels of avoidance. As a result, responsiveness abates (see above: habituation), or becomes enhanced. This malleability seems to separate the harmless-animal channel from the genuine-predator channels, as first conceived in the pied flycatcher. It is perhaps no coincidence that in two out of three cases (blackbird, teleost) of cultural transmission (see below) the object learnt was initially of no biological relevance. Second, how is cultural transmission of enemy recognition achieved in the absence of the predator to be avoided? The answer to this problem may happen to be nontrivial (Section III,D,4,b). Third, the developmental basis of cultural transmission in the presence of the predator, as established in a bird, a monkey, and a teleost fish (Section III,D,4,a), remains to be explored. To what extent does transmission depend on experience with the reinforcer, that is, conspecific versus alien alarm behavior, and/or on experience with alien harmless and predatory species? Further, the potential impact of bonding between the novice and the knowledgeable teacher on transmission (Section III,D,4.a) is a virtually unexplored field, both in causal and functional terms.
v.
SUMMARY
The present review focuses on antipredator behavior in vertebrates as elicited by visual stimuli. Prey animals utilize three major mechanisms of predator stimulus decoding to forestall an attack. First, there is enemy identification down to the class level, with each enemy class provoking a different response, or entering a distinct afferent channel tuned to it. In this multichannel organization underlying the decoding process, highly diverse predators elicit the same response. This perceptual organization is accompanied by a close coaction of predator key stimuli, thus preventing confusion of enemies with similar yet harmless species. Second, enemy recognition is often crucially modified by context. In conjunction with predator type, context dependence of stimulus evaluation translates into a perceived risk that continually changes with the circumstances of an encounter. The importance of context is forcefully borne out by the effect of a stationary novel (i.e., nonclassified) animal close to something which is at stake. Stationariness can completely replace predator key stimuli in eliciting defense behavior. Third, apart from assessing overt risk, prey animals make use of various risk-assessment mechanisms even in the absence of any overt predator cues. Though they have been studied least, these hidden-risk mechanisms are already known to be highly diverse and to consist, for example, of an assessment of unclassifiable risk, of risk
226
E. CURIO
permanence (resulting from object permanence) after the predator’s disappearance, and of the risk posed by the presence of an especially vulnerable prey conducive to attack. The enemy specificity as well as the relationship of these risk-assessment mechanisms to predator-specific channels remain to be explored. Skepticism is expressed against the overoptimistic view that an understanding of decoding processes at the neural level will be achieved soon. The implication of risk assessment at all three levels of perception (i.e., of predator type, context, and cues of a predator even in its absence) renders such a view naive. Risk is a functional concept. The existence of a number of risk-assessment mechanisms deems any attempt to indulge in a classical stimulus analysis of predator cues alone doomed to failure. These mechanisms make it clear that an analysis of behavior causation in proximate terms will be rudimentary at best unless the functional question of risk is asked. For the normal development of behavior, individual experience with the predator is largely dispensable. Accordingly, the deprivation experiment is eminently suited for a study of innate enemy recognition. When operationally defined (Section I), innate stimulus-specific recognition and risk assessment have been shown to exist in a large number of prey species. Novelty per se has some releasing value which, however, is invariably less stimulating than enemy-specific stimulus patterns. How predatorspecific channels come to attain their functional independence of each other is unknown, though decoding by various channels has been shown to be innate. Parts of a predator can be properly identified prior to any experience with the whole of the Gestalt. However, the ways in which the rules underlying stimulus coaction change during ontogeny are unknown. Similarly, there is a dearth of information on the development of the mechanisms which decipher context and hidden risk. According to the rarity principle, predators were thought to be avoided because of their rarity. Evidence on habituation to predators in the wild, the key variable underlying this idea, is at variance with the rarity principle. It may apply when restricted to the identification by prey animals of harmless species. However, the idea even fails when applied to the response to the flying raptor, for the recognition of which it was originally proposed. Whereas individual experience is apt to change the responses to harmless, moderately aversive species, genuine predator-specific IRMs appear to be immune to such modification. The ways by which experience modifies responses to harmless yet potentially dangerous animals are predatory pursuit, experiencing such pursuit in other prey, priming via an encounter, parental care in the absence of any predator, and cultural transmission in
ASPECTS OF ANTIPREDATOR BEHAVIOR
227
the presence of the predator. For the most part, the experiential factors modulating the latter learning process remain to be explored, especially the role of pair-bonding between the novice and the knowledgeable teacher.
Acknowledgments This review owes its gestation to nearly 40 years of field and laboratory work in Germany. Spain, and the Galapagos Islands. During this work many students happily helped, and I have freely borrowed from the published and unpublished studies of many graduate students (H.-J. Augst, U. Ernst, W. Hoffmann, G. Klump. B. Stevens, W. Vieth, P. Volkel, A. Zell) and guests (E. Frankenberg, C. Lombardi. M. Shaker) in our Bochum research group. Dr. W. Winkel (Arbeitsgruppe fur Populationsokologie. Institut fur Vogelforschung, Wilhelmshaven) aided our field work with the great tit in his study areas near Wolfsburg. P. J. B. Slater, M. Milinski, W. Windt, and an anonymous referee critically read the final draft of this paper. Mrs. G. Croitoru typed various drafts of it. The Deutsche Forschungsgemeinschaft has been funding the work since 1960 by numerous grants. To all these individuals and institutions I am deeply grateful.
References Alder, E. M. (1975). Genetic and maternal influences on docility in the skomer vole, Clethrionomys glareolits skomerensis. Behau. B i d . 13, 25 1-255. Altmann. M. (1958). The Right distance in free-ranging big game. J. Wildl. Manage. 22, 207-209. Altmann. S . A,. and Altmann. J. (1970). Baboon ecology. Bibl. Primatol. l2, 171-188. Andersson. M. ( I971 1. Breeding behaviour of the long-tailed skua Stercororirts longicaudits (Vieillot). Ornis Scand. 2, 35-54. Andrew. R. J., and Clayton, D. A. (1979). Effects of testosterone on investigation of stimulus change by the domestic chick. Behauiour 69, 135-144. Augst. H. J. (1975-1976). Zur Wirksamkeit von Haaverhalten auslosenden Reizsituationen bei Meisen. Diploma thesis. Ruhr-Universitat Bochum. Augst, H. J. (1977). Meisen (Parus)erkennen den Grad der Gefahrdung durch einen Feind. J . Ornithol. 118, 301-305. Baerends. G . P., and Drent, R. H. (1982). The herring gull and its egg. Behrtuiour 82, 1-416. Barash. D. P. (1976). Mobbing behavior by crows: The effect of the "crow-in-distress" model. Condor 78, 120. Benzie. V. L. (l%5). Some aspects of the anti-predator responses of two species of stickleback. Ph.D. thesis, Oxford University. Berger, D. D., Hamerstrom. F., and Hamerstrom. F. N. (1963). The effect of raptors on prairie chickens on booming grounds. J. Wild/. Manage. 27, 778-791, Bertram, B. C. (1980). Vigilance and group size in ostriches. Anim. Behau. 28, 278-286. Booth. C. (1962). Some observations on behavior of Cercopithecus monkeys. Ann. N . Y. Acad. Sci. 102, 477-487. Bower, T. G. R. (1966). Heterogeneous summation in human infants. Anim. Behau. 14, 389-398. Breden, F., and Stoner, G. (1987). Male predation risk determines female preference in the Trinidad guppy. Nature (London) 329,831-833.
228
E. CURIO
Bronson, G. W. (1%8). The fear of novelty. Psychol. Bull. 69, 350-358. Brown, L. (1970). “Eagles.” Barker, London; Arc0 Publ. Co.. New York. Brown, L. H. (1971). The relations of the crowned eagle Stephanoadtrrs coronafus and some of its prey animals. Ibis 113, 240-243. Bruckner. G. H. ( 1933). Untersuchungen zur Tiersoziologie, insbesondere zur Auflosung der Familie. Z. Psychol. 128, 1-1 10. Buitron. D. (1983). Variability in the responses of black-billed magpies to natural predators. Behaviour 87, 209-236. Burger. J.. and Gochfeld. M. (1981). Discrimination of the threat of direct versus tangential approach to the nest by incubating herring and great black-backed gulls. J . Comp. Physiol. Psychol. 95, 676-684. Burger. J.. Gochfeld, M.. and Murray, B.G.. Jr. (1991). Role of a predator’s eye size in risk perception by basking black iguana. Ctenosaura similis. Anim. Behau. 42, 471-476. Burghardt, G., and Greene. H. W. (1988). Predator simulation and duration of death feigning in neonate hognose snakes. Anim. Behau. 36, 1842-1843. Burkhardt. D. (1990). Sinnesorgane: Selektive Projektion und Kontrolle des Verhaltens. Verh. Dtsch. Zool. Ges. 83, 73-88. Caine, N . G. (1990). Unrecognized anti-predator behaviour can bias observational data. Anim. Behau. 39, 195-197. Caraco. T. (1979). Time budgeting and group size: A test of theory. Ecology 60,618-627. Caraco. T.. Martindale. S., and Pulliam, H. R. ( 1980). Avian flocking in the presence of a predator. Nature (London) 285,400-401. Chandler, C. R.. and Rose, R. K. (1988). Comparative analysis of the effects of visual and auditory stimuli on avian mobbing behavior. J . Field Ornifhol. 59, 269-277. Clayton, D. A.. and Andrew, R. J. (1979). Phases of inhibition and response during investigation of stimulus change by the domestic chick. Behauioirr 69, 36-56. Collias, N. E. (1960). An ecological and functional classification of animal sounds. Am. Inst. Biol. Sci. Pub. 7 , 368-391. Conover, M. R. (1987). Acquisition of predator information by active and passive mobbers in ring-billed gull colonies. Behauioirr 102, 41-57. Conover. M. R., and Perito. J. J. (1981). Response of starlings to distress calls and predator models holding conspecific prey. Z . Tierpsychol. 57, 163-172. Coss. R. G. (1970). The perceptual aspects of eye-spot patterns and their relevance to gaze behaviour. I n “Behaviour Studies in Psychiatry” (C. Hutt and S . J. Hutt. eds.), pp. 121-147. Pergamon, Oxford. Coss, R. G. (1978a). Development of face aversion by the jewel fish (Hemichromis bimaculatus, Gill. 1862). Z. Tierpsychol. 48, 28-46. Coss, R. G. (1978b). Perceptual determinants of gaze aversion by the lesser mouse lemur (Microcebus murinrrs). the role of two facing eyes. Behauiour 64, 248-270. Coss, R. G. (1979). Delayed plasticity of an instinct: Recognition and avoidance of 2 facing eyes by the jewel fish. Deu. Psychobiol. It, 335-345. Coss, R. G. (1985). Evolutionary restraints on learning: Phylogenetic and synaptic interpretations. I n “Memory Systems of the Brain” (N.M. Weinberger, J. L. McGaugh, and G. Lynch. eds.). pp. 253-278. Guilford Press. New York. Coss. R. G . . and Owings, D. H. (1978). Snake-directed behavior by snake naive and experienced California ground squirrels in a simulated burrow. Z. Tierpsychol. 48, 421-435. Coss, R. G., and Owings, D. H. (1985). Restraints on ground squirrel antipredator behavior: Adjustments over multiple time scales. I n “Issues in the Ecological Study of Learning” (T. D. Johnston and A. T. Pietrowicz, eds.), pp. 167-200. Erlbaum. Hillsdale, NJ. Coutlee, E. L. (1971). Vocalizations in the genus Spinus. Anim. Behau. 19, 556-565. Csiinyi, V. (1985). Ethological analysis of predator avoidance by the paradise fish (Macropo-
ASPECTS OF ANTIPREDATOR BEHAVIOR
229
dtrs opercrtlnris L. ). I. Recognition and learning of predators. Bc,lriruiot/r. 92. 227240. Csanyi. V.. Csizmadia. G.. and Miklosi. A. (1989). Long-term memory and recognition of another species in the paradise fish. Anirn. Beltiru. 58, 908-91 I . Csermely. D.. Mainardi. D.. and Spano. S. (1983-1984). Escape-reaction of captive young red-legged partriges (Alectoris rrrfa) reared with or without visual contact with man. Appl. Anim. Etltol. 11, 177-182. Cully. J. F.. Jr.. and Ligon. J . D. (1976). Comparative mobbing behavior of scrub and Mexican jays. Auk 93, 116-125. Curio. E. (1963). Probleme des Feinderkennens bei Vogeln. Proc. In!. Ornithol. Congr. 13, 206-239. Curio, E. (1965). Zur geographischen Variation des Feinderkennens einiger Darwinfinken (Geospizidae). Verh. Disch. Zool. Ges. Zi)iil. Anz. 28. 466-492. Curio. E. (1969). Funktionsweise und Stammesgeschichte des Flugfeinderkennens einiger Darwinfinken (Geospizinae). Z. Tierpsgchol. 26, 394-487. Curio. E. ( 1975).The functional organization of anti-predator behaviour in the pied flycatcher: A study of avian visual perception. Anim. BeAau. 23, 1-1 15. Curio, E. (1976). "The Ethology of Predation." Springer Verlag, Berlin. and New York. Curio. E. (1978).The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Z. Tierpsvchol. 48, 175-183. Curio. E. (1979). Fehlen eines optischen Verstarkers verstarkt eine Lautdressur von Kohlmeisen: Ein nichtklassifizierbares Risiko? Verlr. Disch. Zool. Ges. 72, 221. Curio. E. (1988a). Relative realized life span and delayed cost of parental care. Am. Ntri. 131.82 1-836. Curio. E. (l988b).Cultural transmission of enemy recognition by birds. In "Social Learning: Psychological and Biological Perspectives" (T. Zentall and B. G. Galef. eds.). pp. 75-97. Erlbaum, Hillsdale, NJ. Curio. E. (1989). Some aspects of avian mortality patterns. Mitt. Zool. M i l s . Brrl. 65. Suppl. 13,47-69. Curio. E.. and Regelmann. K. (1985). The behavioural dynamics of great tits (Pirrrrs ,nirjor)* approaching a predator. Z. Tierpsvchol. 69, 3- 18. Curio. E.. Blaich. R.. and Rieder. N. (1969). Der Funktionszusammenhang zwischen einer Handlung und der ihr zugrunde liegenden Erregung als Grundlage der Ethometrie von Schliisselreizen. Z. Vergl. Phvsiol. 62, 301-3 17. Curio. E., Ernst. U.. and Vieth. W. (1978a). The adaptive significance of avian mobbing. 11. Cultural transmission of enemy recognition in blackbirds: Effectiveness and some constraints. Z. Tierpsvchol. 48, 184-202. Curio. E.. Augst. H. J.. Bocking. H. W.. Milinski. M.. and Ohguchi. 0. (1978b). Wie Singvogel auf Feindrufe hassen lernen. J . Orniiltol. 119, 23 1-234. Curio. E.. Klump, G.. and Regelmann. K. (1983). An anti-predator response in the great tit (Partrs major): Is it tuned to predator risk? Oecologia 60, 83-88. Davis, J. M. (1975). Socially induced flight reactions in pigeons. Anim. Belrtru. 23,597-601. Denson. R. D. (1979). Owl predation on a mobbing crow. Wilson B i t / / . 91, 133. Dieterlen. F. ( 1959). Das Verhalten des syrischen Goldhamsters (Mesoc,riceirrs ittrruirrs Waterhouse). Z. Tierpsvchol. 16, 47-103. Dill, L. M. (1974).The escape response of the zebra danio (Britcliyfirnio rerii)). 11. The effect of experience. Anim. Behau. 22, 723-730. Dimond. S..and Lazarus. J. (1974). The problem of vigilance in animal life. Bririn. Behou. E d . 9, 60-79. Dowell. S . (1986). The development of anti predator responses in gamebird chicks. Gtrmc Conservancy Annu. Reu. 18,93-98.
230
E. CURIO
Drost. R. (1971). Uber das Verhalten freilebender Teichhuhner (Gollinrrla chloropirs) gegenuber Menschen. Vogelwarte 26, 175-182. Duckworth. J. W. (19911. Responses of breeding reed warblers Acrocephalus scirpaceus to mounts of Sparrowhawk Accipiter nisus. Cuckoo Cucrrlus canorus and jay Garrulus glandarius. Ibis 133, 68-74. Ebersole. J . P. (1977). The adaptive significance of interspecific territoriality in the reef fish Eupornacentrus leucostictus. Ecology 58, 9 14-920. Edmunds, M. (1974). “Defence in Animals.” Longman, Essex, New York. Elgar, M. A. (1989). Predator vigilance and group size in mammals and birds: A critical review of the empirical evidence. Biol. Rev. Cambridge Philos. Soc. 64, 13-33. Ewert. J. P., and Traud, R. (1979). Releasing stimuli for antipredator behaviour in the common toad Bufo bufo (L.).Behauiour 68, 170-180. Ferguson. J. W. H. (1987). Vigilance behaviour in white-browed sparrow-weavers Plocepasser mahali. Ethology 76, 223-235. Fox, M. W. (1972). Socio-ecological implications of individual differences in wolf litters: A developmental and evolutionary perspective. Behauiour 41, 298-313. Francq. E. N. (1%9). Behavioral aspects offeigned death in the Opossum Didelphis rnarsupialis. Am. Midl. Nat. 81, 556-568. Frankenberg, E. (1981 ). The adaptive significance of avian mobbing. 1V. “Alerting others” and “perception advertisement” in blackbirds facing an owl. Z. Tierpsychol. 55,97-118. Fraser, D. F., and Huntingford, F. A. (1986). Feeding and avoiding predation hazard: The behavioural response of the prey. Ethology 13, 56-68. Fraser. D. F., and Mottolese. T. N. (1984). Discrimination and avoidance reactions towards predatory and nonpredatory fish by blacknose dace, Rhinichthys atratulus (Pisces: Cyprinidae). Z. Tierpsychol. 66, 89-100. Galef, B. G., Jr.. and Nord. S.. (1975). Observational learning of a discriminated flight response by Norway rats. MS. Galloway. D. M. (1970). The Oxford expedition to the Falkland Islands 1969. Predator recognition in two species of Falkland Islands passerines. Bull. Oxford Uniu. Explor. Club 18, 27-54. Galloway. D. M. (1972). An alternative to mobbing as a measure of predator recognition. Br. Birds 65, 522-526. Gallup, G. G . . Jr., Nash. R. F., and Ellison, A. L., Jr. (1971 ). Tonic immobility as a reaction to predation: Artificial eyes as a fear stimulus for chichens. Psychon. Sci. 23, 79-80. Gallup, G. G., Jr., Cummings. W. H., and Nash. R. F. (1972). The experimenter as an independent variable in studies of animal hypnosis in chickens (Gallus gallus). Anim. Behau. 20, 166-169. Gard, N. W.. Bird, D. M., Densmore, R., and Hamel, M. (1989). Responses of breeding American kestrels to live and mounted great horned owls. J . Raptor Res. 23, 99-102. Gerkema. M. P., and Verhulst, S. (1990). Warning against an unseen predator: A functional aspect of synchronous feeding in the common vole, Microtrts arualis. Anim. Behau. 40, 1169-1 178. Geyr von Schweppenburg, H. Frhr. (1958).Toten von Artgenossen. J . Ornithol. 99,389-393. Gilbert. B. K. (I%&. Development of social behavior in the fallow deer (Duma dama). 2. Tierpsychol. 25, 867-876. Giles, N. (1984). Development of the overhead fright response in wild and predator-naive three-spined sticklebacks, Gasterosteus aculeatus L. Anim. Behau. 32, 276-279. Giles. N. (1987). Population biology of three-spined sticklebacks, Gasterosteus aculeatus, in Scotland. J . Zoo/. 212, 255-265. Giles, N.. and Huntingford, F. A. (1984). Predation risk and inter-population variation in
ASPECTS OF ANTIPREDATOR BEHAVIOR
23 1
anti-predator behaviour in the three-spined stickleback, Gasterosteus aculeatus L. Anim. Behav. 32, 264-275. Goldman, P. (1980). Flocking as a possible predator defense in dark-eyed juncos. Wilson Bull. 92, 88-95. Goodey, W.. and Liley. N. R. (1986). The influence of early experience on escape behaviour in the guppy (foecilio rericulata). Can. J . Zoo/. 64, 885-888. Goodwin, D. (1952). A comparative study of the voice and some aspects of behaviour in two old-world jays. Behaviour 4, 293-3 16. Goodwin, D. (1953).The reactions of some nesting passerines towards live and stuffed jays. Br. Birds 6, 193-201. Goodwin. D. (1976). "Crows of the World." Br. Mus. (Nat. Hist.). London. Grant. P. R., and Grant, B. R. (1980). The breeding and feeding characteristics of Darwin's Finches on Isla Genovesa, GalBpagos. Ecol. Monogr. 50, 381-410. Green, M., Green, R.. and Carr. W. J. (1966). The hawk-goose phenomenon: A replication and an extension. fsychon. Sci. 4, 185-186. Greig-Smith. P. W. (1980). Parental investment in nest defence by stonechats (Saxicola torquata). Anim. Behau. 28, 604-619. Crier, J. W. (1971). Pre-attack posture of the red-tailed hawk. Wilson Bid/. 83, 115-123. Grubb, T. C., Jr. (1977). Discrimination of aerial predators by American coots in nature. Anim. Behav. 25, 1065-1066. Gyger. M., Marler, P.. and Pickert, R. (1987). Semantics of an avian alarm call system: The male domestic fowl, Callus domesticus. Behaviour 102, 15-40. Hailman, J. P. (1967). The ontogeny of an instinct. Behauiour, Suppl. 15, 1-159. Hailman, J. P. (1970). Comments on the coding of releasing stimuli. I n "Development and Evolution of Behavior" (L. R. Aronson, E. Tobach. D. S. Lehrman. and J. S. Rosenblatt, eds.). pp. 138-157. Freeman, San Francisco. Hamerstrom, F., Berger, D. D., and Hamerstrom. F. N., Jr. (1965). The effect of mammals on prairie chickens on booming grounds. J. Wildl. Manage. 29, 536-542. Hamilton, W. D. (1971). Geometry for the selfish herd. J . Theor. B i d . 31, 295-31 I . Hartley, P. H. T. (1950). An experimental analysis of interspecific recognition. Symp. Soc. Exp. Biol. 4, 313-336. Harvey, P. H., and Greenwood, P. J. (1978). Anti-predator defence strategies: Some evolutionary problems. I n "Behavioural Ecology" (J. R. Krebs and N. B. Davies, eds.). pp. 129-151. Blackwell, Oxford. Heiligenberg, W. (1976). The interaction of stimulus patterns controlling aggressiveness in the cichlid fish Haplochromis burtoni. Anim. Behau. 24,452-458. Heiligenberg, W., Kramer, U.. and Schulz, V. (1972). The angular orientation of the black eyebar in Haplochromis burtoni (Cichlidae, Pisces) and its relevance to aggressivity. Z. Vergl. fhysiol. 76, 168-176. Heinroth, M. (1917). Erfahrungen uber Biologie und Technik bei Aufzucht junger Vogel. J. Ornirhol. 65, 392-395. Heinroth, 0.. and Heinroth, M. (1924-1934). "Die Vogel Mitteleuropas," Vols. 1-4. Bermuhler, Berlin. Helfrnan, G. S . ( 1989).Threat-sensitive predator avoidance in damselfish trumpetfish interactions. Behau. Ecol. Sociobiol. 24, 47-58. Hennessy, D. F., and Owings, D. H. (1988). Rattlesnakes create a context for localizing their search for potential prey. Ethology 77, 317-329. Hermstein, R. J., and Loveland, D. H. (1964). Complex visual concept in the pigeon. Science 146, 549-55 1. Hinde, R. A. (1954a).Factorsgoverning the changes in strength ofapartially inborn response,
232
E. CURIO
as shown by the mobbing behaviour of the chaffinch (Fringilla coelebs). I. The nature of the response, and an examination of its course. Proc. R . SOC.London 142,306-331. Hinde. R. A (1954b). Factors governing the changes in strength of a partially inborn response, as shown by the mobbing behaviour of the chaffinch (Fringilla coelebs). 11. The waning of the response. Proc. R . Soc. London, 142, 331-358. Hinde. R. A. (1970). "Animal Behaviour." McGraw-Hill, New York. Hirsch, J.. Lindley, R. H., and Tolman, E. C. (1955). An experimental test of an alleged innate sign stimulus. J . Comp. Physiol. Psychol. 48, 278-280. Hirsch, S. M., and Bolles, R. C. (1980). On the ability of prey to recognize predators. Z. Tierpsychol. 54, 71-84. Hobson. K. A., Bouchart, M.L.. and Sealy. S. G. (1988). Response of naive yellow warblers to a novel nest predator. Anim. Behav. 36, 1823-1830. Hoffmann. W. (1979). Antworten von Zebrafinken auf bekannte und fremde Vogelarten. 11. Der Einfluss von Vorerfahrung und Paarpartner. Diploma Thesis, Ruhr-Universitat Bochum. Hohlt, H. (1957). Studien an einer suddeutschen Population der Wacholderdrossel (Turdus pilaris). J. Ornirhol. 98, 71-118. Hoogland. J. L. (1979). The effect of colony size on individual alertness of prairie dogs (Sciuridae: Cynomys spp.). Anim. Behav. 27, 394-407. Hudson. P. J., and Newborn, D. (1990). Brood defence in a precocial species: Variations in the distraction displays of red grouse, Lagopus lagopus scoticus. Anim. Behav. 40, 254-261.
Huntingford, F. A. (1982). Do inter- and intraspecific aggression vary in relation to predation pressure in sticklebacks? Anim. Behav. 30,909-916. Inglis. I. R.. and Isaacson, A. J. (1984). The responses of woodpigeons (Columbapalumbits) to pigeon decoys in various postures: A quest for a super-normal alarm stimulus. Behavior 90,224-240. Inglis, I. R.. Huson. L. W.. Marshall, M.B..and Neville, P. A. (1983). The feeding behaviour of starlings (Stirmus vulgaris) in the presence of 'eyes'. Z. Tierpsvchol. 62, 181-208. Itzkowitz, M. (1979). Territorial tactics and habitat quality. Am. Nut. 114,585-590. Jacobsson, S . , and Jarvi, T. (1977). Antipredator beteende hos tvaarig lax Salmo salar. Zool. Revy 58,57-70. Jennings, T.. and Evans, S.M. (1980). Influence of position in flock and flock size on vigilance in the starling, Strrrnits vulgaris. Anim. Behav. 28, 634-635. Johnson, T. H., and Stattersfield. A. J. (1990). A global review of island endemic birds, Ibis 132, 167-180.
Jones, R. B. (1980). Reactions of male domestic chicks to two-dimensional eye like shapes. Anim. Behav. 28, 212-218. Kagan. 3. (1970). Attention and psychological change in the young child. Science 170, 826-832.
Karplus. I. (1979). The tactile communication between Cryptocentrus steinitzi (Pisces, Gobiidae) and Alpheus purpurilenticularis (Crustacea, Alpheidae). Z . Tierpsychol. 49, 173-196
Karplus. I.. and Algom, D. (1981). Visual cues for predator face recognition by reef fishes. Z. Tierpsychol. 55, 343-364. Karplus. 1.. and Bentuvia. S. (1979). Warning signals of Cryptocentrus steinitzi (Pisces, Gobiidae) and predator models. Z. Tierpsychol. 51, 225-232. Kerlinger. P.. and Lehrer. P. H. (1982). Owl recognition and anti-predator behaviour of sharpshinned hawks. Z. Tierpsychol. 58, 163-173. Kilham, L. (1982). Common crows and a Florida red-shouldered hawk mobbing feathers on the ground. Flu. Field Nat. 10, 23.
ASPECTS OF ANTIPREDATOR BEHAVIOR
233
Klopfer. P. H. (1957). An experiment on emphatic learning in ducks. Am. Nar. 91, 6163. Klump. G . (1984). Struktur and Funktion der Luftfeind-Alarmrufe der Kohlmeise (Pants major) auperhalb der Brutzeit. Ph. D. Dissertation, Ruhr-Universitat Bochum. Klump. G. M.. and Shaker, M. D. (1984). Acoustic behaviour of birds and mammals in the predator context. I. Factors affecting the structure of alarm signals. II. The functional significance and evolution of alarm signals. Z. Tierpsvchol. 66, 189-226. Knight, R. L.. and Temple, S . A. (1986a). Methodological problems in studies of avian nest defence. Anim. Behau. 34, 561-566. Knight R. L., and Temple. S . A. (1986b). Nest defence in the American goldfinch. Anim. Behav. 34,887-897. Knight, R. L., and Temple, S. A. (1988). Nest-defense behavior in the red-winged blackbird. Condor 90, 193-200. Kobayashi. T. (1987). Does the Siberian chipmunk respond to the snake by identifying it? J . Ethol. 5, 137-144. Koenig. L. (I95 I ). Beitrage zu einem Aktionssystem des Bienenfressers (Merops apiaster L.). Z. Tierpsychol. 8, 169-210 Kramer. G . (1941). Beobachtungen uber das Verhalten der Aaskrahe (Coruus corone) zu Freund und Feind. J. Ornithol. 89, 105-13 I . Kramer. G . , and von St. Paul, U. (1951). Uber angeborenes und erworbenes Feinderkennen beim Gimpel (Pyrrhula pyrrhrtla L.). Behavioitr 3, 243-255. Kruuk, H. (1964). Predators and anti-predator behaviour of the black-headed gull. Behavioitr 11, 1-129. Kruuk, H. (1972). “The Spotted Hyena.” Univ. of Chicago Press, Chicago and London. Kruuk, H. (1976). The biological function of gulls’ attraction towards predators. Anim. Behau. 24, 146-153. Kuenzer, P. (1975). Analyse der auslosenden Reizsituationen fur die Anschwimm-, Eindringund Fluchtreaktion junger Hemihaplochromis mulricolor (Cichlidae). Z . Tierpsychol. 38, 505-545. Lazarus, J. (1972). Natural selection and the functions of flocking in birds: A reply to Murton. Ibis 114, 555-558. Lendrem, D. W. (1980). Vigilance of a nest-building female blue tit (Pants caeruleus). Z. Tierpsychol. 54, 279-284. Lendrem. D. W. (1983). Sleeping and vigilance in birds. I. Field observations of the mallard (Anas platyrhynchos). Anim. Behau. 31, 532-538. Lendrem, D. W. (1984a). Sleeping and vigilance in birds. 11. An experimental study of the barbary dove (Streptopelia risoria). Anim. Behau. 32,243-248. Lendrem. D. W. (1984b). Flocking, feeding and predation risk: Absolute and instantaneous feeding rates. Anim. Behav. 32, 298-299. Leong. C. Y. (1969). The quantitative effect of releasers on the attack readiness of the fish Haplochromis burtoni (Cichlidae, Pisces). Z. Vergl. Physiol. 65, 29-50. Levesley, P. B., and Magurran, A. E. (1988). Population differences in the reaction of minnows to alarm substance. J . Fish Biol. 32, 699-706. Licht, T. (1989). Discriminating between hungry and satiated predators: The response of guppies (Poecilia reticulato) from high and low predation sites. Ethology 82, 238243. Lohrl, H. (1950a). Zum Verhalten der Rabenkrahe (Coruus c . corone) gegenuber dem Habicht. Z. Tierpsychol. 7, 130-133. Lohrl, H. (1950b). Beobachtungen zur Soziologie und Verhaltensweise von Sumpfmeisen (Parus palustris communis) im Winter. Z. Tierpsychol. 7,417-424. Lohrl, H. (1980). Eichelhaher mit Waldkauzruf. J . Ornithol. l21, 408.
234
E. CURIO
Lombardi. C. M., and Curio, E. (1985a). Influence of environment on mobbing by Zebra Finches. Bird Eehau. 6, 28-33. Lombardi. C. M., and Curio, E. (1985b). Social faciliation of mobbing in the Zebra Finch Taeniopygia grcttata. Bird Eehau. 6, 34-40. Lorenz, K. (1931). Beitrage zur Ethologie sozialer Corviden. J . Ornithol. 79, 67-127. Lorenz, K. (1935). DerKumpaninderUmweltdes Voge1s.J. Ornithol. 83,137-213.289-413. Lorenz, K. (1943). Die angeborenen Formen moglicher Erfahrung. Z. Tierpsychol. 5, 235-409. Loughry, W. J . (1987). Differences in experimental and natural encounters of black-tailed prairie dogs with snakes. Anim. Eehau. 35, 1568-1570. Loughry, W. J. (1988). Population differences in how black-tailed prairie dogs deal with snakes. Eehau. Ecol. Sociobiol. 22, 61-67. MacDonald, J. D. (1973). "Birds of Australia." H. F. and G. Witherby. London. MacLean. G. L. (1973). The sociable weaver. Part 4: Predators. parasites and symbionts. Ostrich 44, 241-253. Magurran. A. E. (1986). Predator inspection behaviour in minnow shoals: Differences between populations and individuals. Behau. Ecol. Sociobiol. 19, 267-273. Magurran. A. E. (1989). Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology 82, 216-223. Magurran, A. E. (1990). The inheritance and development of minnow anti-predator behaviour. Anim. Behau. 39,834-842. Magurran. A. E., and Girling, S. L. (1986). Predator model recognition and response habituation in shoaling minnows. Anim. Eehau. 34, 510-518. Magurran, A. E.. Oulton, W. J., and Pitcher, T. J. (1985). Vigilant behaviour and shoal size in minnows. Z. Tierpsychol. 67, 167-178. Margolis, R. L.. Mariscal, S. K.. Gordon, J. D., Dollinger. J.. and Gould, J. L. (1987). The ontogeny of the pecking response of laughing gull chicks. Anim. Eehau. 35, 191-202. Markgren. M. (1960). Fugitive reactions in avian behaviour. Acta Vertebratica 2, 1-160. Marler. P.. and Hamilton, W. J., I11 (1966). "Mechanisms of Animal Behaviour." Wiley, New York. Martin, R. C., and Melvin, K. B. (1964). Fear responses of bobwhite quail (Colinus uirginianus) to a model and a live red-tailed hawk (Buteojamaicensis). Psycho/. Forsch. 27, 323-336. McLean, I. G., and Rhodes. G. (1991). Enemy recognition and response in birds. Curr. Ornithol. 8, 173-21 I. McLean, I. G., Smith, J. N . M.. and Stewart, K. G. (1986). Mobbing behaviour, nest exposure, and breeding success in the American robin. Behauiour %, 171-186. McNicholl. M. K. (1973). Habituation of aggressive responses to avian predators by terns. Auk 90,902-904. McPhail. J. D. (1%9). Predation and the evolution of a stickleback (Gnsterosteus). J. Fish. Res. Board Can. 26,3183-3208. Meinertzhagen, R. (1950). Tameness in birds. Ibis. 92, 151-152. Meinertzhagen, R. (1955). The effects of model scorpion and lizard on a bird-table. Er. Birds 48, 556-557. Meinertzhagen. R. (1959). "Pirates and Predators." Oliver & Boyd, Edinburgh and London. Melchior, H. R. (1971). Characteristics of arctic ground squirrel alarm calls. Oecologia 7, 184- 190. Melvin, K. B. (1969). Habituation of responses of quail (Colinus uirginianrrs) to a hawk (Buteo swainsoni): Measurement through an 'innate suppression' technique. Anim. Eehau. 17,468-473.
ASPECTS OF ANTIPREDATOR BEHAVIOR
235
Merritt. P. G. (1984). Observer recognition by the northern mockingbird. J . Field Ornir/iol. 55, 252-253. Mineka. S., and Cook, M. (1988). Social learning and the acquisition of snake fear in monkeys. I n "Social Learning: Psychological and Biological Perspectives" (T. Zentall and B. G. Galef. eds.). pp. 51-73. Erlbaum. Hillsdale. NJ. Mineka. S.. and Keir, R. (1983). The effects of flooding on reducing snake fear in rhesus monkeys: 6-month follow-up and further flooding. Behau. Res. T h r . 21, 527-535. Moholt, R. K. (1989). Dominance, predator interactions, and social gatherings of the blackbilled magpie. Master's thesis. Idaho State University. Pocatello. Montevecchi. W. A., and Maccarone. A. D. (1987). Differential effects of agreat horned owl decoy on the behavior ofjuvenile and adult gray jays. J . Field Ornirhol. 58, 148-151. Montgomerie, R. D., and Weatherhead, P. J. (1988). Risks and rewards of nest defence by parent birds. Q. Reu. Biol. 63, 167-187. Mueller. H. C.. and Parker. P. G. (1980). Naive ducklings show different cardiac response to hawk than to goose models. Behauiortr 74, 101-1 13. Muller, D. (l%l). Quantitative Luftfeind-Attrappenversuchebei Auer- und Birkhuhnern (Tetra0 urogallits L. und Lvrrrrirs terrix L.) Z . Natrrrforsch. 16, 551-553. Murphy, L. B. (1978). The practical problems of recognizing and measuring fear and exploration behaviour in the domestic fowl. Anim. Behau. 26, 422-431. Murphy. L. B.. and Duncan. 1. J. H. (1977). Attempts to modify the responses of domestic fowl towards human beings. I. The association of human contact with a food reward. Anim. Erhol. 3, 321-334. Murphy, L. B., and Duncan, 1. J. H. (1978). Attempts to modify the responses of domestic fowl towards human beings. 11. The effect of early experience. Anim. Efhol. 4, 512.
Murray, S. G., and King, J. E. (1973). Snake avoidance in feral and laboratory reared squirrel monkeys. Behauiour 47, 281-289. Myrberg, A. A., and Thresher, R. E. (1974). lnterspecific aggression and its relevance to the concept of territoriality in reef fishes. Am. Zool. 14, 81-%. Nash, A. D., and Nash, S. V. (1985). Large frogmouth Barruchosrornrrs airritrrs mobbed by a greater racket-tailed drongo. Krtkilu 2, 67. Neil, S . J. (1984). Field studies of the behavioral ecology and agonistic behavior of Chic~hlasoma meeki (Pisces: Cichlidae). Environ. Biol. Fish. 10, 59-68. Neill, S . R., and Cullen, J. M. (1974). Experiments on whether schooling by their prey affects the hunting behaviour of cephalopod and fish predators. J. Zool. London 172,549-569. Nice. M. M. (1943). Studies in the life history of the Song Sparrow. I I . The behavior of the Song Sparrow and other passerines. Trans. Linn. Soc. N . Y . 6 , 1-329. Nicolai, J. (1950). Steinschmatzerbeobachtungen. Gef. Welt 74, 10. Onnebrink. H., and Curio, E. (1991). Brood defense and age of young: A test of the vulnerability hypothesis. Behav. Ecol. Sociobiol. 29, 61-68. Owings. D. H., and Coss, R. G. (1977). Snake mobbing by California ground squirrels: Adaptive variation and ontogeny. Behauiour 62, 50-69. Owings, D. H., and Coss, R. G. (1981). How ground squirrels deal with snakes. Anima 99, 37-43.
Owings, D. H.. and Owings, S. C. (1979). Snake-directed behavior by black-tailed prairie dogs (Cynomys ludoviciunus). Z. Tierpsychol. 49, 35-54. Pereira. M. E., and Macedonia, J. M. (1991). Ringtailed lemur anti-predator calls denote predator class, not response urgency. Anim. Behau. 41, 543-544. Perrone, M. (1978). The economy of brood defence by parental cichlid fishes, Cichlasoma maculicauda. Oikos 31, 137-141.
236
E. CURIO
Pettifor, R. A. (1990). The effects of avian mobbing on a potential predator, the European kestrel, Falco tinnunculus. Annim. Eehav. 39, 821-827. Pomeroy, H., and Heppner, F. (1977). Laboratory determination of startle reaction time of the starling (Sturnus vulgaris). Anim. Eehav. 25, 720-725. Portielje, A. F. J. (1926). Zur Ethologie bzw. Psychologie von Eotaurus stelloris (L.).Ardea 15, 1-15.
Potts, G. W. (1980). The predatory behaviour of Carnax melampygus (Pisces) in the channel environment of Aldabra Atoll (Indian Ocean). J. Zool. 192, 323-350. Poysa, H.(1987). Feeding-vigilance trade-off in the teal (Anus crecca): Effects of feeding method and predation risk. Eehaviour 103, 108-122. Prins, H. H. T.. and lason. G. R. (1989). Dangerous lions and nonchalant buffalo. Eehaviour 108, 262-296. Ratner. S . C. (1967). Comparative aspects of hypnosis. In “Handbook of Clinical and Experimental Hypnosis” ( J . E. Gordon. ed.). pp. 550-587. Macmillan. New York. Reist. J. D. (1983). Behavioral variation in pelvic phenotypes of brook stickleback. Culuea inconsfans. in response to predation by northern pike, Esox Iucirrs. Environ. Eiol. Fishes 8,255-267.
Richardson. W. B. (1942). Reaction toward snakes as shown by the wood rat, Neotoma albigula. J. Comp. Psychol. 34, 1-10. Roberts, W. A. (1988). Concept learning at different levels of abstraction by pigeons. monkeys. and people. J. Exp. Psychol. 14, 247-260. Roberts, W. A.. and Mazmanian, D. S. (1988). Concept learning at different levels of abstraction by pigeons. monkeys and people. J. Exp. Psychol.: Anim. Eehau. Proc. 14, 247-260.
Robertson, R. J.. and Norman. R. F. (1976). Behavioral defenses to brood parasitism by potential hosts of the brown-headed cowbird. Condor 78, 166-173. Robinson. S. K. (1985). Coloniality in the yellow-rumped cacique as a defense against nest predators. Auk 102, 506-519. Robinson. S. R. (1980). Antipredator behaviour and predator recognition in Belding’s ground squirrels. Anim. Eehau. 28, 840-852. Roell, A., and Bossema, I. (1982). A comparison ofnest defence byjackdaws, rooks, magpies and crows. Eehav. Ecol. Sociobiol. 11, 1-6. Rood. J. P. (1983). Banded mongoose rescues pack member from eagle. Anim. Eehav. 31, 1261-1262.
Root, R. B. (1969). The behavior and reproductive success of the blue-gray gnatcatcher. Condor 71, 16-3 I . Rothschild. M.. and Lane. C. (1960). Warning and alarm signals by birds seizing aposematic insects. Ibis 102, 328-330. Rowe. M. P.. and Owings, D. H. (1990). Probing, assessment, and management during interactions between ground squirrels and rattlesnakes. Part 1. Risks related to rattlesnake size and body temperature. Ethology 86, 237-249. Rubel, E. W. (1970). Effects of early experience on fear behaviour of Coturnix cotrtrnix. Anim. Eehav. 18,427-433.
Satinder, K. P. (1976). Reactions of selectively bred strains of rats to a cat. Anim. Learn. Eehav. 4, 172-176.
Sauer, F. (1954). Die Entwicklung der Lautausserungen vom Ei ab schalldicht gehaltener Dorngrasmucken (Sylviac. communis, Latham) im Vergleich mit spater isolierten und mit wildlebenden Artgenossen. Z. Tierpsvchol. 11, 10-93. Scaife, M. (1976a). The response to eye-like shapes by birds. I. The effect of context: A predator and a strange bird. Anim. Eehav. 24, 195-199.
ASPECTS OF ANTIPREDATOR BEHAVIOR
237
Scaife, M. (1976b). The response to eye-like shapes by birds, 11. The importance of staring, pairedness and shape. Anim. Behav. 24,200-206. Schaller. G. B. (1972). "The Serengeti Lion." Univ. of Chicago Press, Chicago. Scherzinger, W. (1970). Zum Aktionssystem des Sperlingskauzes (Glaucidium passerinurn, L.). Zoologica ( N . Y . ) 118, 1-120. Schleidt, W. M. (I%la). Reaktionen von Truthiihnern auf fliegende Raubvogel und Versuche zur Analyse ihrer AAM's. Z . Tierpsychol. 5 , 534-560. Schleidt, W. M. (1961b). Uber die Auslosung der Flucht vor Raubvogeln bei Truthiihnern. Nafurwissenschaften 5 , 141-142. Schleidt, W. M. (1962). Die historische Entwicklung der Begriffe "Angeborenes auslosendes Schema" und "Angeborener Auslosemechanismus" in der Ethologie. Z . Tierpsychol. 19,697-722.
Schleidt. W. M. (1964). Verhalten. Wirkungen ausserer Faktoren auf das Verhalten. Fortschr. Zool. 16, 469-499. Schleidt, W. M., Shaker, M. D., and Carawan, T. C. (1983). The effect of spatial context on habituation to a predator model. Z . Tierpsychol. 61, 67-70. Seghers, B. H. (1973). An analysis of geographic variation in the antipredator adaptations of the guppy, Poecilia reficulata. Ph.D. thesis, University of British Columbia. Seghers. B. H. (1974). Schooling behavior in the guppy (Poecilia reficulata):An evolutionary response to predation. Evolufion (Lawrence, Kans.) 3,486-489. Seitz, A. (1940-1941). Die Paarbildung bei einigen Cichliden I. Die Paarbildung bei Asfafofilapia sfrigigena Pfeffer. Z . Tierpsychol. 4, 40-84. Seyfarth. R. M.. and Cheney, D. L. (1980). The ontogeny of vervet monkey alarm calling behavior: A preliminary report. Z . Tierpsychol. 54, 37-56. Seyfarth, R. M., and Cheney, D. L. (1990). The assessment by vervet monkeys of their own and another species' alarm calls. Anim. Behau. 40, 754-764. Seyfarth, R. M.. Cheney, D. L., and Marler, P. (1980). Vervet monkey alarm calls: Semantic communication in a free-ranging primate. Anim. Behau. 28, 1070-1094. Shaker, M. D. (1975). Lack of spatial generalization in habituation tests of fowl. J . Comp. Physiol. Psychol. 89, 258-262. Shaker, M. D. (1978a). Effect of spatial context on the mobbing reaction of pied flycatchers to a predator model. Anim. Behav. 26, 1219-1221. Shaker, M. D. (1978b). Mobbing in the pied flycatcher. Effect of experiencing a live owl on responses to a stuffed facsimile. Z. Tierpsychol. 47, 173-179. Shaker, M. D., Fentress, J. C., and Young, G. W. (1977). Determinants of response of wolf pups to auditory signals. Behaviour 60, 98-1 14. Sherman, P. W. (1980). The limits of ground squirrel nepotism. l h "Sociobiology: Beyond Nature/Nurture?" (G. W. Barlow and J. Silverberg, eds.), pp. 505-544. Westview Press, Boulder, CO. Smith, M. I., and Graves, H. B. (1978). Some factors influencing mobbing behavior in barn swallows (Hirundo rustics). Behav. Biol. 23, 355-372. Smith, W. J. (1977). "The Behavior of Communicating." Harvard Univ. Press, Cambridge, MA. Snyder, N. F. R.. and Snyder, H. A. (1971). Defenses of the Florida apple snail Pomacea paludosa. Behauiour 40, 175-215. Stinson, C. H. (1976). On the recognition of offspring by raptors. Rapfor Res. 10, 30-32. Stone, E., and Trost, C. H. (1991). Predators, risks and context for mobbing and alarm calls in black-billed magpies. Anim. Behau. 41, 633-638. Stoner, G., and Breden, F. (1988). Phenotypic differentiation in female preference related t o geographic variation in male predation risk in the Trinidad guppy (Poecilia reticulafa). Behav. Ecol. Sociobiol. 22, 285-291.
238
E. CURIO
Strauss, E. (1939). Versuche an gefangenen Rabenvogeln. Z. Tierpsychol. 2, 172-197. Suboski, M. D., and Templeton. J. J. (1989). Life skills training for hatchery fish: Social learning and survival. Fish. Res. 7, 343-352. Suboski, M. D., Bain, S. Carty. A. E.. McQuoid. L. M., Seelen. M. I.. and Seifert. M. (1990). Alarm reaction in acquisition and social transmission of simulated-predator recognition by zebra danio fish (Brachydanio rerio). J . Comp. Psychol. 104, 101-1 12. Thresher. R. E. (1976). Field experiments on species recognition by the threespot damselfish. Eupomacentrus planifrons (Pisces: Pomacentridae). Anim. Behau. 24, 562-569. Tinbergen, N . (1951). "The Study of Instinct." Oxford Univ. Press (Clarendon), London. Tinbergen, N. (1957). On anti-predator responses in certain birds-a reply. J. Comp. Physiol. Psychol. 50,412-414. Tinbergen, N. (1958). "Die Welt der Silbermowe." Musterschmidt-Verlag, Gottingen. Toenhardt, H. (1935). Beitrtige LU dem Problem des "Hassens" der Singvogel auf die Eulen. Ph. D. Dissertation, Triltsch & Huther. Berlin. Tulley. J. J., and Huntingford, F. A. (1987a). Paternal care and the development of adaptive variation in anti-predator responses in sticklebacks. Anim. Behav. 35, 1570-1572. Tulley, J. J.. and Huntingford, F. A. (1987b). Age, experience and the development of adaptive variation in anti-predator responses in three-spined sticklebacks (Gasterosteus aculeatus). Ethology 75, 285-290. Tulley, J. J., and Huntingford, F. A. (1988). Additional information on the relationship between intraspecific and anti-predator behaviour in the three-spined stickleback, Gasterosteus aculeatus. Ethology 78, 219-222. Veen, J. (1977). Functional and causal aspects of nest distribution in colonies ofthe sandwich tern (Sterna s . sanduicensis Lath.). Ph.D. thesis, University of Gr@ningen. Verbeek, N . A. M. (1972a). The exploitation system of the yellow-billed magpie. Uniu. Calif., Berkeley, Publ. Zool. 76, 1-58. Verbeek, N . A. M. (1972b). Comparison of displays of the yellow-billed magpie (Pica nuttalli) and other corvids. J . Ornithol. 113, 297-314. Vogel, C. ( 1975). Okologie, Lebensweise und Sozialverhalten der Grauen Languren in verschiedenen Biotopen Indiens. Z. Tierpsychol., Suppl. 17, 1-59. Volkel. P., and Zell, R. A. (1980). Beobachtungen und Versuche zum Mischschwarmund Feindverhalten einiger neotropischer Singvogel. Diploma Thesis, Ruhr-Universitat Bochum. von Fersen, L., and Delius. J. D. (1989). Long-term retention of many visual patterns by pigeons. Ethology 82, 141-155. von Frisch, K. (1941). Die Bedeutung des Geruchsinnes im Leben der Fische. Naturwissenschafien 29,322-333. von Frisch, 0. (1958). Die Bedeutung des elterlichen Warnrufs fur Brachvogel- und andere Limicolenkucken. Z. Tierpsychol. 15, 381 -382. von Frisch. 0. (1964). "Der Grosse Brachvogel." Ziemsen. Wittenberg, Lutherstadt. van Lawick-Goodall, H., and van Lawick-Goodall, J. (1970). "Innocent Killers." Collins, London. von St. Paul, U. (1948). Uber das angeborene Erkennen von Feinden bei Wurgern. Ph. D. Dissertation, Heidelberg. Walters, J. R. (1990). Anti-predatory behavior of lapwings: Field evidence of discriminative abilities. Wilson Bull. 102, 49-70. Woolpy, J. H., and Ginsburg, B. E. (1967). Wolf socialization: A study of temperament in a wild social species. Am. Zool. 7, 357-363. Zimmermann. U., and Curio, E. (1988). Two conflicting needs affecting predator mobbing by great tits, Parus major. Anim. Behau. 36, 926-932.
ADVANCES IN THE STUDY OF BEHAVIOR. VOL. 22
Newborn Lambs and Their Dams: The Interaction That Leads to Sucking MARGARET A. VINCE AFRC INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS RESEARCH BABRAHAM, CAMBRIDGE CB2 4AT, ENGLAND
I. INTRODUCTION
This article is concerned mainly with the first hour or two of life in the sheep; with the sensory and behavioral factors which play a part in keeping dam and offspring together and organizing their relationship so that the newborn is fed, and bonding between ewe and lamb can begin. Some of these factors come into operation before birth, some bridge the changes at birth, and some come into play later. The ewe normally lies down when giving birth. When the lamb is born the dam gets on to her feet, moves round, and begins to lick it. The lamb, therefore, comes almost at once to lie at her head end. It has to move away from there and make for the udder before the teat can be located and it can begin to suck.’ This cannot occur without the dam’s cooperation. Meanwhile, feeding is not the lamb’s only requirement. To survive, it has to stay with the dam and become bonded to her. The lamb is born very mature compared to mammals with altricial young; it stands quickly after birth, in some breeds within a few minutes, and all sensory systems are already functional. One problem for the newly born lamb is that, unless its mother is attentive, its response to other objects can lead it away from her.
’
For the sake of c l a r i t y , in this article “sucking” denotes lamb behavior and “suckling” is provided by the dam; the lamb sucks and the dam suckles it. 239 Copyright 0 1993 by Academic Press, Inc. All rights of reproduction in any form reserved.
240
MARGARET A. VlNCE
11. PRE-A N D PERINATAL FACTORS THATPLAYA PARTI N THE EWEA N D
LAMBRELATIONSHIP AFTER BIRTH A.
FACTORS THATAFFECTTHE DAM’SBEHAVIOR
The mother’s physiological condition at the time of giving birth is the first essential for a successful interaction. Maternal behavior begins during the early stages of parturition. The ewe paws the ground, licking up the fetal fluids after the birth membranes have ruptured, and begins making soft, low-frequency “rumble”-type vocalizations (Shillito and Hoyland, 1971). When her lamb emerges in a pool of amniotic fluid she rises within about a minute (Bareham, 1976; Arnold and Morgan, 1975), turns to the lamb, and begins to lick it, at the same time sucking up and ingesting the fetal fluids and membranes. The dam’s behavior has been rendered maternal by gonadal steroids (Poindron and LeNeindre, 1980) comparable with those acting during pregnancy in the rat (Rosenblatt and Siegel, 1983). However, Poindron et al. (1988) have shown that the full complement of her maternal behavior, defined as licking, low-pitched bleats, and acceptance at the udder, is not always elicited by hormonal priming alone. It is facilitated by the smell of fetal fluid (Levy et al., 1983), amniotic fluid from her own lamb being more powerfully attractive than that of an alien one (Levy and Poindron, 1984, 1987), and by the vaginal-cervical stimulation which occurs during labor and expulsion of the lamb (Keverne et al., 1983). The ewe’s maternal behavior is also affected by previous experience. In primiparous animals it tends to develop more slowly after giving birth and is less certain. In the induction of maternal behaviour in nonpregnant animals, primiparous animals were found to be less responsive to hormones than multiparas (LeNeindre et al., 1979; Poindron and LeNeindre, 1980). Among pregnant ewes delivered by cesarian section, no primiparous animals showed’maternalbehavior within 3 days, whereas almost all multiparas did so, suggesting that the former require stimulation of the birth canal for a normal response to the lamb (Alexander et al., 1988). Also, unlike multiparas, amniotic fluid on the birth coat is necessary for primiparas to develop maternal behavior at parturition (Levy and Poindron, 1987). More recently, oxytocin has been implicated in the hormonal stimulation of the ewe’s maternal behavior (Kendrick et al., 1987), and Levy et al. (1992) have shown that vaginocervical stimulation, as the major factor facilitating a rapid onset of maternal behavior, acts via intracerebral oxytocin secretion in primiparous as well as multiparous parturient ewes. The ewe’s maternal behavior gradually declines unless it is reinforced by the presence of a lamb. If the lamb is removed at birth and kept away
24 1
NEWBORN LAMBS AND THEIR DAMS
for 1-4hr, many dams will still accept it, although the numbers that accept fall off with the time since separation (Poindron et af., 1979; Alexander et af., 1986). However, if her own lamb is removed at birth, the ewe will usually accept a newly born alien lamb (Smith et af., 1966). Once she has licked her lamb for a few minutes she will butt away an alien (Herscher et af., 1963),although it takes 2-4 hr for ewes to become completely selective (Poindron et al., 1980); therefore learning her own lamb’s characteristics can modify, or direct, the ewe’s maternal behavior. This learning appears to be based on smell: Poindron (1976) has shown that the dam recognizes her lamb by its odor when it comes to suck, and Alexander and Stevens (1985) have demonstrated that this odor can be transferred to an alien lamb, ultimately making it acceptable, even at 2-3 days after birth. Its smell, although important, is not the only factor which makes a newborn lamb acceptable. Baldwin and Shillito (1974) found that anosmic Soay ewes accepted their lambs, although they failed to lick them sufficiently and did not form the usual exclusive relationship with them. At parturition the dam is also attracted by lambs which are warm (Lynch and Alexander, 1973),newly born, wet and lying down (Poindron et af., 1980),and bleating (Smith et af., 1966).
B. SENSORY FACTORS MEDIATING THE ACTIVITY OF AND NEWBORN
THE
FETUS
Before it can suck, the newborn lamb has to right itself, stand, approach the udder, and locate the teat; the sensory systems on which these depend are known to develop during the 5 months of gestation. Persson and Sternberg (1972) obtained pupillary reflexes from the 92-day fetus (gestation period 145 days) and concluded that retinal function is present at that time. However, patterned visual experience seems unlikely before birth. When the lamb is born its eyes open at once. It is believed to make an almost immediate response to visual patterns. According to Smith (1965), it makes for the nearest large object and puts its head under any object protruding at about head height. We do not know whether its novelty makes visual experience the most prominent aspect of the lamb’s immediately postnatal environment, but movement toward the visually perceived, large object is of prime importance in the lamb’s first interaction with the dam (Section 111, B). As regards the lamb’s experience of sound, there is more continuity between pre- and postnatal life. The fetus will undoubtedly have heard parts of the acoustic environment which come to it both from inside and outside the dam. Bernhard et af. (1959)found that the fetal lamb responds
242
MARGARET A. VlNCE
to sound from about the 100th day of the 145-day gestation period. Recordings from a hydrophone implanted inside the amniotic sac during the last 2 weeks of pregnancy showed that sounds from inside the dam, originating in, for example, her drinking, chewing, ruminating, and stepping, occurred loudly at frequencies up to about 300 Hz but rarely at frequencies above 500 Hz. Sounds from outside the dam (such as human voices) were picked up by the hydrophone and were attenuated at frequencies above 500-600 Hz, giving a muffled effect (Vince et al., 1982b).From a miniaturized radio transmitter sutured to the fetus, recordings were made throughout parturition. These suggested that the mother’s bleat, which has a fundamental frequency of about 200 Hz or less and little energy above about 3-5 kHz (Shillito Walser and Hague, 1980), was likely to be the loudest sound heard habitually by the fetus, since this sound came to the amniotic sac both from outside the dam and also from inside, where it was less attenuated. During parturition the recordings included periods when the maternal heart sounds increased in rate and amplitude, the sound of breathing became louder, and contractions (monitored by the experimenter) were accompanied by a slow irregular buildup of very low frequency sound peaking at about 40 Hz (Vince et al., 1985a). The significance of the newborn lamb’s prenatal sound experience has only been partially assessed. The sound environment will change at birth to include higher frequencies; and, in contrast to that during birth, normal conditions in the field might well sound very quiet. The change would be bridged by the dam’s soft “rumble”-type vocalizations, which do not include the high frequencies occurring in bleats (compare the sonagram of a rumble, shown by Shillito [1972] as a series of clicks with energy up to about 1 kHz, with that of ewes’ normal bleats, which have harmonics up to about 5 kHz [Shillito Walser and Hague, 19801). In two experiments, newly born lambs presented with artificially made-up sounds which could, or could not, have been heard before birth, showed more heart rate acceleration in response to the unfamiliar sound, suggesting habituation to the sound heard before birth (Vince et al., 1982a, 1985a).The effect, however, was small and whether its prenatal experience of sound contributes to the lamb’s postnatal learning remains uncertain. Older lambs are known to recognize their own mothers’ bleats (Shillito, 1975); when ewes were hidden behind canvas, 2 1-day-old lambs were able to find their own mothers by voice (Shillito Walser and Alexander, 1980). As to olfactory sensation, functional nasal chemoreception in the fetal lamb has been demonstrated by Schaal et al. (1991), and there is work suggesting that lambs become familiar with the maternal odor during gestation (Vince and Ward, 1984; Section 111,D). At birth the lamb’s coat and
NEWBORN LAMBS AND THEIR DAMS
243
its nasal and buccal cavities are still saturated with amniotic fluid, so its postnatal olfactory experience must be to some extent familiar. Experiments on fetal and neonatal rats (Smotherman, 1982; Smotherman and Robinson, 1988; Pedersen and Blass, 1982) have shown that prenatal olfactory experience affects later behavior of the fetus and the newborn in this species. In the sheep, Schaal and Orgeur (1992)have found evidence that prenatal exposure to a weak solution of citral reduced newly born lambs’ aversion to this substance. The lamb’s sense of taste is known to develop in utero: Bradley and Mistretta (1973) made recordings from taste neurons in the medulla from the 84th day of gestation. They found that chemical stimulation of the tongue elicits responses from the chorda tympani nerve by the 96th day and, during the later part of gestation, the fetus swallows 70-491 ml of amniotic fluid daily. As the composition of the fluid varies to some extent from day to day (Mellor and Slater, 1971), there is a possibility that the fetus responds to its taste, another factor which could provide continuity between its prenatal and immediately postnatal experience. During the last half of the gestation period, fetal lambs are sensitive to a 1°C increase in temperature (Robinson, in Dawes, 1973); the drop in environmental temperature at birth, exaggerated by evaporation of birth fluids, therefore provides a marked discontinuity with prenatal life, which may well be bridged in part by maternal licking and could increase the significance of the dam’s presence. The vestibular system is known to develop early in the sheep fetus which, as it grows too big to float, will be exposed to gravitational stimuli, such as linear and angular acceleration when the mother moves (Bradley and Mistretta, 1975). The newly born lamb’s response, first to gravitation and then to touch, provides in large part a key to its behavior at least until it has sucked (Section 111). The fetal lamb’s response to touch was studied by Barcroft and Barron (1939). They demonstrated reflex responses to tactile stimulation in the exteriorized fetus at about 40 days of age. At that stage, touch on the skin from beneath the eye to the top of the nose already elicits extension of the head and foreleg and opening of the mouth. Stimulation of the forehead is followed by extension of the neck and legs. Stroking of the lower jaw and lip results in opening of the mouth and turning of the head toward the stimulus, often with a protruded tongue curled toward the same side. Touch on the tongue elicits closure of the mouth, with the tongue curled round the stimulus, and also chewing and swallowing. In the mature fetus, Fraser (1985) observed frequent bouts of sucking and swallowing.
244
MARGARET A. VlNCE
The lamb’s immediately postnatal environment will be partly familiar and partly new. The next section considers effects of this on the interaction with the ewe which leads to the lamb beginning to suck from the teat. 111. SENSORY AND BEHAVIORAL FACTORS INVOLVED I N THE POSTNATAL
INTERACTION BETWEEN EWEAND LAMB A.
EWEAND LAMBBEHAVIOR UNTIL THE LAMBSTANDS
Once the membranes have ruptured during parturition, the ewe begins licking up the birth fluids from the ground. When the lamb emerges the dam gets onto her feet and turns; her licking includes the lamb and the fluids and membranes while she vocalizes softly. She is attracted to the lamb, not only because of the fetal fluids, but also because of its bleats, temperature, and posture (Section 11,A). The lamb’s first response is to gravity; it raises and shakes its head and ears. At first drooped, the ears are soon cocked (Fraser, 1985; Vince, 1986). The lamb first turns onto its sternum, then raises itself onto its knees, pushing up on and straightening its hind legs. Finally, it stands by straightening its forelegs, thus following the sequence in which sheep normally stand, according to Barcroft and Barron (1936). Before it gets on to all four feet, the lamb begins to creep and lurch toward and under the dam and toward the udder (Collias, 1956). Fraser (1985) describes this movement as including nosing with the head extended on the same level as the trunk. Nosing is one of the lamb’s most important activities at this stage and until it has sucked (Section I K C , D, and E). The rate at which lambs right themselves, stand, and move varies greatly between breeds. Slee and Springbett (1986) report mean latencies for these behavior patterns of between 17 and 54 min. The rate also depends on a number of environmental factors. Merino lambs were removed from the dam at birth and observed for 30 min in a circular arena in the presence of a silent model ewe which did not smell of sheep. These lambs stood more rapidly, and approached and nosed the model more when it was moving than when it was stationary (Fig. 1). Lambs which heard loud recorded bleats of the kind given by ewes deprived of their offspring made more righting and standing movements than those in all other groups in this experiment, whereas lambs given simulated licking tended to be slow to stand, as also were lambs kept in a small pen with the dam (Vince et al., 1985b). Unlike the response they make to bleats, lambs stimulated with recorded low-frequency vocalizations, or rumbles, such as those given by the dam when caring for a newborn lamb, stood more slowly than
245
NEWBORN LAMBS AND THEIR DAMS
Mean 2nd
Mean lst half
holf
Successive S-minute periods FIG.I . Mean number of 10-sec intervals in each of six successive 5-minperiods of testing in which lambs approached or touched moving and stationary models. (From Vince et al., 1985b. by courtesy of E. J. Brill, Leiden.)
lambs which did not hear these sounds. This effect occurred whether the lambs were in the presence of a moving model, or not (Fig. 2; Vince, 1986). For the lamb, therefore, the ewe would appear to be a composite stimulus with different effects; her presence, her licking, and her lowfrequency vocalizations calm it and depress its activity, whereas it is activated by her movement. There are other conditions in which the lamb’s righting and standing can be slowed or accelerated; standing (and also teat-seeking) may be slowed, or reduced, in cold or wet weather, which depletes the neonate’s reserves of energy (Lynch and Alexander, 1973). Merino lambs kept with the dam, but blindfolded from birth, failed to stand until the blindfold was removed at 1 hr of age (Vince et al., 1987). It seems possible that the lack of visual stimulation exaggerated the inhibiting effect of maternal vocalizations. Also, some lambs left on their own fail to stand and subsequently die (Herscher et al., 1963), although most unattended lambs in a flock do stand, seek out a ewe, and attempt to suck. In unpublished observations on primiparous Soay ewe/lamb pairs, some ewes initially backed away from their lambs and, in constantly lurching toward her, they began standing exceptionally quickly, about 3 to 6 min after birth. Standing, therefore, depends on long-established reflexes, which appear not to operate without postnatal stimulation, especially visual.
246
MAKGARET A . VlNCE
5-MINUTE PERIODS FIG. 2. Number of lambs which stood up in six successive 5-min test periods. Lambs presented with (0---0) low-frequency vocalizations or “rumbles.” (0-0) model and rumbles, (0-0) model alone, (0-0) no stimulation. (From Vince, 1986.)
TOWARD T H E UDDER A N D COUNTERACTING B. LAMBMOVEMENT MOVEMENTS OF THE DAM
Discussion of movement toward the udder (“approach”) overlaps with that of standing, as approach often begins before the lamb stands: the lamb works its way toward the dam or the udder on front knees and hind feet (Collias, 1956). Approach tends to begin at the dam’s head, where the lamb finds itself when being licked. Unpublished observations on small groups of British sheep (Table I ) have shown that successful approaches, those ending in the position for sucking (Section III,C), began at the dam’s head in 74 out of 85 animals. Approach is believed to be elicited by visual cues (Herscher et al., 1963; Smith, 1965). In lambs which had already been suckled, Bareham (1975) found that blindfolding prevented them from sucking. In newly born lambs kept with the dam and blindfolded at birth, it was found that they did not move toward the udder, or stand, until the blindfold was removed. Then they stood up at once and approached the udder. On the other hand,
247
NEWBORN LAMBS AND THEIR DAMS
lambs rendered anosmic by a nasal spray did not differ in their approaches to the udder from untreated controls (Vince et al., 1987). Similarly, evidence that newly born lambs approach silent models not smelling of sheep, and that they approach sooner when the models are moving (Vince et al., 1985b; Section III,A), is consistent with the view that the stimulus for approach is a visual one. Bareham (1976)noted that lambs move toward the udder while generally maintaining physical contact with and nudging at the dam, and that the lamb’s early approaches are normally combined with nuzzling (Section 111,C). Approach and nuzzling may, however, be separate responses, as lambs which moved toward the udder after 1 hr of being blindfolded did so without the usual “teat-seeking” activities (Vince et al., 1987). Such nuzzling may help to support a very young, unstable lamb as well as enabling it to locate the teat.
TABLE I DIRECTION FROM WHICH LAMBMOVEDTOWARD THE UDDER WHEN FIRST ACHIEVING THE POSTUREFOR SUCKING Number which moved from dam’s head end
Number which achieved posture differently from those in first column
Number which failed within observation period
4
I moved from under the dam; 1 moved from about 45 cm away from dam
0
6
-
0
7 8
-
A. Groups kept with the dam
Soays Multiparous Primiparous Clun Forest Mu1tiparous Primiparous Dalesbreds Jacobs
6 12
2 moved from under the dam -
3 4
1
0
B. Groups removed from dam at birth or standing and returned after 30 min or 1 hr 10 3 moved from under the dam; I 0 Soays went toward dam from side of pen Clun forest 21 1 sucked without being licked; 2 8 went to dam from about 30 cm away
248
MARGARET A. VINCE
Fraser (1985) suggests that the “shaded underbelly” of the dam is the visual stimulus which causes the newborn ungulate to move under her. The lamb’s movements of approach to the udder may be slowed, controlled, or obstructed by the dam. Her most vigorous and sustained licking occurs immediately after birth (Vince et al., 1987), and at that time the lamb’s movements of approach tend to be counteracted by the dam moving her hindquarters away from it (“circling”). In this way, she keeps the lamb at her head while she continues to lick it. A more accepting ewe lets the lamb go toward the udder, while she turns her head and her licking moves to its rear end. Circling has to be overcome before the lamb can suck. Approaches to the udder begin very soon after birth and are repeated at frequent intervals, perhaps each time the dam circles, or each time the lamb itself returns to the dam’s head.
C. TEATLOCATION AND SUCKING, THE SUCKING POSITION,A N D THE RESPONSE TO TOUCHIN EWEA N D LAMB Successful sucking depends on ewe and lamb getting into the “inverse parallel” position described by Poindron (1976). In this position, the lamb’s muzzle pushes against the teat while the dam stands firmly with her head turned back, nosing at its hindquarters. Her back is arched and her hind leg extended in a way which raises the teat and makes it more prominent. According to Poindron (1976), 81% of sucking episodes in older lambs take place with the pair in this position and, for reasons given below, this is almost always the case for the first sucking episode. Tactile stimulation plays a large part in the achievement of the ewe’s suckling posture, the stimulation being provided by the lamb’s nuzzling during its approaches to the udder. Twelve Clun Forest ewes were tested for their response to touch, soon after suckling the lamb for the first time or on the next day. Each was tested in her pen, with her lamb or lambs in front of her. Under these conditions, a hand placed gently but firmly against the ewe’s belly, udder, inguinal area, or teat caused her to arch her back or extend a hind leg on the side that was stimulated. Ewes were unresponsive to touch in other areas, such as the back of the udder, axillary area, outer surfaces of the body, the shoulder, or upper part of the hind leg (Table IIa and b; Vince, 1987).
The suckling posture stops the ewe from circling, at least for a time. Attainment of this posture may be followed immediately by sucking, or the posture may have to be attained several times before the lamb sucks
249
NEWBORN LAMBS AND THEIR DAMS
TABLE IIa NUMBER OF LACTATING CLUN FORESTEWESOUT OF 12 RESPONDINGTO TOUCHON UNDERSIDEAND OUTERAREAS"
THE
Site stimulated Response
Shoulder
Axillary area
Back leg
Back arched Tail lowered Hind leg moved outward
0 0 0
1 0 0
0 0 0
Inguinal area
Belly
Teat 5 9
6 10 8
12
1. 2
7
(as shown by weight gain). Initially, the lamb may appear to be sucking, but is still losing weight, by evaporative water loss o r the dam's licking. Thus, the initial sucking period usually includes several bouts of attaining the sucking position and appearing to suck (Vince and Stanier, 1991). But attainment of the sucking position does mark a definite stage in the ewe/ lamb interaction, a point when the dam's behavior is controlled by that of the lamb. Teat location by the lamb also depends on touch. Bareham (1976) reported that newborn lambs nudge their mothers with forceful, pushing movements; and lambs also make munching and sucking movements against any part of the ewe with which their muzzles come into contact
TABLE IIb OF LACTATING CLUN FORESTEWESOUT OF 12 RESPONDINGTO TOUCHON NUMBER DIFFERENT PARTS OF THE UNDERSIDE' Site stimulated
Response Back arched Tail lowered Back leg moved outward Teat moved away from back leg
Mid belly
End of wool ventral to udder
Skin in front of teat
Lowest part of udder
I1
II
8
1 I
4 4
7
7 9
5
4
6
2
' From Vince (19871, by courtesy of E. J.
Brill, Leiden.
Inguinal area
Back of udder 3 I
4
5 9 7
0
5
3
0
250
MARGARET A. VINCE
back back
ears fore-
eves nose mouth chin
20 VI
10
! O
LC
0
0 unsuckled suckled Number of movements made by lambs in response to touch on each of eight different sites, before sucking (open columns) and after sucking (hatched columns). (From Vince er al., 1984.) FIG. 3.
(Collias, 1956; Smith, 1965). Much, or most of this nuzzling, or “teatseeking” activity, has been found to be a response to touch. Vince et a1 (1984) found that powerful forward and upward head movements, munching, and sucking occurred in response to covering the head and face. In a more detailed investigation using two fingers placed at different sites, these authors showed that touch on the lamb’s back, back of head or chin had little effect, but touch on the top of the head, upper parts of the face, and especially covering the eyes, resulted in the most intense forward and upward movements of the head and neck, whereas touch on the nose and mouth elicited most oral activity (Fig. 3). These responses tend to disappear after sucking (Section 111,E). Tactile stimulation of the lamb arises, initially. from licking by the dam, and most authors have found that she tends at first to lick her lamb’s front end (Shillito, 1971; Herscher et al., 1963; Sharafeldin and Kandeel, 1971). Later it must also result from the lamb’s own movements. In going toward the dam and pushing its muzzle against and under her, it receives the type of stimulation which results in its well known “search” for the teat. Whether this is a response to touch alone, or touch and loss of vision, has not been finally established. In Soay lambs the response to touch on the face was maintained for longer when they were blindfolded than when
NEWBORN LAMBS AND THEIR DAMS
25 1
they were able to see, but similar tests on Clun Forest lambs were inconclusive (see Vince, 1987, for summary). Covering the forehead, eyes, and muzzle results in vigorous and forceful movements which change direction from moment to moment; they include forward head movements, lengthening of the neck and upward tilting of the muzzle, jaw movements, tongue protrusions, mouth opening, arching back of the upper lip as in sucking, and munching movements (Figs. 4B, C , D, F, GI. The lamb’s head movements are oriented toward the source of stimulation: touch on the nose elicits upward movements of the head, and most lambs turn their heads in the appropriate direction when touched on the right or left lip. Responses to touch on the face include reaching movements of the muzzle, lower jaw, tongue, and upper or lower lip in the direction of the stimulus (Fig. 4B, E, G). Video-recordings made through a sheet of warmed plate glass against which the lamb’s muzzle was placed revealed patterns of oral activity: lambs moved their opened mouths over the glass with munching-type movements and almost incessant movements of the tongue, including licking, holding the tongue in a scoop- or U-shape, and moving it short distances in and out. Lambs respond visually also by turning their heads toward a finger appearing from behind their heads, but, when they .are touched, they respond sooner and more vigorously, they open their mouths more and make more munching movements, often grasping the finger. The response to touch changes as the lambs develop (Section 111,E); before they stand it appears only weakly. In Merino and crossbred lambs observed in the field, Vince et al. (1987) reported that nosing by the lamb increased during the first 30-45 min of life to about one-third of the time; it rose as the lambs stood more actively. At the same time the dam’s licking declined, and nosing and licking reached about the same level in the second half-hour of observation, although licking then continued to decline. At that stage, nosing o r nuzzling by the lamb would seem to play some part in keeping ewe and lamb together. The lamb appears to have a compulsion for nosing. Soay lambs removed from the dam at first standing and returned to her about 30 min later began nuzzling her for almost 80% of the time, more than they were licked by the dam. Clun Forest lambs removed from the dam at birth and returned to her about 1 hr later were divided into four groups according to their success in approaching the dam and sucking. These lambs nuzzled for between half and three fourths of the time, and those licked less by the dam directed much of their nuzzling to the sides of the pen, the straw bedding, or a fence (Table 111).
252
MARGARET A. VINCE
k F
NEWBORN LAMBS AND
253
THEIR DAMS
TABLE I11 PERCENTAGE OF TIMESPENTBY EWEA N D LAMBLICKING AND NUZZLING IN INTERRUPTED SOAYS“(FIRST2 1/2 MIN) A N D C L U N S(FIRST ~ 5 MIN) AFTER RETURNTO THE EWE Cluns
Number in group Ewe licks lamb Lamb nuzzles ewe Lamb nuzzles fence etc.
Soays
Subgroup A
Subgroup B
Subgroup C
Subgroup D
14 59.4 77.8 2.3
9 48.7 61.9 10.37
12 32.75 16.7 28.8
4 30.2 36.33 16.0
7 33.6 16.3 34.0
The Soay lambs were removed from the dam when first beginning to stand and returned to her about 30 min later. The Clun Forest lambs were removed from the dam at birth and returned to her after 60 min and observed for 30 min. Lambs in subgroup A all sucked within 10 min of being returned. Subgroup B all sucked, but after more than 10 min. Subgroup C failed to suck, but all achieved the sucking posture, and subgroup D failed to achieve the sucking posture within the observation period. All the Soays sucked.
The lamb’s responses to touch and sight indicate how it comes to locate the teat. After birth it makes for the dam, which under normal circumstances is the nearest large object, and noses first at her forequarters. Lambs often nuzzle in the dam’s axillary area before moving further toward the udder. Indeed, Stephens and Linzell(l974) found in the goat that the newborn located the teat and sucked earlier when the udder had been transplanted to the dam’s neck. Moving toward the udder with the directional mouthing, licking, sucking, and other reflex movements described, the lamb’s tongue or lip eventually comes into contact with, grasps, and sucks on any protuberance.
FIG.4. Elements of the response to facial touch in lambs tested before sucking. (A) The normal profile of a Clun Forest lamb when relaxed; (B) Soay lamb giving the full head up posture, mouth open and tongue protruded; (C) Clun Forest lamb, neck lengthened, head partially tilted upward, mouth open, upper lip drawn back, and lower lip extended forward; (D) Clun Forest lamb, head tilted upward, mouth open, upper lip drawn back, lower lip and tongue extended forward; (E)Clun Forest lamb, mouth open, upper lip drawn back, lower jaw and lip turned toward the stimulus; (F) Clun Forest lamb, neck extended, mouth open, upper lip and tongue reaching upward; (G)Clun Forest lamb, head, neck, and tongue stretched vertically upward toward stimulus. Diagrams were traced from video recordings. (From Vince, 1987. by courtesy of E. J. Brill, Leiden.)
254
MARGARET A. VlNCE
D. QUALITIES OF THE EWETHATAID I N TEATLOCATION BY THE LAMB Stephens and Linzell (1974) reported that the newly born kid nuzzles the dam in random forward and backward movements along her flank, and Bareham (1975) found that this pattern of teat-seeking occurs also in the newborn lamb. However, it was observed by Stephens and Linzell(l974) that, as the ewe’s teat lies in the groin, the curve of her abdomen leads the lamb into a funnel-shaped dark recess. The lamb’s nosing, giving an appearance of randomness, may be seen as superimposed on an underlying movement toward the udder, although this is frequently interrupted and reversed by the lamb or by the dam’s circling. This underlying movement depends partly on the lamb’s approaches to a visual pattern and partly on other qualities of the dam’s body. From the fetal stage (Section II,B), the lamb responds to temperature, and the dam’s surfaces differ in this respect. Those within the lamb’s reach were examined using an electric thermometer and a touch-on probe. Recordings made at 15 sites on the surfaces of lactating Clun Forest ewes (Fig. 5a) showed that there were marked differences between areas of naked skin and those covered with wool. Of the naked areas, highest readings were obtained from the inguinal region at the base of the udder, although the axillary area, the udder, and its surrounding wool-free skin also gave high readings (Vince, 1984). Recordings made from the smaller Soay sheep (Fig. 5b) showed similar differences between sites, although in general the readings were lower (Vince and Billing, 1986). It seems, therefore, that newly born lambs could be drawn toward the udder in much the same way as newborn kittens have been shown to use a thermal gradient, in this case consisting of parts of the mother’s body and littermates, in orienting toward home (Freeman and Rosenblatt, 1978). Newly born lambs were found by Vince (1984) to be attracted, and activated, by warmth. Two compartments were constructed, each 28 cm deep, 22 cm across, and 36 cm high. The back was closed in. One had a smooth warm (36-39°C) and the other a smooth cold (6-7°C) roof. Lambs were tested before they had sucked by holding each with the head just inside one of the compartments, and then releasing it. When inside, lambs pushed their heads actively forward and upward against the roof but they spent longer and were more active in the warm than in the cold compartment. In lambs which had not yet sucked, warmth enhanced the response to touch. When the side of a lamb’s face was placed gently but firmly against a warm (about 40°C) or a cold (about 8°C) surface and released, it maintained contact with the warm surface for longer than with the cold one, moved its
255
NEWBORN LAMBS AND THEIR DAMS
a
/
/
21.1
/(
29.0
34.4 35.1 24.7-E
b *20.0
17.6
4k23.3 *20.4 *26.1 18.3
26.1 37.2 31.8
32.7 36.2
35.5
34.0
18.4ik
18.6 FIG.5. Surface temperatures ("C)of lactating ewes: (a) Clun Forest and (b) Soay. Asterisks indicate sites at which measurements from the two breeds were significantly different. (From Vince, 1987, by courtesy of E. J . Brill, Leiden.)
muzzle over the surface for longer, and made more munching movements (Table IV). After sucking, there were no effects of temperature (Section
111,E). Billing and Vince (1987a) used the duration of nosing, number of times the lamb's mouth opened, and number of licks it made on a smooth surface as indices of its response in a more detailed analysis of the lamb's capacity to use temperature as a cue for teat location. At ambient temperatures of 18-20°C, newborn Clun Forest lambs opened their mouths more on surfaces held at 36 and 4 0 T , corresponding with the ewe's bare skin areas, than on surfaces at temperatures between 20 and 32"C, which are closer to
256
MARGARET A. VlNCE
TABLE IV LAMBS'RESPONSETO FACIAL CONTACT WITH WARM AND COLDSMOOTH SURFACES BEFORE AND AFTER BEING SUCKLED, IN 2o-SEC OBSERVATION PERIODS" After sucking (N = 1 I )
Before sucking (N = 11)
Mean behavior 1. Time muzzle
remained in contact (seconds) 2. Number of munches 3. Time mouth kept open (seconds) 4. Number of tongue protrusions 5 . Total distance of head movement (mm): a. Up b. Forward c. Down 6. Time muzzle moved over surface (seconds)
Warm surface
Difference between surfacesh
Cold surface
Warm surface
Difference between surfacesh
Cold surface
10.4
p
< .01
7.3
0.2
NS
0.6
23.9
p < .001
1.4
0.8
NS
0.3
1.8
NS
0.5
0.2
NS
0.5
I .9
NS
0.3
0
< .02 NS NS p < .01
81.3 60.9 43.2 9.3
12.7 2.5 20.3 0.6
109.2 81.3 38.1 12.3
p
0
NS NS NS NS
7.6 2.5 20.3
0. I
From Vince (1984). For items 1,2, 5a, 5b and 6. there were significant differences ( p < .001) between scores of lambs tested before and after sucking; for item 4. p < .05.
those of her woolly areas. They showed finer discrimination by responding more on a surface at 36 than at 32°C. In an ambient temperature 10°C lower, mouth opening increased most markedly at lower surface temperatures, that is, between 28 and 32°C. The extent to which activity is affected at ambient temperatures above 20°C is not known, but should the lamb lose its ability to utilize thermal cues in a very warm ambient temperature, its response to touch would still enable it to find the teat. The order in which sites at different temperatures were encountered was found to be important: change from a warm to a cool site elicited a smaller response on the cool site than if the cool site was encountered first. The dam's body varies also in its texture (smooth or woolly) and in the degree of surface yield, the udder being the most yielding. Billing and
NEWBORN LAMBS AND THEIR DAMS
257
Vince (1987b) found that, when the face of a newborn Clun Forest lamb was pressed against a warm smooth surface, more oral activity was produced than when the surface was woolly. Similarly tested Soay lambs nosed and opened their mouths against the most udderlike, intermediateyielding surfaces more than they did against the highest and lowestyielding ones presented to them, and Clun Forest lambs nosed a lowyielding surface which was fixed less than they nosed a similar, but movable surface. The possibility that odors from the dam may aid in teat location was investigated by Vince and Ward (1984). in this case using changes in heart and respiration rate as well as behavior as indices of response. One odorous substance is the inguinal wax produced by a gland on the outer surface of the udder; this tends to spread over the surrounding skin and wool. Lambs taken from the dam at birth were tested at about the time of first standing with samples of their own dam’s inguinal wax, wool from her back, and her milk, and also with these three substances taken from an alien ewe. Lambs responded with more movements to the dam’s than to alien wax. There was no significant effect on heart rate, but their respiration rate rose during stimulation with maternal wax whereas it showed little change to the alien substance. It seems possible that this result reflects the lamb’s prenatal experience. In this experiment, the direction of the heart rate response differs from that carried out with sound (Section IIB). It is not known whether this difference is due to the sensory modality (audition or olfaction), to sniffing, or to differences in the experimental situations: in the first, the only change was introduced by the recorded sound, whereas the second included movement when the stimulus was presented. The experiment on olfaction (Vince and Ward, 1984) shows that inguinal wax has properties characteristic of individual ewes. Similarly, a ewe’s bleats have been found to include a combination of characteristics which distinguish them from the bleats of other ewes (Shillito Walser and Hague, 1980; Shillito Walser et al., 1981). However, warmth and tactile qualities are common to all lactating ewes and, as these are important stimuli for the lamb’s presucking activity, it is mainly the dam’s behavior (specifically her olfactory discrimination and licking) which keeps the pair together at first (Section 11,A); when kept in a flock, unattended lambs often approach and nuzzle alien ewes. The dam possesses physical qualities, the possible effects of which still need investigating. One of these is her mobility; some breeds are more mobile than others and mobility is affected by age and parity; primiparous ewes are often “nervous” or “wary.” The ewe’s head, in licking or looking up in response to sudden sounds or movements, is especially
258
MARGARET A. VlNCE
mobile and could affect the newborn. Shillito Walser et al. (1984) found that older lambs were more attracted to maternal bleats when the bleats were accompanied by raising of the ewe’s head. The interchange of vocalizations between ewe and lamb, noted by Bareham (1976). might also repay more detailed investigation.
E. DEVELOPMENTAL ASPECTS OF THE LAMB’S RESPONSE TO TOUCH AND THE EFFECTOF SUCKING ON LAMBBEHAVIOR There are obvious developmental changes in the lamb immediately after birth: it rights itself, struggles to stand, gets on to all four feet, and its coordination improves. During this time its response to touch also changes. Upward head movements in response to touch on the face (Section III,C) become stronger when the lamb stands; earlier they are sometimes replaced by a downward movement of the head. Also, when stimulated by touch on the haunches or under the tail, lambs which had not stood moved their legs, or pushed up on their hind legs without nosing or munching movements, whereas lambs already standing made stepping movements and many nosed at nearby objects (Vince, 1987). Nuzzling at the dam increased rapidly during the first 45 min of life in Merino and crossbred lambs observed in the field with the dam (Vince et al., 1987). This nuzzling, with its concomitant head and neck movements (Section III,C), is readily elicited by touch in the period between standing and sucking, but is more difficult to elicit at any time after the first sucking bout, especially in lambs kept with the dam. There is evidence that this change results from feeding. Keeping age constant by testing at 2 hr after birth, more lambs which had not fed responded to touch on the face, and they responded more vigorously, than did lambs which had fed 1 hr earlier. Older Soay lambs (1-16 hr of age), kept with the dam and already suckled, responded to discrete amounts of tactile stimulation on the head and face with fewer head movements and much less oral activity than did lambs tested before feeding. Massage of the top of the head and forehead in the older lambs was associated with forward and downward head movements (Vince et al., 1984). Similarly, in Clun Forest lambs tested before and then again 30 min after sucking, an initial vigorous response to touch on forehead, eyes, and muzzle declined into small upward movements of the head and minimal amounts of oral activity (Vince, 1987; and Fig. 6). The effect of food intake on the newborn lamb’s response to facial touch has been investigated in more detail by Vince and Stanier (1991). Soay and Clun Forest lambs were observed in the field with their dams during the presucking phase. They were taken, weighed, and tested for their response to facial touch each time they appeared to have sucked. Their
259
NEWBORN LAMBS AND THEIR DAMS
-1
MOUTH OPENED
TIME HEAD UP
LIP ARCHED
n
TONGUE MOVEMENTS
c
0
j, E C
n
FIG.6. Effect of feeding on the lamb's response to facial touch. A hand was placed over the lamb's face before (open columns) and after (hatched columns) it had spent 30 min with the dam. (From Vince and Bilking, 1986. by courtesy of Ablex Publishing Corp.)
response to touch remained vigorous until they had achieved a gain in weight; they appeared to go on responding until satiated. However, the response to facial touch is not abolished completely, even in lambs kept with the dam and suckled normally. Soay lambs aged between 1 and 7 days were tested after being muzzled for 4 hr to prevent their sucking. In these, the response to facial touch reappeared, albeit in a diminished form compared with that in lambs tested before sucking. So, it would appear that, under normal conditions with the dam, lambs are fed too frequently to become very hungry. According to Bareham (1976), lambs are fed about 10 times an hour during the first few hours after birth. The response to facial touch as provided by an experimenter is not linked to feeding alone. Lambs reared artificially by feeding every 4 hr from a trough with teats attached, and tested 3.5 hr after feeding, continued to respond as vigorously as they did before their first feed after birth until they were about 1 week old (Vince and Stanier, 1991). Thus, they behaved differently from the Soays kept with the dam and tested after being muzzled. Under normal conditions, lambs are not only fed frequently, they are becoming conditioned to the dam. As with touch, lambs appear to be more sensitive to warmth before, than after, feeding. Brought into facial contact with a warm, smooth surface, the minimal response of suckled lambs aged up to 16 hr was not
260
MARGARET A . VINCE
affected by temperature (Table IV; Section III,D) and they stood or lay down quietly, whether the compartment in which they were placed was warm or cold; conditions in which unsuckled lambs discriminated by staying longer, and becoming more active, in the warm (Vince, 1984). The lamb’s response to odor also changed, but in a different way, between the pre- and postsucking phases. The increase in the activity and respiration rate observed in unsuckled lambs in the presence of maternal, but not alien inguinal wax (Section III,D) did not occur after sucking in lambs aged between 3 and 21 hr. However, in response to the same stimulus, these suckled lambs gave a more marked increase in heart rate and showed a significant difference between maternal and alien wax. This, again, suggests conditioning to the dam.
F. CIRCLING BY THE DAMAND EWEA N D LAMB PATTERNS OF MOVEMENTINVOLVED I N THE PRESUCKING, SUCKING, A N D IMMEDIATELY POSTSUCKING PHASES Section III,B describes the lamb’s approaches to the udder and the dam’s “circling,” which interrupts or prevents the movement. Circling usually initiates another movement toward the udder. In some ewes, especially those lambing for the first time, the dam may initially circle repeatedly or retreat from the lamb (Alexander, 1960; Sharafeldin and Kandeel, 1971). In Soay sheep, lamb movement toward the udder followed by circling can occur as frequently as once per minute, demonstrating the strength and persistence of the lamb’s movements of approach, which can ultimately bring a recalcitrant dam into the posture for suckling (Vince, 1992). Circling may be obstructive, as in a primiparous ewe which may lick her lamb but avoid its nosing of the udder. However, it can be beneficial. Especially in the early stages after birth, lambs often nose at the dam’s forequarters, or at her undersides (possibly kept there by her warmth), or they may go past the udder and nose at her rear end. These are areas which do not induce the sucking pattern (Section 111,A). Sometimes lambs nose at the placenta. Circling brings the lamb back to the dam’s head, from which a new and more successful approach can be made from the original position. The first time ewe and lamb get into the sucking position the lamb’s approach has in almost all cases been made from the ewe’s head end (Table I; Section 111,B).If the stimulus for approach is a visual pattern, as has been suggested in Section I K B , this is the position in which it becomes available to the lamb. Recent work on Soay ewe/lamb pairs (Vince, 1992) has shown that the to-and-fro pattern, made up of approaches and circlings, continues
NEWBORN LAMBS AND THEIR DAMS
26 1
between sucking, or apparent sucking, bouts and for some time after the lamb appears to be satiated. However, one aspect of the pattern changes after sucking: circling by the dam falls off and tends to be replaced by the lamb itself returning intermittently to the dam’s head. At the same time, there is a considerable drop in nosing (Table V). It seems that, as activity associated with teat location declines, the lamb responds more to other aspects of the dam, such as her forequarters, her vocalizations, and head movements. The movement of approach appears to be a more persistent pattern than the reflex nuzzling. After sucking, the time spent nuzzling by Soay lambs fell to about half, whereas the number of approaches fell much less. Lambs tended to keep on going toward the udder, perhaps sucking (or apparently sucking) briefly, nosing the udder, or just walking round the dam’s hindquarters and returning to her head. When at her head they stood about, or first began frolicking or nosing the grass near her muzzle as she grazed, then finally lying down beside the dam and going to sleep. The new behavior patterns indicate an end to the first sucking period (Vince, 1992). In the newborn, the to-and-fro pattern contains the elements of the pattern in which older lambs approach the udder (Poindron, 1976). Mostly, older lambs move toward and round the dam’s head before proceeding to the udder, allowing the ewe to sniff at their hindquarters, an act which complements vision and hearing in their identification (Alexander and Shillito, 1977). The pattern is important at all stages, and the newborn’s approaches and returns may indicate how it develops. It seems possible that the newborn’s movements of approach are not only reinforced ultiTABLE V LAMBA N D EWEACTIVITY AT THREE STAGES FROM STANDING TO LYINGDOWNAFTER FIRSTSUCKING PERIOD“ Before sucking
During sucking
A. Mean number of movements per minute (weighted mean)” Lamb approaches 0.89 (0.20-1 S O ) I .27 (0.73-1.73) 0.70 (0.49-0.83) Lamb returns 0.28 (0.00-0.98) 0.40 (0.00-1.50) 0.58 (0.40-1.00) Ewe circlings B. Mean number of seconds per minute of lamb nosing At dam’s forequarters 13.06 (5.23-24.60) 4.16 (1.03-96.0) At dam’s hindquarters 18.53 (5.93-32.60) 30.06 (16.13-46.6) (including sucking)
After sucking 0.97 (0.20-1.62) 0.61 (0.20-1.03) 0.34 (0.00-1.16)
2.14 (0.60-7.35) 14.60 (5.41-29.8)
From Vince (1992), by courtesy of Elsevier Science Publishers. Weighted means are shown and different lengths of time were included in means for different lambs. The range for each mean is given in parentheses.
262
MARGARET A. VlNCE
mately by sucking but earlier may be instigated by the dam’s circling: the lamb is known to respond in particular to moving objects. The stimulus for the lamb’s movements of return to the dam’s head is unknown. They could be elicited by her vocalizations or her head movements. The postnatal interaction is both flexible and adaptive. The lamb’s vigorous response to touch, its approaches to the udder, and the to-and-fro pattern of movement occur whether the dam is accepting or less accepting, except that in the latter case more approaches are needed before the dam is brought into the position for suckling. IV. DISCUSSION
In the lamb, all sensory systems are functional at the time of birth and all are involved, at some stage, in the newborn’s interaction with the dam. There are indications, however, that the lamb’s behavior is not always dominated by stimulation in the same sensory modality. In the first stage after birth, as well as responding to gravity, the newborn responds to touch in the form of maternal licking and to the sound of the dam’s low-frequency vocalizations; both of the last two slow the lamb’s standing, but visual stimulation, resulting in the lamb’s struggle to stand and move toward and under the dam, appears to predominate. The ewe is a composite stimulus for the lamb, and it stands up and moves toward the dam despite her quieting aspects. There is evidence that a ewe’s highfrequency bleats also activate an isolated lamb and advance its standing, but ewes rarely bleat in this way during the presucking stage unless separated from their lambs (Section 111,A). After standing, movement toward the dam continues as movement along her flank and toward the udder, still in response to visual stimulation. At this stage, of equal or greater importance is the lamb’s response to touch on the head, face, and muzzle as it comes up against the dam. This response to touch provides its “teat-seeking’’ behavior, and it is enhanced by the dam’s warmth, odor, and tactile qualities (Section 111,D).The lamb’s response to facial touch is an overwhelmingly important, but transitory, component of its development and it leads to teat location and sucking (Section 111,C). Under normal conditions with the dam, once the lamb is satiated its response to facial touch declines or disappears. New behavior patterns appear and, before lying down with the dam and going to sleep, the lamb circles around her, or stands, sometimes frolicking or making grazing movements, by her head (Section IILF). The next stage is to become bonded to the dam. Although an isolated lamb under about 3 days of age tends to stand still and bleat until the dam
NEWBORN LAMBS A N D THEIR DAMS
263
finds it (Shillito, 1973, there is evidence that, during the first few days after birth, it comes to recognize the dam by voice (Shillito Walser et af., 1982),and many lambs discriminate between the dam and an alien by sight within 24 hr of birth (Shillito and Alexander, 1975). Nowak et al. (1987, 1989) found that even younger, 12-hr-old,crossbred lambs spent more time next to the dam than next to an alien ewe when these were at close quarters to, but separated from, them. Merino lambs were slower to achieve this discrimination, which these authors found to be based on visual and auditory cues arising from the dam’s behavior. The dam made low-frequency vocalizations and moved actively toward the lamb, whereas the alien ewe did not. Similarly, discrimination of the dam at a distance, evident between 2 and 3 days of age, was found to depend on visual and auditory stimulation (Nowak, 1991). The lamb, therefore, appears to be learning rapidly during the first hours and days of life, and the learning is more subtle than simply of the whereabouts of the teat. However, the gradual buildup of this process of learning and the factors involved in it, stemming from either partner, still need detailed investigation. We do not know what are the salient features of the interaction which have lasting effects on the lamb’s behavior. Analysis of the ewe/lamb interaction before sucking shows that, although olfaction is of primary importance for the dam’s maternal behavior and the lamb responds to her in all sensory modalities, it is mainly visual stimulation which initiates, and then mainly touch which maintains, the lamb’s presucking activity and enables it to locate the teat. Tactile stimulation from the lamb also brings the dam into the posture for suckling. This last process resembles that in the Norway rat, in which tactile stimuli from the young elicit the dam’s nursing posture (Stern and Johnson, 1988). However, in altricial young such as the rat, rabbit (Distel and Hudson, 1985), and the kitten (Larson and Stein, 1984; Freeman and Rosenblatt, 1978), olfactory cues are of great importance in their search and feeding behavior. Such animals are born at a very immature stage, and blind, into the restricted conditions within a nest. In the active and precocial sheep the possibility of separation from the dam is greater than in these altricial species and the route to the teat less direct. The lamb’s “search” behavior depends much less on olfaction and more on sight and touch, which help to maintain contact with the dam as well as to bring the lamb to the udder and enable it to locate and grasp the teat. V. SUMMARY By the time of the lamb’s birth, the dam’s maternal behavior and all sensory systems of the newborn are already functioning; factors involved
264
MARGARET A. VINCE
in this twofold development are discussed as they affect the behavioral interaction between ewe and lamb which leads to teat location and sucking. The lamb’s response to gravity in righting itself and standing is modified by the dam’s activities, vocalizations, and some environmental factors. Even before standing, it begins to move under the dam and toward the udder, apparently responding to visual cues. Movement of the lamb toward the udder, often counteracted by the dam’s licking and “circling,” is frequently repeated and results in tactile stimulation of the newborn’s head and muzzle. This contact elicits vigorous head movements and a directional, oral “search” which ends with teat location and sucking. The lamb’s response to touch is facilitated by thermal, olfactory, and textural qualities in the dam, while its nuzzling in the udder area elicits a response to touch in the dam also, causing her to stand and present the teat. The lamb’s response to touch gives it some affinity with the altricial newborn, but in sheep this response is transitory, at its height between the times of first standing and sucking, and it diminishes or disappears when the lamb has sucked to satiation, reappearing only under exceptional conditions. After sucking, new behavior patterns appear in the lamb and the later ewe/lamb interactions which lead to effective bonding are known to depend mainly on sight and sound.
Acknowledgments In working on sheep, I am deeply indebted to my colleagues at the AFRC Institute of Animal Physiology, Babraham, Cambridge and also at the CSIRO Division of Animal Reproduction, Armidale. New South Wales, Australia for their friendly cooperation, help, and stimulation.
References Alexander, G. (1960). Maternal behaviour in the Merino ewe. Proc. Ausr. Soc. Anim. Prod.
3, 105-114. Alexander, G . , and Shillito, E. E. (1977). The importance of odor, appearance and voice in maternal recognition of the young in merino sheep (Ouis aries). Appl. Anim, Erhol. 3, 127-135. Alexander, G.. and Stevens, D. (1985). Fostering in sheep. 111. facilitation by the use of odorants. Appl. Anim. Behau. Sci. 14, 345-354. Alexander, G.. Poindron, P., LeNeindre, P., Stevens, D., Levy, F., and Bradley, L. (1986). Importance of the first hour post-partum for exclusive maternal bonding in sheep. Appl. Anim. Behau. Sci. 16,295-300. Alexander, G., Stevens, D., and Bradley, L. R. (1988). Maternal behaviour in ewes following Caesarian section. Appl. Anim. Behau. Sci. 19, 273-217.
NEWBORN LAMBS AND THEIR DAMS
265
Arnold, G. W., and Morgan, P. D. (1975). Behaviour of the ewe and lamb at lambing and its relationship to lamb mortality. Appl. Anim. Erhol. 2, 25-46. Baldwin, B. A., and Shillito, E. E. (1974). The effect of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. Anim. Behau. 22,220-223. Barcroft, J., and Barron, D. H. (1936). “The Development of the Righting Movements in the Foetal Sheep.” Film presented to the Physiological Society (UK). Now deposited with the Wellcome Institute for the History of Medicine, 183, Euston Rd. London, NW 1 2BP. Barcroft, J., and Barron, D. H. (1939). The development of behaviour in foetal sheep. J . Comp. Neurol. 70, 477-502. Bareham, J. R. (1975). The effect of lack of vision on suckling behaviour of lambs. Appl. Anim. Ethol. 1, 245-250. Bareham, J. R. (1976). The behaviour of lambs on the first day after birth. Br. Vet. J . 132, 152- 161. Bernhard, C. G., Kaiser, I. H., and Kolmodin, G. M. (1959). On the development of cortical activity in fetal sheep. Acra Physiol. Scand. 47, 333-349. Billing, A. E., and Vince. M. A. (1987a). Teat-seeking behaviour in newborn lambs. 1. Evidence for the influence of maternal skin temperature. Appl. Anim. Behau. Sci. 18, 301-3 13. Billing, A. E., and Vince, M. A. (1987b).Teat-seeking behaviour in newborn lambs: Evidence for the influence of the dam’s surface textures and degree of surface yield. Appl. Anim. Behau. Sci. 18, 315-325. Bradley, R. M., and Mistretta, C. M. (1973). The gustatory sense in foetal sheep during the last third of gestation. J. Physiol. (London) 231, 271-282. Bradley, R. M., and Mistretta, C. W. (1975). Fetal sensory receptors. Physiol. Rev. 55, 352-382. Collias, N. E. (1956). The analysis of socialisation in sheep and goats. Ecology 37, 228-239. Dawes, G. S. (1973). Breathing and rapid eye-movement sleep before birth. I n “Foetal and Neonatal Physiology: Proceedings of the Sir Joseph Barcroft Centenary Symposium” (R. S. Comline, K. W. Cross, G. S. Dawes, and P. W. Nathalielsz, eds), p. 55. Cambridge Univ. Press, Cambridge. Distel, H., and Hudson, R. (1985). The contribution of the olfactory and tactile modalities to the nipple-search behaviour of newborn rabbits. J . Comp. Physiol. A 15, 599-605. Fraser, A. F. (1985). Kinetic behaviour of the fetus and newborn. I n “Ethology of Farm Animals’’ (A. F. Fraser, ed.), Chapter 10. Elsevier, Amsterdam. Freeman, N. C. G., ancfRosenblatt, J. S. (1978). The interrelationship between thermal and olfactory stimulation in the development of home orientation in newborn kittens. Deu. Psychobiol. 11,437-457. Herscher, L., Richmond, J. B., and Moore, A. U. (1963). Maternal behaviour in sheep and goats. I n “Maternal Behaviour in Mammals” (H. L. Rheingold, ed.), pp. 203-232. Wiley, New York. Kendrick, K. M., Keverne, E. B., and Baldwin, B. A. (1987). Intracerebroventricular oxytocin stimulates maternal behavior in sheep. Neuroendocrinology 44, 56-61. Keverne, E. B., Levy, F., Poindron, P., and Lindsay, D. R. (1983). Vaginal stimulation: An important determinant of maternal bonding in sheep. Science 219, 8 1-83. Larson, M. A., and Stein, B. E. (1984). The use of tactile and olfactory cues in neonatal orientation and localisation of the nipple. Deu. Psychobiol. 17, 423-436. LeNeindre, P., Poindron, P., and Delouis, C. (1979). Hormonal induction of maternal behaviour in non-pregnant ewes. Physiol. Behau. 22, 731-734. Levy, F., and Poindron, P. (1984). Influence of amniotic fluids in the manifestation of maternal behaviour in parturient ewes. Biol. Behau. 9, 271-278.
266
MARGARET A. VINCE
Levy, F., and Poindron, P. (1987). The importance of amniotic fluids for the establishment of maternal behaviour in experienced and inexperienced ewes. Anim. Eehau. 35, 1188-1 192. Levy, F., Poindron, P.. and LeNeindre, P. (1983). Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition. Physiol. Eehau. 31, 687-692. Levy, F., Kendrick, K. M., Keverne, E. B., Piketty, V., and Poindron, P. (1992). Intracerebra1 oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anaesthesia. Eehau. Neurosci. 106, 427-432. Lynch, J. J. and Alexander, G. (1973). Animal behaviour in the pastoral industries. In “The Pastoral Industries of Australia” ( G . Alexander and B.O. Williams. eds). pp. 371-400. Sydney Univ. Press, Sydney, Australia. Mellor, D. J., and Slater, J. S. (1971). Daily changes in amniotic and allantoic fluid during the last three months of pregnancy in conscious, unstressed ewes, with catheters in their foetal fluid sacs. J . Physiol. (London)217, 573-604. Nowak, R. (1991). Senses involved in discrimination of merino ewes at close contact and from a distance by their newborn lambs. Anim. Eehau. 42, 357-366. Nowak, R.,Poindron, P., LeNeindre, P., and Putu, 1. G. (1987). Ability of 12-h-old Merino and crossbred lambs to recognise their mothers. Appl. Anim. Eehau. Sci. 17, 263-271. Nowak, R., Poindron, P., and Putu, I. G. (1989). Development of mother discrimination by single and multiple newborn lambs. Deu. Psychobiol. 22, 833-845. Pedersen, P., and Blass, E. M. (1982). Prenatal and postnatal determinants of the 1st suckling episode in albino rats. Deu. Psychobiol. 15, 349-355. Persson. H . E., and Sternberg, D. (1972). Early prenatal development of cortical surface responses to visual stimuli in sheep. Exp. Neurol. 37, 199-208. Poindron. P. (1976). Mother-young relationships in intact or anosmic ewes at the time of sucking. Eiol. Eehau. 2, 161-177. Poindron, P., and LeNeindre, P. (1980). Endocrine and sensory regulation of maternal behaviour in the ewe. Ad. Study Eehau. 11, 75-1 19. Poindron, P., Martin, G . B., and Hooley. R. D. (1979). Effects of lambing induction on the sensitive period for the establishment of maternal behaviour in sheep. Physiol. Eehau. 23, 1081-1087. Poindron, P., LeNeindre, P., Raksanyi, I., Trillat, G., and Orgeur, P. (1980). Importance of the characteristics of the young in the manifestation and establishment of maternal behaviour in sheep. Reprod. Nutr. Deu. 20,817-826. Poindron, P., Levy, F., and Krehbiel, D. (1988).Genital, olfactory and endocrine interactions in the development of maternal behaviour in the parturient ewe. PsychoneuroendocrinolORY 13999-125. Rosenblatt. J. S.. and Siegel, H. 1. (1983). Physiological and behavioural changes during pregnancy and parturition underlying the onset of maternal behaviour in rodents. In “Parental Behaviour of Rodents” (R.W. Elwood. ed.), pp. 23-66. Wiley, New York. Schaal, B.. and Orgeur, P. (1992). Olfaction in utero: Can the rodent model be generalised? Q. J . Exp. Psychol. B . Comp. Physiol. Psychol. 44B, 245-278. Schaal, B., Orgeur, P.,Lecanuet, J.-P., Locatelli, A., Granier-Deferre, C., and Poindron, P. (1991). Chimioreception nasale in utero: Experiences prkliminaires chez le foetus ovin. C.R. Seances Acad. Sci., Ser. 313, 319-325. Sharafeldin, M. A., and Kandeel, A. A. (1971). Post-lambing maternal behaviour. J . Agric. Sci. 77,33-36. Shillito, E. E. (1971). Observations on parturition and maternal care in Soay sheep. J . 2001. 165, 509-5 12.
NEWBORN LAMBS AND THEIR DAMS
267
Shillito. E. E. (1972). Vocalisation in sheep. J. Physiol. (London) 226, 45P-46P. Shillito. E. E. (1975). A comparison of the role of vision and hearing in lambs finding their own dams. Appl. Anim. Ethol. 1, 369-377. Shillito. E. E.. and Alexander, G. (1975). Mutual recognition amongst ewes and lambs of four breeds of sheep (Ouis aries). Appl. Anim. Ethol. 1, 151-165. Shillito, E. E. and Hoyland, V. J. (1971). Observations on parturition and maternal care in Soay sheep. J . Zoo1 165, 509-512. Shillito Walser. E. E.. and Alexander. G. (1980). Mutual recognition between ewes and lambs. Reprod. Nirtr. Deu. 20, 807-816. Shillito Walser. E. E.. and Hague, P. (1980). Variation in the structure of bleats from sheep of four different breeds. Behauiour 75, 212-235. Shillito Walser, E. E., Walters. E., and Hague. P. (1981).A statistical analysisofthe structure of bleats from sheep of four different breeds. Behauior~r77, 67-76. Shillito Walser. E. E., Willadsen. S.. and Hague P. (1982). Maternal vocal recognition in lambs born to Jacob and Dalesbred ewes after embryo transplantation between breeds. Appl. Anim. Ethol. 8, 479-486. Shillito Walser, E. E., Walters, E.. and Ellison, J. (1984). Observations on vocalisation of ewes and lambs in the field. Behauiour 91, 190-203. Slee, J., and Springbett, A. (1986). Early post-natal behaviour in lambs of ten breeds. Appl. Anim. Behau. Sci. 15, 229-240. Smith, F. V. (1965). Instinct and learning in the attachment of ewe and lamb. Anim. Behau. 13, 84-86. Smith, F. V., Van Toller, C., and Boyes, T. (1966). The critical period in the attachment of lambs and ewes. Anim. Behau. 14, 120-125. Smotherman, W. P. (1982). Odor aversion learning by the rat fetus. Phvsiol. Behau. 29, 769-77 I . Smotherman, W. P., and Robinson, S. R. (1988). Behavior of rat fetuses following chemical or tactile stimulation. Behau. Neurosci. 102, 24-34. Stephens, D. B., and Linzell, J. L. (1974). The development of suckling behaviour in the newborn goat. Anim. Behau. 22, 628-633. Stern, J. M., and Johnson, S. K. (1988). Perioral somatosensory determinants of nursing behaviour in Norway rats. J . Comp. Psycho/. 103, 269-280. Vince, M. A. (1984).Teat-seeking behaviour in newly born lambs: Possible effects of maternal skin temperature. Anim. Behau. 32, 249-254. Vince, M. A. (1986).Response of the newly born Clun Forest lamb to maternal vocalisations. Behauiour 96, 164-170. Vince, M. A. (1987).Tactile communication between ewe and lamb and the onset of suckling. Behauiour 101, 156-176. Vince, M. A. (1992). The newly born lamb's patterns of activity before, during and after the first sucking bout. Appl. Anim. Behau. Sci. 33, 27-33. Vince, M. A., and Billing, A. E. (1986). Infancy in the sheep: The part played by sensory stimulation in bonding between ewe and lamb. I n "Advances in Infancy Research" (L. P. Lipsitt and C. Rovee-Collier, eds.), Vol. 4, pp. 1-37. Ablex, Nonvood, NJ. Vince, M. A., and Stanier, M. (1991). The effect of food intake on young Soay and Clun Forest lambs' response to touch on the face. Appl. Anim. Behau. Sci. 30, 87-96. Vince. M. A., and Ward, T. M. (1984).The responsiveness of newly born Clun Forest lambs to odour sources in the ewe. Behauiour 89, 117-127. Vince, M. A., Armitage, S. E., Shillito Walser. E. E., and Reader, M. (1982a). Postnatal consequences of prenatal sound stimulation in the sheep. Behauiour 81, 128139.
268
MARGARET A. VINCE
Vince, M. A., Armitage, S.E., Baldwin, B. A.. Toner, J., and Moore. B. C. J. (1982b). The sound environment of the foetal sheep. Behaviour 81, 296-315. Vince, M. A., Ward, T. M., and Reader, M. (1984). Tactile stimulation and teat-seeking behaviour in newly born lambs. Anim. Behau. 32, 1179-1 184. Vince, M.A., Billing, A. E., Baldwin, B. A., Toner, J. N., and Weller. C. (1985a). Maternal vocalisations and other sounds in the fetal lamb's sound environment. Early Hum. Deu. 11, 179-190. Vince, M. A., Lynch, J. J., Mottershead, B.,Green, G., and Elwin. R. (1985b). Sensory factors involved in immediately postnatal ewellamb bonding. Behaviour 90, 60-84. Vince, M. A., Lynch, J. J., Mottershead, B. E.. Green, G. C., and Elwin. R. L. (1987). Interactions between normal ewes and newly born lambs deprived of visual, olfactory and tactile information. Appl. Anim. Behau. Sci. 19, 119-136.
ADVANCES
IN T H E STUDY OF BEHAVIOR.
VOL. ??
The Ontogeny of Social Displays: Form Development, Form Fixation, and Change in Context T. G. G. GROOTHUIS ZOOLOGICAL L.ABORATORY UNIVERSITY OF GRONINGEN 9750 AA HAREN. THE NETHERLANDS
I. GENERALINTRODUCTION A.
WHY STUDYTHE DEVELOPMENT OF DISPLAYS?
Displays are conspicuous, stereotyped, and often species-specific postures, movements, and vocalizations which are used in social interactions. These motor patterns are part of the behavioral repertoire of numerous animal species from different taxa, ranging from insects and crabs via reptiles and birds to mammals, including man. These displays have caught the attention of ethologists since the beginning of Ethology. The conspicuous and stereotyped form of these motor patterns, together with their species specificity, have raised the question as to the function and evolution of displays (e.g., Tinbergen, 1952, 1959, 1965). Although answers to these questions were partly derived from the analysis of the proximate causation of displays (e.g., Moynihan, 1955; see also Baerends, 1975 for a review), this has received less attention, especially in recent decades. The causal analysis of the ontogeny of displays has been even more neglected, with the exception of song development in songbirds. Although descriptive studies on the ontogeny of displays have been published, few papers report a quantitative and experimental approach to the analysis of the underlying causal mechanisms. This may be for two reasons:
1. The species specificity of many displays, together with their stereotyped form, may have led to the conclusion that the ontogeny of these motor patterns depends mainly on genetic information. Consequently, display development has been interpreted as an uninteresting subject for studies of behavioral development. 269 CopyriKht Q 1993 by Academic Press. Inc. All rights of reproduction in any form reserved.
270
T. G. G. GROOTHUIS
2. Displays are part of social behavior and therefore more difficult to manipulate than motor patterns involved in nonsocial behavior, such as locomotion, feeding, or comfort behavior.
The first reason is a view which was expressed, and might have been encouraged, by Lorenz’s definition of a “Fixed Action Pattern.” In this definition, he incorporated not only the stereotypy of the form of the motor pattern as a criterion, but also its causation and ontogeny. In relation to the latter he assumed that such patterns were “innate,” which literally means “present at birth.” However, no convincing evidence was given for this. Furthermore, innate is often, more or less explicitly, used to mean “determined by genes alone.” Although remnants of the old nature-nurture dichotomy still survive in the literature, the idea is clearly obsolete (Lehrmann, 1953; Kruijt, 1964; Hailman, 1967; Bateson, 1983; Oyama, 1985; Johnston, 1988). The outcome of developmental processes is the result of a continuous interaction between genetic information and other internal and external factors. Genetic information is obviously involved in the development of all species-specific behavior, but this information alone is nothing more than the genes themselves, the potential of which can only be expressed and translated into behavior in interaction with other factors. It is the task of the developmental biologist to unravel this interactive process. The following sections show that further research is both useful and necessary. As far as the second reason is concerned, in the following sections it is shown that the ontogeny of social display can be experimentally manipulated in order to test its underlying mechanism just as with other motor patterns. This approach is necessary because, without further research, it can be questioned whether the ontogeny of nonsocial motor patterns follows the same principles as the ontogeny of social displays. Apart from the fact that not much is known about the ontogeny of social displays, there are two other good reasons to study its underlying mechanism: (a) Since displays consist of conspicuous and stereotyped motor patterns which are complex in form but easily recognizable, they offer interesting opportunities for the study of motor development. (b) Since displays are part of social behavior, the analysis of their ontogeny may give insight into the development of social behavior in general. Furthermore, by following the development of the increasing complexity of adult social behavior one may gain insight into the causal mechanisms of adult social behavior, the developmental outcome.
B. QUESTIONS TO BE ASKED A N D FRAMEWORK OF THIS ARTICLE In my view, at least five different but related aspects of the development of displays need to be considered.
ONTOGENY OF SOCIAL DISPLAYS
27 I
1. The mechanisms underlying the development of theJinal adult form of display. This aspect requires a detailed quantitative description of the course of normal development of the form of display and the manipulation of relevant internal and external factors. Questions to be considered here are, Does display develop gradually or is it completely present early in ontogeny? Is the species specificity of the adult form of behavior due to species-specific experience, or based on some sort of predisposition, or an interaction between the two? What is the nature of the relevant experience or predisposition? How flexible is the developmental process, both with respect to the timing of emergence and to the form of the display? These questions and, consequently, a discussion of possible causal mechanisms underlying display development, are dealt with in Section 11. 2. The process by which display becomes stable in the adult stereotyped form. This aspect needs to be considered separately from the preceding one: it concerns the aspect of form fixation of already developed motor patterns. The idea, which is frequently encountered in the literature, that adult animals perform more stereotyped motor patterns than young ones, needs more quantitative evidence and a causal explanation. The questions why adult animals rarely fall back on juvenile behavior patterns, and whether these juvenile patterns still exist in the adult or have been reorganized in the course of development are also relevant in this context. Form fixation is discussed in Section 111. 3. The way in which the separate motor patterns become integrated in functional behavioral programs. While the first two aspects concern the development of motor form and stereotypy, this one deals with how the young animal develops the ability to use the motor patterns in the proper context. The main questions here are whether the application of the displays changes in the course of development, whether this change depends on experience, and how this change is related to changes in the motivational background of the display. It requires a detailed analysis of ontogenetic shifts in context of the displays and in their temporal sequences with other motor patterns, which is not an easy task because it often requires the analysis of complex social interactions. Some results on this aspect of display development are mentioned in Section IV. 4. The ontogeny of comprehension of the signal value of the different displays. This asks when and how the young animal acquires the ability to understand the meaning of the display, performed by a conspecific. It requires the analysis of changes in reactions of the young animal to the different displays. One approach is the analysis of complex social interactions, but play-back experiments in the case of vocal displays and the use of (moving) models in the case of visual displays seem the obvious methods here. Apart from some preliminary findings, that are mentioned in Section IV, this aspect is not discussed in this article.
272
T. G . G . GROOTHUIS
5. The survival value of the different phases in the ontogeny of displays. This is still a somewhat neglected area of research. Too often, the young animal is considered only as an imperfect adult. However, natural selection will operate on each developmental stage and, consequently, young animals must show adaptation in their behavior to the specific needs of each developmental phase if they are to reach maturity and then reproduce. A functional interpretation of the causal mechanisms underlying the ontogeny of displays is given in Section V. Clearly, these five different aspects of the development of display do not necessarily involve independent mechanisms. The development of the final form of display (aspect 1) may be influenced by reactions to that display by peers, which in turn may depend on how young animals may interpret that display (aspect 4).A retardation in one aspect, for example, form development (aspect l), may influence the timing of other aspects, for example, that of form fixation (aspect 2). The likelihood of form fixation (aspect 2) may be greater in the proper species-specific form of display than in incomplete or deviating display (aspect 1). Form fixation (aspect 2) may involve a change in control of the motor pattern, and thereby a change in the context of the display (aspect 3). The application of the display in social interactions (aspect 3) may depend on how the young animal will perceive the display of its opponent during such interactions (aspects 4). Finally, the causal mechanisms of development (aspects 1 to 4) have arisen in evolution in relation to the functions which these mechanisms fulfill (aspect 5). Partly because of the scarce literature in this field, the emphasis in this article is laid on the display behavior of the black-headed gull (Larus ridibundus), but throughout the article these results will be embedded in other data from the literature. In Section VI, a summary and synthesis is given of the results of the analysis of the causal mechanisms underlying display behavior in this species. Development of displays and other motor patterns in other species is briefly discussed in relation with this (see also Groothuis, 1993a,b). The species-specific postures and vocalizations of the black-headed gull were chosen as a model for the study of the ontogeny of display behavior for the following reasons: 1 . The form and context of the adult display patterns are well described in the literature (Moynihan, 1955; Tinbergen, 1959; Manley, 1960; van Rhijn, 1981). 2. Qualitative observations suggest that display in this species develops gradually in form over a relatively long period (Moynihan, 1959). This raises the interesting possibility that extensive experience is necessary for
ONTOGENY OF SOCIAL DISPLAYS
273
the young bird to develop the normal adult display pattern. Furthermore, this long developmental period provides the ethologist with ample opportunity to manipulate this developmental process. 3. The species can easily be kept in captivity, where they successfully breed. Furthermore, young of this species can be raised by hand relatively easily (van Rhijn and Groothuis, 1985). 4. The species breeds in large colonies in the vicinity of our laboratory, facilitating observations under normal field conditions.
11. MECHANISMS OF FORM DEVELOPMENT
A. INTRODUCTION Before postulating and testing hypotheses on mechanisms of form development of display, the course of normal display development has first to be established. The obvious questions to be asked are, How early in ontogeny does the complete adult display emerge, and Is the expression of the complete display pattern preceded by the performance of display that is different from the adult pattern in one or more form elements? With regard to the last question, two types of contrasting results are present in the literature. Some authors have explicitly reported a gradual development of the motor patterns, while others have found that the complete display is more or less completely present early in ontogeny. As far as visual displays are concerned, a gradual development was reported for a threat display in black-headed gulls (Henty, 1966), for the displays of junglefowl (Kruijt, 1964), for some displays in two species of gulls (Moynihan, 1959), and for the display repertoire of cichlid fish (Williams, 1972; Wyman and Ward, 1973). For vocal display, a gradual development was reported for crowing in chickens (Andrew, 1969), for the calls of the sage grouse (Meinert, 1983), for the triumph call in four species of geese (Wurdinger, 1970), and for the calls of several species of grass finches (Zann, 1975). Platz (1974) found a gradual development in form in both the visual and vocal displays of a duck species. The early presence in ontogeny of more or less complete display is reported for the copulation posture in the domestic chick (Andrew, 1963, 1966), for the bobbing display in lizard species (Roggenbruck and Jenssen, 1986; Stamps, 1978), for strutting in turkey chicks (Schleidt, 1970; Schulman, 1970), and for crowing quail (Schleidt and Shalter, 1973). These two different types of results, even reported for the same species [by Andrew (1963, 1966, 1969) and Kruijt (1964) for the fowl], may be explained by the different methods applied in the above-mentioned studies. The
274
T. G . G. GROOTHUIS
less detailed the form analysis of the displays, the earlier a motor pattern will be considered to be completely present in ontogeny. Further, the chance to find precursors of adult display will be greater when the appropriate stimuli triggering the performance of display are offered early in ontogeny. The two contrasting types of results may also be due to different developmental processes. However, such a conclusion can only be based on the results of both descriptive and experimental studies. This discrepancy in the literature is therefore addressed at the end of Section 11, after a review of possible mechanisms underlying display development and experimental evidence for these.
B. FORMDEVELOPMENT OF DISPLAY I. Methods Two methodological issues that are relevant for the analysis of motor development are (a) when and under what conditions should the behavior of the young animals be observed, and (b) what kind of motor aspects should be measured. The latter is especially of importance because, in this area of research, we need clear form criteria for motor development that can be quantified, in particular in such cases as the development of complex behavior where we cannot apply electromyograms to register the activity of separate muscles. The two methodological issues that are dealt with briefly from the perspective of the analysis of gull display. a. Observations. In order to obtain an accurate inventory of the display patterns performed by young animals, the total range of (social) contexts in which the young may perform display behavior, including precursors of these patterns, should be taken into account. Therefore, some knowledge of the development of behavior in the natural field condition of the species under study is required. Observations in a large colony of territorial black-headed gulls in the course of the breeding season revealed that young of this species vigorously defend their territory, often less than 2 m2 in size, against intruders, including adult birds. To parents and siblings they mainly address begging behavior. Display-like motor patterns or their “precursors” appeared to be almost exclusively performed in these social interactions and during disturbances of the colony by a predator. Detailed registration of display development in the field was hampered by several practical problems, such as height of the vegetation, lack of the possibility to recognize individuals, and disturbance of the territorial structure around the hide. Recording of vocalizations was interfered with by too much background noise. Therefore, based on the information of these field observations, young birds were raised at the laboratory in two types of seminatural conditions: (a) by their own or foster parents in large
ONTOGENY OF SOCIAL DISPLAYS
275
aviaries, containing several breeding pairs; (b) by hand from the age of 1-5 days onward in aviaries containing at least 9 young of the same age. In the latter condition, chicks before the age of 7 days will form groups of 2 to 4 peers. The normal clutch size in this species is three and within peer-groups young interact as siblings do in the field. Furthermore, these peer-groups defend a particular spot in the cage against members of other groups. To compensate for the lack of interactions with adult conspecifics, these young were confronted with a stuffed or live adult black-headed gull at least once a week. These seminatural rearing conditions seemed to simulate most of the field conditions adequately, and control observations made in the latter were in close agreement with observations carried out in the former. Interactions between all different possible participants were video-taped and analyzed, often in slow motion or frame by frame. To anticipate the possibility that major behavioral reorganization would take place in the first weeks after hatching, video observations were started from the moment young chicks hatched and vocalizations were recorded even before hatching. b. CIassiJication of the Motor Patterns. Classification of gull display was based on data from the literature (Moynihan, 1955, 1959; Tinbergen, 1959; Manley, 1960; Henty, 1966; van Rhijn, 1981), on my own work on the displays of adult gulls, and on an initial scan of videotape recordings of display of young black-headed gulls of various age classes. On the basis of this information, the different display patterns were split up into as many varying form elements as possible, and their different positions in space were classified in young gulls of different age classes. As far as postural displays are concerned, the following elements were taken into account: (a) the position of the bill in the vertical plane, (b) closed or open bill, (c) the position of the neck in the vertical plane, (d) the degree of extension of the neck, (e) the position of the body in the vertical plane, (f) the position of the carpal joints and wings (ranging from held against the body to totally unfolded), (g) whether the bird was sitting or standing. For some postures, additional criteria were taken into account, such as the presence of a thickened neck, of raised feathers on the neck or back, of head movements, of tail spreading, the symmetry of wing positions, and the duration of the posture. An illustration of this approach is given for one display posture in Fig. 1. Form analysis of the vocaliations concerned the following: (a) the duration of separate notes, (b) the duration of intervals between notes, (c) the frequency spectra in hertz of notes, (d) the position of the different notes in a sequence. The combination of the different postures with different vocalization types was also taken into account. Except for the element duration, which was quantified in tenths of
276
T. G . G . GROOTHUIS
FIG. 1 . Form analysis of the complete adult choking display of a black-headed gull. (A) Bill position downward, (B)bill closed, (C) rapid head movements with a small amplitude, (D) carpal joints somewhat extended (score 2). (E) body axis tilted to the ground (angle minus 45”). (F) standing, (G) neck not extended.
seconds, the position of a particular element was scored in two to five mutually exclusive categories. These categories were designed to cover as much as possible the observed development in form of each particular display of this species and were therefore not always similar for each posture or each element. This method of classification, if open to verification by other investigators, is preferable to one that is based on arbitrary criteria designed without any knowledge of the motor pattern under study. The latter may seem objective, but may hide relevant information such as small but important variations in one element that do not occur in another element or in the same element of another display. Obviously, numerous combinations of the possible positions of the different elements showed up in the data. In order to arrange the results conveniently, the data were separately analyzed for four mutually exclusive categories, representing the four main display patterns in this gull species (see Fig. 2): 1. Choking-like postures, in which the neck is held at an angle of less than 45” above the horizontal, and in which the bill is held at an angle of at least 20” below the horizontal (Fig. 2C to G).The “choking” posture in adult black-headed gulls is depicted in Fig. 2G. In young birds it is almost always accompanied by a series of short soft-soundingnotes with short intervals, the “choking call.” This call is by far the commonest call during choking in adult birds. 2. Erect postures in which the neck is extended further than in the normal relaxed position and held at an angle of at least 45” above the horizontal (Fig. 2H to K). These postures share the typical characteristic of the erect adult “oblique” posture (Fig. 2K), the most frequently performed
FIG.2. Summary of the course of emergence in form of four species-specific displays in black-headed gulls in the course of ontogeny. (From Groothuis, 1989b. Reproduced with permission.)
278
T. G. G. GROOTHUIS
display in this species, in which the neck is mostly held oblique and the carpal joints are raised. The adult oblique is always accompanied by a series of loud harsh-sounding notes, the “long call.” Therefore, if erect postures in the young bird were accompanied by long-call-like vocalizations (see below), they were classified as oblique-like display. (The adult “upright” display, an erect posture that is performed without vocalization, often during sexual encounters, has been left out of the analysis due to lack of enough data from young birds.) 3. Pumping movements (Fig. 2M to P) in which the head is moved rapidly up and down, while in every downward movement one short note is uttered. 4. Forward-like postures (Fig. 2R to U) in which the head is held in front of the body, with the bill held horizontally or upwardly inclined. This category includes several types of the adult “forward” display (Fig. 2T and U) in which the neck is extended and the carpal joints are raised. The performance of this display is not associated with the performance of a particular type of vocalization. This type of form analysis was also used for other aims, for example, to describe deviating forms of display in adult gulls (see Section 11,C). Results and a First Conclusion In young black-headed gulls, the species-specific form of the adult display emerges gradually in the course of ontogeny. Evidence for this is discussed for two displays and their accompanying vocalizations: choking and the oblique (for more details, see Groothuis, 1989a).These two examples have been chosen because they illustrate different aspects of display development to which I repeatedly return in this article. a. The Choking Posture. The first element to appear in this display is the basic structure of the choking vocalization: bouts of short harshsounding notes with short intervals (see Section II,B,2,c for more details). Short bouts of these notes can already be heard from the egg. In the first 2 weeks after hatching, these bouts become increasingly long and exclusively linked to agonistic situations, in which the chick is threatened by an intruder and tries to hide away by crouching in a dark place. This vocalization becomes progressively linked with incomplete forms of the choking posture. In the first 2 weeks after hatching, the majority of these call bouts are performed in the normal relaxed posture with a horizontal bill, and less than 10% with the bill vertically down. In the course of ontogeny these percentages change in such a way that, in adult birds, all these call bouts are performed in a choking-like posture, with the bill pointing downward, mostly vertically downward (Fig. 3A). On the other 2.
279
ONTOGENY OF SOCIAL DISPLAYS
I
CHOKlNC POSTURE bill obliquedown
0 bill vertlcal down
80
-
CANDING
1001 TILTED BODY
620
0-2
3
349
124
202
4-6 10-12 ADULT age (weeks)
364
620
349
0-2
3
4-6
124
202
10-12 ADULT
age (weeks)
FIG.3. Percentage of choking-like postures in which a specific form element, typical for the complete adult posture, is present for five age classes of black-headed gulls. (After Groothuis, 1989b.)
hand, in all age classes, more than 90% of the choking-like postures are accompanied by choking-like vocalizations. Thus, the first element of the display that appears, the choking call, becomes gradually closely linked with the posture. The second element to appear, the typical bill position,
280
T. G. G. GROOTHUIS
is closely linked with the first element, the choking call, from the moment this posture emerges. In these postures with a bill down position and accompanied by chokinglike vocalizations, the presence of five other form elements, typical for the complete adult choking posture, were scored for different age classes. The presence of all of these five elements increases gradually with increasing age (Fig. 3). Thus, the choking posture gradually emerges in form in the course of ontogeny. This is qualitatively summarized in the upper part of Fig. 2. The display emerges from incomplete motor patterns, the first being no more than crouching when hiding in the vegetation upon the threat of an intruder in the territory. Then, by addition of, or change in, several different form elements the complete adult motor pattern emerges and with this the bird openly displays in front of the intruder. b. The Oblique Posture. The data on the oblique-like displays are based on the same type of analysis as applied for the choking display. If the main element of the posture, in this case an extended neck held at an angle of more than 45" above the horizontal was accompanied by a vocalization containing elements of the call typical for this display (in this case, longcall-like vocalizations; see below), the presence of other elements typical for the adult display was scored. While Fig. 3 properly illustrates the emergence of separate elements of a posture, it gives neither an impression of the sequence in which the diffferent transitional forms of display may succeed each other in the course of ontogeny, nor of changes in the duration of these postures. Therefore, the data for the oblique display are presented in a different way in Fig. 4. Clearly, and similarly to choking-like display, the oblique-like displays change in form in the course of ontogeny. Furthermore, the oblique posture seems to emerge gradually from incomplete choking postures. The first incomplete oblique postures, often performed during crouching as in incomplete choking (Fig. 2H), are still performed with the bill pointing downward (Figs. 21 and 4), an important element of choking too. The relative frequency of these postures decreases with age, and, via a transitional form with vertical neck and horizontal bill (probably the source for the development of another display, the upright), the normal adult display gradually emerges (Figs. 2K and 4). The duration of the postures increases with increasing age (Fig. 4). Together with the fact that the display is increasingly frequently performed with extended carpal joints, it gives the impression that the motor pattern becomes increasingly conspicuous in the course of ontogeny. c . The Choking Call and Long Call. Characteristic for the choking call is a sequence of short notes placed in a regular sequence with short
28 1
ONTOGENY OF SOCIAL DISPLAYS
relative freq Obl-like postures %
100
2
50
1
0
2
3
4-6
>9 aoe in weeks
60
255
234
149
I
n
FIG.4. Changes in form of oblique-like postures in the course of ontogeny of black-headed gulls. Shown are the relative frequencies (left y-axis) of three categories of combinations of different bill and neck positions, together with the duration of the display (right y-axis), for four age classes of young black-headed gulls. Bars with densest stippling: bill downward, neck oblique or vertical; bars with less stippling: bill horizontal, neck vertical; white bars: the normal adult form: neck oblique, bill horizontal or upward or neck vertical, bill upward. The depicted postures represent the most frequently performed form within the form category.
intervals. The long call consists of such a sequence of notes also, and the final parts of the long call in adult birds may be quite similar to the choking call. However, especially at the beginning of the bout, the notes of the former differ from those of the latter in that they are louder, longer lasting, and higher in pitch. Both these call types gradually change in form in the course of ontogeny. Furthermore, these changes support the interpretation that the oblique display emerges from the choking display. Quantitative evidence for this, based on the form criteria mentioned in Section II,b,l,b, can be found elsewhere (Groothuis, 1989b). The course of development of these calls is qualitatively depicted in Fig. 5 . The early-appearing harsh-sounding notes that can already be heard from the egg become more harsh and embedded in the typical sequential structure with short note intervals (Fig. SA-C). From this point on, two developmental pathways can be found: first, toward the adult choking call. Here a gradual change in pitch and duration of the call takes place (Fig. SD),resulting in the call sounding more muffled. This is probably caused by the fact that the bird is now performing the
i"?yPi time (sec)
I
1
1
I
ONTOGENY OF SOCIAL DISPLAYS
283
choking display with closed bill. Second, a change toward the adult long call. This starts at about 3 weeks of age with the insertion of some highpitched notes with a slightly longer duration between the precursors of the choking call (Fig. 5E).Although the essential structure of the call does not change thereafter, changes in the overall tonal quality still take place. In the course of the third month after hatching, the calls sound much clearer and higher in pitch (Fig. 5F), whereas in early spring at the age of 10 months the calls sound extremely hoarse (Fig. 5G). Finally, about 2 months later, the calls are indistinguishable from the normal adult call (Fig. 5H). d . Conclusion. Both the species-specific display postures and accompanying calls emerge gradually in the course of ontogeny. The ontogenetic sequence of changes in forward-like postures and in the pumping movement, the begging display of young birds, which have not been discussed so far, are also depicted in Fig. 1. Based on data concerning the form, the sequence, and the accompanying vocalizations of the different motor patterns, it could be shown that the development of pumping concerns the integration of the alert (in which the chick scans the surroundings with an extended vertical neck when there are disturbances in the environment) and the forward-like postures. Ontogenetic changes in the latter are therefore also reflected by ontogenetic changes in the pumping movement, which thereby becomes an increasingly conspicuous begging display. The course of changes in form of the motor patterns consists of changes in the spatial position of separate elements and the addition of new form elements. Combinations of a specific call and a specific posture become gradually more clear. Furthermore, a display may emerge from building blocks of another display or by an integration of two different motor patterns which have emerged independently at an earlier stage. By these changes, the motor patterns gradually change in form toward a more pronounced display. Finally, in the course of development, transitional forms of display follow each other in a more or less fixed sequence. e . Final Remarks. i. Frequency changes and regression. All four display types gradually increase in frequency in the course of the first 4 weeks
FIG.5. Sonagrams representing the course of emergence of the choking call (A to D) and the long call (A, B, C, E to H) in the black-headed gull. (A) Harsh call day I after hatching, showing irregular note intervals; (B) harsh call day 5, showing the typical regular note intervals of short duration and less well defined frequency spectra; (C) harsh call day 19 in which tonal quality is almost totally absent; (D) typical stifled rhythmic choking call, performed with the bill closed, day 26; (E) long-call-like vocalization, day 30, with high-pitched notes of a slightly longer duration in the beginning of a harsh call bout; (F) long-call-like vocalization week 10, with well-defined frequency spectra; (G) hoarse long call in first spring, similar in frequency spectra with early harsh calls; (H)adult long call.
284
T. G. G. GROOTHUIS
after hatching. Interestingly, the expression of a more complete display in a certain individual during a certain developmental stage often took place in concordance with a higher frequency of performance of that display by that individual. On the other hand, the frequency of performance of certain transitional forms of display decreases considerably with, increasing age of the bird. Moreover, the complete pumping display disappears altogether from the repertoire of older birds (although the incomplete pattern returns in a slightly different form more than a year later in the male’s repertoire as a precopulation display). This leads to the question of whether the neural mechanisms for some displays become reorganized. This seems not to be the case. For example, a gull raised in abnormal social conditions (see below) started to reperform complete pumping frequently when adult. Further, adult birds, when heavily attacked by other birds in a situation where they cannot escape (for example in a small cage and with their wings clipped), reperform crouching in the form typical of young chicks. Thus, the neural coordination mechanisms for juvenile display still seem to be present in adult birds. This is reminiscent of the finding of Bekoff and Kauer (1982) that the neural circuitry for the hatching movement of chicks is still present after hatching. The inhibition of motor patterns that were expressed at an earlier stage of development draws attention to the fact that ontogeny of behavior includes not only progression but also regression. This, of course, must be related to the function the motor patterns fulfill at each particular stage of ontogeny (see Section V). ii. Discontinuities. To some extent, emphasis has been laid on the finding that displays gradually change in form in the course of ontogeny. However, the data presented so far are mean scores of groups of birds and differences were found between individuals in the time span in which the different transitional forms of display were performed. Furthermore, individual birds could suddenly come up with the next transitional display, which then became the main display type for some time, although they had hardly performed this motor pattern before. Thus, a young bird may suddenly jump from one developmental stage to another. Such discontinuities may mark important stages in development and should be analyzed in more detail (see also Plooy [1980] and Plooy and Van de Rijt-Plooy [1989] for the development of behavior in chimpanzees and humans). iii. Integration and Differentiation. In the first half of this century, two contrasting views on motor development were prevalent. One was the idea that, in the course of ontogeny, separate motor units become integrated in larger functional units (Kortlandt, 1940). The other was that the subunits, such as limb coordination, gradually differentiate from an early movement
ONTOGENY OF SOCIAL DISPLAYS
285
pattern that involves the whole body of the animal (Coghill, 1929). However, several authors are now of the opinion that both processes take place in ontogeny (e.g., Plooy, 1980; Fentress and Mcleod, 1987), and this is clearly the case for the development of displays after hatching in the blackheaded gull. For example, in the course of development of the choking display, different motor units, such as extended carpaljoints, a tilted body, and movements of the head, gradually “differentiate” as separate motor units that can be performed together or apart from the other units. Furthermore, the oblique display, both the posture and the long call, seems to differentiate from the choking display, and later in ontogeny,both displays are performed in slightly different contexts (Moynihan, 1955). Integration of two different motor units, the alert and forward-like displays, takes place in the development of the pumping display. However, whether a description of motor development in these two ways really refers to causal processes underlying the development of neural circuitry needs further study. iu. Onrogeny and phylogeny. Displays are thought to have evolved in the course of evolution from intention movements, for example, for locomotion, aggression or escape behavior (e.g., Tinbergen, 1952; Baerends, 1975). Because more conspicuous forms of these intention movements could function as important tools for intraspecific communication, these movements gradually evolved by natural selection to the present conspicuous displays. This process is called ritualization (Daanje, 1951;Tinbergen, 1952;Morris, 1957;Hinde, 1969).Because species recognition is strongly adaptive, closely related species developed different displays, although often with common basic features because of their common ancestor. The gradual development in form of displays in the course of ontogeny in the black-headed gull shows striking similarities with the changes in form that are postulated to have occurred in evolution. As discussed earlier, the display patterns in young gulls become increasingly conspicuous. Furthermore, young gulls frequently perform incomplete display in alternation with intention movements of aggression and escape (Groothuis, 1989~).Moreover, several incomplete or transitional forms of display in young black-headed gulls show great resemblance to adult display of related gull species (Groothuis, 1989~).It is often found in developmental biology that ontogeny “recapitulates” phylogeny. The reason for this is the fact that evolution takes place by modifying already existing mechanisms in the course of the life of an organism. Therefore, phylogeny is modified ontogeny (de Beer, 1940). From this perspective, the data on the ontogeny of social displays presented so far seem to support current ideas about the evolution of these motor patterns.
286
c.
T. G. G. GROOTHUIS
POSSIBLE MECHANISMS OF DISPLAY DEVELOPMENT
In this section, four not mutually exclusive hypotheses are discussed to explain the data presented in Section I1,B. In the next Section (II,D), I discuss experiments aimed at testing these mechanisms. The first three hypotheses have in common that the neural coordination for the complete display is present early in ontogeny. The gradual emergence of the complete display may than be explained by assuming that the expression of the circuitry changes gradually, depending on other factors: 1 . A change in the motor apparatus, such as growth of muscles or efferent neural connections. This is often called maturation, and might explain changes in motor patterns early in life, such as those reported in the development of bill pecking in gulls (Hailman, 1967) or of head-bobbing in lizards (Roggenbruck and Jenssen, 1986). 2. A change in external stimuli. A young animal may have most of its interactions with young of approximately the same,age, and only later in ontogeny with larger adult conspecifics. The latter may provide stronger external stimuli than the former and therefore may trigger the motor pattern more completely. 3. A change in internal stimuli, such as the development of the proper motivational state for aggressive behavior, which triggers the complete display. In his classical study on the ontogeny of social behavior in junglefowl, Kruijt (1964) explained the development of displays in this way by postulating a development of different motivational systems and changes in the relationship among these systems. However, alternatively, the neural coordination mechanisms themselves may not be complete at first and their development may also explain the gradual emergence of the adult displays. Which factors may influence this development? 4. One plausible hypothesis is that the young animal may shape its display on the basis of proprioceptive feedback, resulting from the performance of incomplete display. This kind of feedback may than be matched against some sort of neural template, in which the information about the species-specific form of display is encoded. This mechanism, discussed by Baerends van Roon and Baerends (1979), is similar to that proposed for the development of song in songbirds, although in the case of display postures proprioceptive feedback will be involved while in the case of song development the feedback is auditory. If this hypothesis is correct, the next question to be answered is how the template itself may develop. Two types of external influences could be relevant for this: 4A. The young animal may acquire the information in the template by
ONTOGENY OF SOCIAL DISPLAYS
287
observing display of conspecifics and copying that form of display through imitation. This is clearly the case in song development in several species of songbirds. However, in song development, the song of the tutor (auditory input) is compared with the bird’s own song output (again using auditory input), and therefore only one sensory mode is involved. This is not the case in imitation of postures or movements. In the many cases when an animal cannot see its own performance, visual input (seeing the motor pattern of the tutor) must be compared with proprioceptive feedback. Complex as this seems, we cannot exclude such a complex cognitive mechanism out of hand and there is some evidence that young human babies already have the capacity to imitate facial expressions (Meltzoff and Moore, 1977; Field et al., 1982). Whether in this case the young baby is really shaping its motor output into a new form on the basis of visual input, or whether it is just triggering already existing motor patterns in response to this visual information remains, however, to be seen. 4B. The young animal may also acquire information about the proper from of display on the basis of social reactions of conspecifics to the different forms of display it shows in interactions with them. If conspecifics are able to differentiate between incomplete and complete display, they may react consistently differently to these forms. If reactions to the property complete display are more reinforcing than reactions to incomplete display, the performer may shape this display by operant conditioning. A prerequisite for this is that subtle differences in the form of display are recognized and carry meaningful information for conspecifics. This has been shown to be the case for several gull species (Beer, 1980; Veen, 1980; Groothuis, 1989b, 1992). That the reactions of a conspecific to the display performed may influence the development in form of that display has been shown to be the case for song development in the cowbird (West and King, 1988). These four hypothesis are not mutually exclusive. Maturation of motor systems has been shown to be dependent on the activity of these motor systems (Drachman and Sokoloff, 1968; for reviews, see Oppenheim. 1981, and Prechtl, 1984). Therefore, the presence of the proper motivational state (hypothesis 3) may stimulate the performance of display, which in turn may stimulate maturation (hypothesis 1). (In fact, the term maturation is so strongly associated with autonomous growth of tissue that this term has become obsolete and the application of it should be avoided.) The proper motivational state may also increase the frequency with which the animal matches its display against the template (hypothesis 4), and stimulate the young to initiate social interactions. These then create the proper situation for the animal to imitate the display of the opponent (4A),
288
T. G. G. GROOTHUIS
or to shape its display on the basis of reactions of conspecifics to its own behavior (4B).Furthermore, as a “safeguard,” more than one mechanism may guide the display to its normal adult form. Therefore, in revealing the mechanisms of display development, confirming one hypothesis does not necessarily make testing of the other hypothesis redundant. D. TESTING THE HYPOTHESES 1 . Limitations in the Motor Side
This hypothesis predicts that limitations in the peripheral motor apparatus explain the occurrence of incomplete display postures in the blackheaded gull. However, even I-week-old chicks are capable of performing many motor elements of the complete adult display postures. This can be deduced from two findings. First, many elements of the complete display can be observed in the young chick in various contexts long before they become incorporated in the display. For example, raised carpal joints are shown early in ontogeny during running; the proper bill and neck position for the adult oblique can be seen in chicks during begging, when they peck to the parent’s bill for food. The closed bill and standing instead of crouching, two elements of complete choking, occur very early in ontogeny, long before the emergence of the complete display. Second, complete oblique display has been observed in young gull chicks, although only briefly and rarely. Although the performance of all the proper form elements in the correct combination may be attributed to a coincidence and not to the result of central coordination, all motor elements did appear. Therefore the first hypothesis should be rejected. However, limitations on the motor side of the machinery may be relevant to explain display development very early in ontogeny and may be more pronounced in altricial species than in a species like the black-headed gull. Maturation may explain the development of some,characteristics of the vocalizations. The increase in note duration may be caused by an increase in the volume of the air sacs of the bird. Changes in pitch may be caused by growth of the membranes of the syrinx, the birds’ primary vocal organ. Evidence for the latter follows from the finding that young gulls that has been treated with testosterone performed calls with adult characteristics, while autopsy showed an enlargement of some parts of the syrinx (Groothuis, 1992).
2 . External Stimuli The second hypothesis postulates that the increase in the completeness of display in the course of ontogeny is caused by an increase in strength
ONTOGENY OF SOCIAL DISPLAYS
289
of external stimuli to which the young are exposed. This hypothesis was tested by rearing young chicks by hand and confronting them weekly with the same strong external stimulus: a stuffed adult black-headed gull in breeding plumage and in the oblique posture. The model was mounted at the top of a long stick and was maneuvered in such a way that attack movements of adult intruders on the territory in the field were simulted. This provided the proper context for the agonistic displays. The experimental birds showed essentially the same gradual emergence of complete display as control birds, although display postures with raised carpal joints were slightly more often performed than in agonistic interactions with young of the same age. These results showed that the second hypothesis is unlikely as far as the black-headed gull is concerned. However, in other species, the role of external stimuli in triggering display early in ontogeny is important, such as in the cichlid fish Aequidens rivularus (Groothuis and Ros, in preparation). In this species, the young gather in large schools during the first months of their life and show a gradual increase in frequency of different displays. Fish that are younger than 6 weeks hardly ever show agonistic display and never show sexual displays. However, in confrontations between young of 6 weeks of age, display frequency increased strongly if the participants had been isolated for 2 days before the tests. This suggests that, in a school, young cichlid fish habituate to each other and, consequently, their companions are less effective for triggering display behavior. This is obviously functional, because premature agonistic interactions will disrupt schooling behavior, which is important for reducing the risk of predation. When the stimulus fish was treated with sex hormones, which induced premature appearance of the adult color patterns, the isolated but hormonally untreated opponent even showed sexual displays in confrontations with this stimulus fish. Similar effects of short-lasting social isolation on the increase of display in confrontations with other young early in ontogeny have been reported by Kruijt (1964) for junglefowl. In this species, adultlike although shortlasting crowing postures have been observed in chicks of I week old, reared in social isolation, during confrontation with an imprinting stimulus (a small blue ball) (T. Groothuis, unpublished observation). These examples show that certain uncommon external stimuli can provoke relatively high frequencies of adultlike display in young animals of several species. Unfortunately, the forms of these premature displays have not been analyzed in detail. 3. Development of Motivational States The gradual emergence of a complete display may be attributed to the fact that the motivational systems controlling that display develop
290
T. G. G. GROOTHUIS
gradually or become increasingly activated. In this case (as in the previous case, 2), one would expect the emergence of display to be the result of a decrease in the threshold for the different motor elements to appear, and not the result of increasing coordination between these elements. Indeed, in the black-headed gull, evidence for such an increased coordination is lacking. In each age class, even in chicks, many elements characteristic for a particular adult display occur more often in combination with another element of that display than could be expected if these elements occurred independently from each other (Groothuis, 1989b). Thus, the change in form of the displays does not consist of a development from random combinations of form elements to well-coordinated motor patterns. This conclusion is in accordance with the finding that display in young gulls is not necessarily less stereotyped than display in adults. On the contrary, the course of changes in display consists of a more or less fixed sequence of transitional forms of display, as is shown in Figs. 2 and 4. This course of changes can be adequately described as a change to the performance of more pronounced display or, in other words, from a low-intensity display to a strongly motivated display. The influence of the development of motivational states can be tested by manipulation of these states that control display in the young animal. If the hypothesis is correct, precocious strong activation of the relevant motivational system should induce precocious complete adult display. In order to carry out such an experiment, determination of the motivational background of display in the young animal is necessary. To this end, an ethological black-box analysis of the motivational systems underlying the occurrence in frequency and form of the four displays depicted in Fig. 2 has been undertaken (Groothuis, 1989~).In this analysis, it is assumed that: (a) if external stimuli are held constant, changes in behavior are due to changes in the internal factors controlling that behavior; (b) that motor patterns showing similarities with each other in form, frequency changes, temporal sequences, and context of occurrence share an internal common causal factor. A stuffed adult black-headed gull was used as the standard external stimulus in this study. It was placed at least weekly in the territories of the chicks, inducing a lot of agonistic behavior. Display behavior, as well as other motor patterns such as overt aggression, overt escape, feeding, and locomotion, were compared with each other. This analysis resulted in the following conclusions: Early in ontogeny both choking-like and forward-like display are primarily under the influence of two subsystems that control fear behavior. These are, respectively, a system controlling a tendency to hide or to stay put and that controlling a tendency to escape. The pumping display is influenced by a state of alertness, induced by hunger. The changes in form of the forward- and
ONTOGENY OF SOCIAL DISPLAYS
29 1
choking-like displays, and the emergence of the oblique from the latter display are due to the influence of a motivational system for aggression. This system becomes increasingly activated, simultaneously with the activation of the other motivational systems. If this interpretation is correct, manipulation of the internal variables controlling aggressive behavior should result in a change in the gradual emergence of complete display. In many animal species, including birds, aggressive behavior and agonistic display in adults are known to be under the influence of sex hormones. Interestingly, in gull species in which the sexes are monomorphic both in plumage and in display behavior, both the male and the female have been shown to be sensitive to the male hormone testosterone (laughing gull; Terkel et al., 1976). Furthermore, both sexes show comparable blood levels of testosterone during a considerable part of the breeding period (Western gull; Wingfield et al., 1982). Moreover, juvenile black-headed gulls of both sexes show an increase in blood levels of testosterone from less than 0.1 to 0.5 ng/ml during the period when they persistently show complete display for the first time in their life (Groothuis and Meeuwissen, 1992). These data justify further analysis of the effect of testosterone on display development in young black-headed gulls. Young black-headed gulls were treated with testosterone at a stage of ontogeny before the emergence of complete display. If the neural coordination mechanisms for the complete display are indeed present early in ontogeny, and if their expression can be activated by testosterone, two kinds of results are to be expected: (a) the complete adult display will be expressed early in ontogeny; (b) birds will be able to skip the performance of incomplete display in developing the complete motor pattern. The second finding would imply that incomplete display patterns are not necessary precursors that fulfill a function in the development of the form of complete display. In contrast, incomplete motor patterns can then be taken as merely epiphenomena of a gradually increasing motivational state for agonistic behavior. This would imply that a mechanism by which the bird matches the actual motor output against a template, in order to develop the complete display (the fourth hypothesis), is not a necessary part of the developmental process of display patterns. To overcome possible confounding influences of limitations in the motor apparatus and in the metabolism of testosterone, the first experiment was carried out with gulls that were already 10 weeks of age (Groothuis and Meeuwissen, 1992). At this age, normally reared gulls are able to perform the complete displays. To prevent the experimental animals from gaining experience with the performance of incomplete display before hormonal treatment, all birds, including the controls that were not hormonally treated, were reared in social deprivation (in isolation or in very small
292
T. G. G. GROOTHUIS
groups). The complete lack of the performance of incomplete display before hormonal treatment, due to the lack of adequate social stimulation, was confirmed by observations. Hormonal treatment consisted of subcutaneous implantation of one or two 25-mg pellets of testosterone propionate which released hormone for at least 3 weeks. After hormonal treatment, both aggression and the oblique-,,forward-, and choking-like displays increased rapidly in frequency; the pumping display did not show such an increase. This confirmed the interpretation of the results of the motivation analysis discussed above: the first three are agonistic and the pumping display is part of nonagonistic behavior. The three agonistic displays also showed a strong acceleration in form development. Some of the data on the oblique display are summarized in Fig. 6. The young birds reached adult percentages of complete oblique postures within 5 days after implantation, which is significantly shorter than in normal development. Moreover, in some birds, during numerous observations, incomplete display was hardly observed or not at all. These individuals showed high percentages of complete oblique postures from the first day after implantation onward (Fig. 7). This indicates that young black-headed gulls do not need to practice their motor output in order to develop complete display.
1001 Mcomplete oblique O O ’
c
0 1 2 3 4 5 days after implantation FIG.6. Frequency and form of oblique-like display in approximately 10-week-old naive young black-headed gulls over the course of 1 I days after testosterone implantation in 14 experimental and 7 control birds. Day 0 is the day of implantation. (A) Total frequency and (B) average percentages for 14 birds of oblique-like postures that consisted of complete adult display. Bars are standard errors. (Modified after Groothuis and Meeuwissen, 1992.)
293
ONTOGENY OF SOCIAL DISPLAYS
40 20 N=O
7
18
0
1
2
21
3
34
0
0
3
10
4
24
3 4 5 0 1 2 3 4 5 days after implantation FIG.7. Percentage of oblique-like display that consisted of complete adult oblique postures in two young naive black-headed gulls (A and B) after implantation of testosterone at the age of 10 weeks (day 0). (Modified after Groothuis and Meeuwissen, 1992.)
This result raises the question of how early in ontogeny the neural coordination mechanism for the adult display may be present. The answer is provided by the results of an experiment in which young black-headed gull chicks were treated with testosterone at day 5 after hatching. Essentially the same results were obtained as with the older gulls in the previous experiment. The hormonally treated chicks performed conspicuous longlasting complete oblique, choking, and forward display (Fig. 8), together with overt aggressive pecking. Some chicks showed complete display in percentages characteristic for adults from the very first day after hormonal treatment onward (Fig. 9). In both experiments, the time period during which the long call emerged was also shortened. After 2 weeks of hormonal treatment in the first experiment, the juvenile gulls produced calls which were indistinguishable from the hoarse calls normally produced at the age of 10 months (Fig. 5G). Some of these individuals eventually produced adult calls before the age of 5 months. Moreover, some of the young chicks in the second experiment even performed long calls with characteristics of the high-pitched long calls (Fig. 5F) or hoarse long calls (Fig. 5G),typical for much older birds.
FIG.8. Depiction of complete choking (A), oblique (B),and forward display ( C )in blackheaded gull chicks treated with testosterone on day 5 after hatching. (Modified after Groothuis and Meeuwissen, 1992.)
294
T. G . G. GROOTHUIS
A with head movements
a complete choking
4 5 11/12 0 1 2 3 4 5 11/12 days after implantation FIG.9. Percentage of choking-like display that was performed with head movements, or that consisted of complete choking, in two black-headed gull chicks after implantation of testosterone at the age of 5 days (day 0). (Modified after Groothuis and Meeuwissen, 1992.)
0
1
2
3
Autopsy of some of these birds and of controls revealed that testosterone treatment had modified some parts of the syrinx, the main vocal organ in birds. This indicates that testosterone influences the development of the vocal displays partly by peripheral effects. The chick calls, however, never acquired the duration of the adult calls, supporting the suggestion given earlier that the size of the bird, and especially of its air sacs, may be the limiting factor for note duration. The data presented so far support the hypothesis that complete display is present early in ontogeny. However, it must be stressed that, although the effect of hormonal treatment is spectacular, in many of the experimental birds, especially in the chick group, a gradual change in form and frequency of display could still be noticed, although in an unusually short time period. This opens the possibiltiy that, although practicing motor output according to the matching hypothesis is not indispensable, for at least some individuals, such a,supplementary mechanism may still be of some importance. Alternatively, gradual emergence of complete display in testosterone-treated birds may be due to the fact that biochemical processes, by which the hormone modifies behavior, need time to become effective. These biochemical processes include conversion of testosterone to active metabolites, development of receptor systems, and modification of DNA transcription and protein synthesis. To test the two possibilities, one could either treat chicks still in the egg with testosterone or test the matching hypothesis more directly. The first experiment may give the biochemical processes time to become effective, while the embryo, because it is still in the egg, is prevented from practicing display behavior.
ONTOGENY OF SOCIAL DISPLAYS
295
These experiments are currently being carried out in Haren. The second experiment has already been carried out and is discussed in the following section. It should be stressed here again (see earlier in this section) that, in the black-headed gull, testosterone appears to influence form and frequency of agonistic behavior in both the male and the female, in contrast with many other animal species. This may be related to the fact that gull species are monomorphic both in plumage and behavior: both sexes perform the same displays, except for precopulation begging in which the male performs vertical head bobbing and the female bill tossing. Furthermore, in homosexual pairs of males, I have seen males performing bill tossing and adopting the female copulation posture, and I have seen a female gull performing the male copulation posture. Moreover, in gull species in spring both sexes develop the breeding plumage, while in most other bird species this only occurs in the male. In males of many animal species this breeding plumage and display behavior are under the control of androgens. Although behavioral effects of testosterone in males may be mediated by aromatization to estrogen and conversion to dihydrotestosterone (DHT) in the brain, the breeding plumage, like other peripheral effects of sex hormones, has been shown to be under the control of androgens. The fact that female gulls need testosterone to develop the breeding plumage, and perform the same displays as males, displays which are normally under the control of testosterone in the male sex, makes the sensitivty of female gulls to the male sex hormone testosterone understandable. In this section, the effect of testosterone on the expression of complete display has been interpreted as due to hormonal effects on a behavioral system for agonistic behavior. Although testosterone affected the development of the calls partly via effects on the syrinx, such peripheral effects do not seem the proper explanation for the hormonal effects on the expression of the display postures. As was concluded earlier in this section, the neural mechanisms for the complete adult display postures are present very early in ontogeny, and need only to be activated by the proper internal stimuli. Therefore, an explanation of the effects of testosterone in terms of sensory motor development does not seem appropriate. Furthermore, testosterone not only activated the complete displays, but also overt aggressive behavior. Moreover, the hormone changed the temporal sequences of the behavior patterns (such as the oblique forward sequence) and the context of the displays in relation to external stimuli and locomotion (T. Groothuis, unpublished data). This leads to the interpretation that testosterone not only lowers the threshold for the displays to occur, but also influences a behavior system coordinating agonistic behavior. (For a further discussion of motivational factors influencing display development,
296
T. G. G. GROOTHUIS
and age-related effects of testosterone on motivational effects, see Groothuis, in preparation). 4 . Matching of the Motor Output
To establish the influence of feedback gained from the performance of motor output, by which a young animal may match its display against a template, the feedback itself should preferably be manipulated. In contrast to the case of song development, where one can easily manipulate the relevant feedback by deafening the bird, this is not readily possible in the case of development of postures, where proprioceptive feedback is involved. There are, however, two other ways to test the hypothesis: (a) One may prevent the young animal from practicing relevant motor patterns for a certain period, after which a possible retardation in motor development could be tested; (b) one may manipulate the information present in the template itself, If this template encodes information which is gained by observing display postures of conspecifics, one could provide the young animal with deviating models. If the relevant information is gained by reactions of conspecifics to the display performed, one could expose the bird to abnormal reactions or try to induce deviating display by operant conditioning. These three experiments (testing the influences of practice, imitation, and social reactions) have been carried out with the black-headed gull (Groothuis, 1989b, 1992; Groothuis and van Mulekom, 1991) and are discussed in this sequence below. a . Influence of Practice. Young birds almost exclusively perform display during social interactions. To prevent young gulls from practicing display postures, chicks were reared either in social isolation, or in small groups of 2 to 4 individuals. In the latter situation, chicks treat each other as siblings, and hardly ever interact aggressively. Display development in these birds was tested either at the age of 15 weeks (when normally reared birds have completed display development) or at the age of 10 to 12 months. All birds tested at the age of 15 weeks showed a retardation in display development, showing a mean incidence of oblique postures with the adult bill and neck position of 60% only, against 85% in control birds. The incidence of oblique display with raised carpal joints was 13%, against 80% in the controls. Birds tested at the age of 10 to 12 months showed high interindividual variation in display development (Table I). Forty percent of the birds raised in visual isolation from other birds and 55% of the birds reared in small groups without adult birds showed consistently normal complete display. Thus, imitation is not indispensible for the development of the proper species-specific adult display. However, many of the other birds
ONTOGENY OF SOCIAL DISPLAYS
297
TABLE I
OBLIQUE DISPLAY AND RAISING CONDITION Display
Control
0
Isolated
Small group
35 25
None Fragmentary Deviating Normal
0 0 100
40
0 20 25 55
N=
18
20
20
0
showed no display at all or fragmentary display (deviating display is discussed later). The latter contained characteristics of the incomplete display of much younger birds. Thus, social deprivation may cause a retardation in display development. The retardation in display development occurring in both age classes may be interpreted as support for the idea that birds need to practice the motor patterns in a social context in order to develop normal display. However, indirect evidence opens a more plausible alternative explanation. In the birds raised in social deprivation, the development of the black plumage on the head also appeared to be retarded as compared with the mask of birds reared in large groups. The development of the mask occurs in this gull species every spring and is regulated by testosterone (Groothuis, 1992). Furthermore, the stage of development of the mask in spring in birds housed in large groups is positively correlated with blood levels of testosterone, as measured by radioimmunoassays (R = .78, n = 6, p <.05). The results therefore indicate that social deprivation may cause a retardation in the production of testosterone, which in turn leads to a retardation of display development. This is in line with the results discussed earlier in which the relationship between testosterone and display development was established by means of implantation experiments. Some of the birds, reared in conditions of social deprivation and showing the retardation in display and mask development, were housed in small groups of 2 to 4 birds. In these groups, social interactions clearly took place, but aggressive interactions were almost completely lacking. This indicates that especially aggressive interactions stimulatetestosterone production and thereby the expression of complete display. In the field, chicks defend their territory in the colony vigorously and so experience many aggressive interactions. Such early aggressive interactions, also occurring in normally reared young in the laboratory, may stimulate the production of testosterone and thus it may explain the gradual increase in testosterone production and thereby the gradual increase in complete display in normal
298
T. G. G. GROOTHUIS
ontogeny. The idea that social interactions may stimulate hormone production is supported by results of studies on adult social behavior (e.g., Cheng, 1979; Wingfield, 1984). b. Imitation. The conclusion that imitation is not indispensable for normal display development has already been presented above. This conclusion was based on experiments in which the possibility of imitation was excluded by rearing young in visual isolation from other birds. However, these experiments are not considered to be conclusive. First, the birds were not acoustically isolated from each other, which may have guided vocal development. Due to the intimate connection between posture and call type, it is conceivable that hearing one another may have guided development of the posture too. For example, the production of the long call may need the performance of certain elements of the oblique posture. Second, although in the absence of models development of complete postures may take place, imitation may still influence this development when models to copy are present. To test this, I offered young birds deviating models, provided by the displays of two related species: the common gull (Larus canus) and the little gull (Larus minutus). In the common gull choking is more or less similar to that of the black-headed gull, whereas in the little gull choking is almost entirely lacking. Both species do not perform the complete adult forward display of the blackheaded gull: the common gull performs incomplete postures only, and in the repertoire of the little gull the display is replaced by a posture with vertical neck and vertical bill. The oblique display of the common gull differs from the posture in the black-headed gull in that it starts with the head held down, as in choking, and often ends with bill tossing. The oblique display in the little gull is more or less similar to that of the blackheaded gull. The vocalizations differ strongly between all of these species (for a description of the displays of the common gull and the little gull see, respectively, Weidmann, 1955, and Moynihan, 1955). Because social interactions are known to enhance learning processes, as reported for song learning by Baptista and Petrinovich (1984) and for sexual imprinting by ten Cate (1984), black-head gull chicks were reared in a situation in which they could freely interact with their tutors. Thus, chicks were reared individually with either chicks of common gulls or little gulls, or by foster parents of these species. After the age of 10 months none of the black-headed gulls had copied elements of display postures or vocalizations of one of the other gull species into its own repertoire. However, some gulls did show abnormal postures and/or calls. This may suggest that, although birds do not imitate models that deviate from the species-specific displays of their own species, the absence of proper models of their own species to copy may lead to failure in display development. However, birds reared in visual isolation,
ONTOCENY OF SOCIAL DISPLAYS
299
and therefore also lacking these proper models, did not develop abnormal display. These abnormal displays may therefore be attributed to the abnormal social interactions that took place in these small groups and are discussed below. So far, we have not found any evidence for imitation of postural or vocal displays in the black-headed gull (but see Groothuis, 1993b, for more recent and positive evidence). c. Social Reactions. The last point to discuss in this section is the influence of social reactions on display development. This possibility was tested by raising young gulls in a context that was likely to create abnormal social interactions. To this end, chicks were raised in abnormally small groups of two to four individuals. In such groups, a clear social rank order appears after a couple of months, which is normally lacking in large groups of gulls. Table I shows that in these small groups abnormal oblique display developed. Display was considered abnormal if it consisted of a pronounced long-lasting posture or call (to distinguish it from incomplete display) in which one or more form elements deviated from the normal species-specific adult display in a stereotyped fashion. Furthermore, two of the four birds reared with another species in a small group developed abnormal obliques too. Apart from the oblique, deviations also appeared in displays other than the oblique, and also in vocalizations or abnormal combinations of posture and vocalization (for a quantitative description, see Groothuis, 1992). None of the deviations appeared in a similar form in more than one bird of the same group, again a result that argues against imitation. Three examples of deviating oblique display are presented in Fig. 10. In the deviating postures and in one of the abnormal calls, the deviating elements show similarities with the incomplete display of younger birds. As has been described earlier (Fig. 4), the typical oblique postures of young birds are executed either with the bill pointing downward (Fig. 2H, I) or with the neck held vertically and the bill in the horizontal position (Fig. 25). Long calls typical for young birds consist of choking-like vocalizations with short notes and short intervals (Fig. 5C, E). Both juvenile postures (Fig. 10A and B) and a choking-like long call (Fig. 1Oc) occurred in the small groups. This suggests that, in these cases, the emergence of the display was prematurely arrested. The most likely explanation so far is that, due to the familiarity of the birds within such small groups, no pressure was present to perform the most complete and pronounced form of display in order to communicate effectively with the companions. Given the clear social rank order in these groups, birds may retreat from the dominant one even when it performs incomplete display only. Such incomplete display may then become more pronounced and fixed in form (see also Section 111).
300
T. G . G . GROOTHUIS
FIG. 10. Three examples of abnormal oblique display (posture and sonagram of the accompanying longcall) in three black-headed gulls raised in very small groups. (A) Abnormal posture (the bill was pointing downward in 81% of the oblique displays of this particular individual, against 1.5% in the oblique of control birds) accompanied by a normal long call. (B)Abnormal posture (upright-like display with vertical neck and horizontal bill that was adopted in 78% of the oblique displays performed by this bird against 3.6% in controls) with abnormal long call (containing elements that show strong similarity with the mew call, typical for males calling their partner in a posture completely different from the oblique). (C) Normal oblique posture that was always accompanied by an abnormal long call, showing very short note durations (0.25 sec against 0.78 in control birds).
Although the data on the black-headed gull are, to my knowledge, the only well-documented quantitative description of deviating displays in the literature, anecdotal reports of deviating display in other species, such as in ducks (de Lannoy, 1967) and monkeys (Hanssen, cited in Fentress and McLeod, 1987), have been given. Further, I found abnormal display
ONTOGENY OF SOCIAL DISPLAYS
301
in male cichlid fish (Aequidens rivulatus) raised in social deprivation (Groothuis, 1993b). Such abnormalities may have been overlooked in the past, and more detailed observations of display behavior of animals reared in abnormal conditions are necessary to establish the generality and causes of development of abnormal display. The context in which abnormal display developed in the gulls suggests that operant conditioning may influence display development. This seems incompatible with the conclusion presented above, that the neural coordination mechanism for the normal complete display is present very early in ontogeny. Two explanations for this incompatibility are conceivable. First, normal social interactions, although not indispensable for normal display development, may also guide normal display development. This may explain why only 40% of the birds raised in isolation performed complete display and why in most of the testosterone-treated chicks gradual display development could still be found. This is in line with the interpretationby Radesater (1974)of the normal developmentof the facingaway component in the cackle ceremony in the Canada gosling. He suggested, partly on the basis of experiments in which bodily contact in aggressive interactions was prevented, that the development of this component is under the influence of experience in contexts that “almost give the impression of a Skinnerian learning situation.” Second, normal social interactions do not influence form development of display, but abnormal interactions may distort normal development. Both of these two possible mechanisms need further study.
E. CONCLUSION In the black-headed gull, in which the emergence of display in normal ontogeny is clearly gradual, the hormonal experiments showed that the complete species-specific adult display is present early in ontogeny. The gradual emergence of the motor patterns is not due to development in motor coordination itself, but to development of the proper motivational state, which then activates the complete display. In the gulls, testosterone is an important component of the motivational state for agonistic display. The production of testosterone gradually increases in the course of ontogeny and the results of social deprivation experiments indicate that this increase is under the influence of experience gained in agonistic interactions. Imitation can be ruled out as a factor influencing display development. Social interactions, at least abnormal social reactions, may induce abnormal forms of display. In the introduction of this section (II,A), a contradiction concerning display development as reported in the literature was mentioned. In some species adult display seems to develop gradually, while in others the
302
T. G . G . GROOTHUIS
complete display is present early in ontogeny. Based on the findings presented so far on display development in the black-headed gull, we now may account for this contradiction as follows. Species-specific differences in display development do not represent differences in the mechanism of motor development itself, but only in the timing of the expression of the complete display. This timing depends on the time span in which the development of the proper motivational state takes place. Species-specific properties of the timing of emergence of complete display may be related to the functional consequences of early performance of the complete display. These functional consequences of display development are discussed in Section V. 111.
FORM FIXATION OF DISPLAYS
Although form fixation has been widely accepted as part of the mechanism of song development in songbirds, it has hardly been discussed within the context of development of displays other than song. For the blackheaded gull displays, the following findings support the presence of form fixation.
1. The adult displays are stable in form. That is, adult birds perform stereotyped display and hardly perform the incomplete display typical for young gulls. However, two findings may moderate this statement. First, form fixation in adult birds is not complete. Only 80 to 90% of adult oblique display and 60% of adult choking can be considered to be complete. Second, form fixation is not permanent. Each year in winter and early spring adult gulls first perform low percentages of complete display before complete display becomes predominant again in the breeding season (see finding 4, below; Fig. 12). Some incomplete display patterns, however, such as the oblique with the bill pointing downward, almost never recurred in adult birds after the complete display had emerged completely. 2. The deviations in form of display that developed in some birds reared in small groups (see section II,D), became a stereotyped part of the behavior of these gulls. The abnormal patterns were still performed when the birds were tested in large groups and exposed to gulls which were unfamiliar to them. Two conclusions can be drawn from this. First, because these motor patterns were abnormal in form, form fixation is not limited to the normal form of display only. Second, because deviating display often developed rather late in ontogeny, after the sixth month of age, form fixation can still take place after the period in which it normally occurs. To test the reversibility of the abnormalities in more detail, the birds
ONTOGENY OF SOCIAL DISPLAYS
303
were, over the course of several years, rehoused repeatedly with birds unfamiliar to them. Gradually, the abnormal displays were replaced by normal ones. However, the abnormal displays never disappeared completely from the behavioral repertoire. Especially in highly aggressive interactions, probably representing situations in which a prompt decision is required, the birds often reverted to the old abnormal routines. Fentress and McLeod (1987) reported similar findings for the return of certain locomotion patterns during stress in wolves and mice. 3. While social isolation from close to hatching onward resulted in incomplete oblique display or no display at all in 60% of the birds (Table I), this decreased to 25% when social isolation started after the display had emerged completely (Groothuis, 1992). Thus, once it has emerged, the complete display is relatively stable in form. 4. When it has developed under the influence of testosterone, the complete display becomes independent of this hormone. This is concluded from the following findings (Groothuis and Meeuwissen, 1992). First, adult gulls frequently perform complete display in autumn, when blood levels of testosterone are very low. Second, young gulls, performing complete display under the influence of testosterone treatment, continued to perform complete display frequently after the hormonal treatment had been terminated. This has been confirmed, with interesting additional results, in the following experiment (T. Groothuis et al., unpublished data). Juvenile gulls of about 5 months of age that had been reared in small groups were implanted with pellets of testosterone propionate and housed in large aviaries together with untreated control birds of the same age. After 2 weeks, the pellets were removed from half of the birds (TO group). In this group, blood levels of testosterone appeared to be very low (mean: 0.5 nglml [S.E. = 0.31 as measured by radioimmunoassays) from 2 days after removal of the pellet onward. The other birds that kept their pellet (T + group) showed persistently heightened blood levels of testosterone (mean at day 3 after removal of the pellet in the TO group: 5.84 ng/ml [S.E. = 1.231; at day 14, mean: 4.2 ng/ml [S.E. = 1.21). In the course of the 5 weeks after removal of the pellet in the TO group, form and frequency of oblique display were measured in all birds. The percentage of complete oblique display after withdrawal of the pellet is depicted in Fig. 1 1 . N o statistically significant differences were found between the T + and the TO groups (Mann-Whitney U test, p = .18). The untreated control birds showed much lower percentages of complete oblique display than both the T + and the TO groups (Mann-Whitney U tests, p = .003 and .002, respectively). Despite these persistently high percentages of complete display in the TO group, and in contrast to the results of Groothuis and Meeuwissen
304
T. G . G . GROOTHUIS
inn,
FORM FIXATION OBLIQUE
FIG.1 1 . Percentage of complete oblique display (mean and S.E.) in three groups ofjuvenile gulls averaged over the course of 5 weeks after removal of the testosterone propionate pellet in one group. See text for details.
(1992), the frequency of display in the TO group decreased considerably after withdrawal of the pellet, although it still remained somewhat above the level of control birds. Thus, TO birds performed complete display, but infrequently. This is different from what we have found in the course of normal ontogeny, during which frequency and completeness in form of a display were positively correlated. This correlation is to be expected because the motivational effect of testosterone is likely to influence both aspects of display behavior. The activation of a motivational system is very often measured on the basis of the frequency of performance of a relevant motor pattern. The disconnection of frequency and form of the display therefore give additional evidence that the form of display becomes uncoupled from its original motivational factor. The independedce of oblique display of testosterone appeared to be limited in time span. It is likely to be built up again each year in the course of the breeding season. Observations on adult gulls in large aviaries in March showed that the frequency and completeness in form of oblique display gradually increase over the course of several weeks, starting from low levels at the beginning (Fig. 12). In this period, testosterone production starts to rise and a positive correlation between blood levels and testosterone production wasfound(r = .78, n = 6 , p < .05). Furthermore, testosterone treatment of adult birds induced far more complete display than in untreated control birds (see Fig. 12). The mechanism by which form fixation takes place is as yet unknown. Three possibilities are conceivable. First, form fixation may be induced by testosterone itself, inducing structural changes in the nervous system.
305
ONTOGENY OF SOCIAL DISPLAYS
100
80-
'
c
:"I /r a
-a c
5
40
s
20
I ) ,
,
p
O 1 2 3 4 weeks weeks FIG.12. Frequency and percentage of complete form of oblique display (mean and S.E.) in two groups of adult gulls (controls and implanted with testosterone propionate pellets at the beginning of week 1) over the course of 4 weeks in early spring.
The latter has been shown to occur in the case of song development in song birds (e.g., Bottjer and Arnold, 1986). Furthermore, Marler et al. (1988) induced crystallized song in song sparrows and swamp sparrows after treatment with testosterone. A direct influence of testosterone on form fixation may explain why incomplete forms of display, occurring when testosterone production is still low, do not become fixed in form. Second, form fixation may be caused by repeated performance of the same motor pattern. This has also been suggested by Andrew (1969) for the development of calls in testosterone-treated domestic chicks. Provine (1990) has drawn attention to the possibility that muscular activity influences properties of the neural circuitry. Such examples are known from the embryonic period and it is conceivable that these processes may also occur later in life. This second explanation of form fixation may account for fixation of stereotypies in farm animals (for a review, see Mason, 1991) that are probably not under the control of sex hormones. The third possibility is that form fixation takes place by experience gained in social interactions. Social experience may then take over the role of testosterone in inducing the performance of the behavior patterns. The results of two experiments indicate that experience with the performance of a certain behavior pattern may cause the behavior to become independent of the original hormonal background. Rosenblatt and Aronson
306
T. G. G. GROOTHUIS
(1958) found that cats continued to copulate in tests with a female after castration, but only if they had been given some experience with copula-
tions before castration. The second example comes from my own study on gull display (T. Groothuis, in preparation). Juvenile gulls, reared in small groups, were at the age of 9 months rehoused in either a large group (Gr) or social isolation (Iso). They were implanted with pellets of testosterone propionate which were removed 2 weeks later. A further 2 weeks later, all birds, including the isolates, were rehoused in (new) groups, and implanted again with pellets of testosterone propionate. Under the influence of the second implant, the frequency of oblique display in the Gr birds rapidly increased. This increase was stronger than during the presence of the first implant in these birds. This suggests that, after having emerged due to the first implant, the display becomes more easily activated by a second implant. As was expected, these birds performed complete display in adult percentages right from the first day after the second implantation was carried out, due to the fact that form fixation had already taken place. However, the Is0 group performed 50% complete display only after the second implantation. In contrast to the Gr birds, these Is0 birds had hardly performed display in the first implant period, due to social isolation. This suggests that experience with the performance of display in the period of the first implant influences the quality of display performance in the second period. The finding that reinstatement of a behavior pattern due to a second treatment with testosterone depends on experience with that pattern during the first treatment has also been reported by Rosenblatt (1965) for copulation behavior in the domestic cat. IV. CHANGE IN CONTEXT OF DISPLAY
The data presented in the previous sections showed that the motor mechanisms for complete display are present very early in ontogeny. These motor patterns must then become embedded in behavioral programs in such a way that the animal may use these tools in a functional way. In the literature, the general idea emerges that, in contrast to the development of the separate motor patterns, experience is needed for the development of the proper application of these motor patterns (e.g., Kruijt, 1964; Fentress and McLeod, 1987). This may lead to changes in the context and causation of display and I shall discuss some of these briefly in this section. The early motor patterns may first occur more or less randomly, and may become more specifically coupled to specific external and/or internal stimuli only later in life. In other cases, the internal or external control of display may be present early in the young animal, but the relevant causal
ONTOGENY OF SOCIAL DISPLAYS
307
factors may change later in development. I discuss these two possibilities in turn. A classical example of the first case is play in young mammals. In play, the performance of the different motor patterns seems to occur in a relatively arbitrary and inappropriate order. Furthermore, the young animals are easily distracted from these social interactions. Older animals are much more persistently involved in such interactions and use their motor patterns in a more predictable manner. The latter may have developed under the influence of experience gained during play (but see Martin and Caro, 1985). In relation to the decrease in distractibility, it is interesting to note that Andrew (1976) presented evidence for an increase in persistence of attention and a decrease in distractibility under the influence of androgens. As has already been discussed, displays, which are often performed during play, are under the control of sex hormones, and the production of these hormones increases with age. Thus, the increasing integration of the different motor patterns of social behavior in ontogeny may partly be due to the development of the proper motivational factors, including testosterone. This may reveal the characteristics of adult behavior, already potentially present in the young, more completely, as was the case in the development in form of these patterns. Some evidence for this is given by the results of the following experiments. Kruijt (1964) reported for the normal ontogeny of social behavior in junglefowl an increasing integration of the separate motor patterns such as pecking, leg movements, and displays. However, young chicks of only 1 week in age, confronted with each other after being reared in isolation for 1 week, not only performed several displays prematurely (see earlier), but performed these displays in the same way as 1-month-old birds in complete fights. Similarly, very young testosterone-treated cichlid fish performed many of their displays in a temporal structure similar to that of adult fish (Groothuis and Ros, in preparation). The same is true for testosterone-treated young black-headed gulls. Although the behavior of young animals may look chaotic, this may in part be attributed to the short duration of the displays and the relatively frequent and rapid transitions between the different motor patterns, including overt aggression and overt escape. In these species at least, the basic temporal structure of the behavior seems to be present early in ontogeny and may be expressed under the influence of the proper combination of internal and external stimuli. However, even in these cases, experience, especially social experience, may influence the temporal structure of the behavior in more detail. Rearing animals from early on in social isolation often results in erratic and highly aggressive behavior (for a review, see Huntingford and Turner, 1987, p 212). Furthermore, such animals often direct their behavior to
308
T. G . G. GROOTHUIS
inappropriate stimuli such as their own body, for example, tail-fighting junglefowl (Kruijt, 1964), wing-pecking in gulls (Groothuis and van Mulekom, 1991), and tail-biting in cichlid fish (Groothuisand Ros, in preparation). In the course of ontogeny a display may also change from one specific context to another, which is not readily explained by an increase of a particular motivational state. For example, young junglefowl males perform the waltzing display to each other in agonistic interactions, whereas adult males perform this display predominantly toward females in sexual encounters. This shift in context depends on social experience (Kruijt, 1964). A similar shift in context, depending on social experience, was found for the quivering display in a species of cichlid fish (Groothuis and Ros, in preparation). Preliminary evidence indicates that operant conditioning is involved in the shift in context of waltzing in the fowl, with copulation opportunity with a female being the reward. Baerends-van Roon and Baerends (1979, p. 85) have suggested that operant conditioning is involved in the development of the context of the “rolling” invitation display in kittens. A change in context of display was more quantitatively established and experimentally manipulated for the case of the displays of the blackheaded gull. In Section 111 I discussed the mechanism leading to fixation in the form of display in this species. During form fixation the form, and to a lesser extent the frequency, of displays become relatively independent of motivational fluctuations. The finding presented earlier, that the oblique display becomes independent of its original hormonal causal factor, testosterone, is in line with this. Interestingly, this change in hormonal background is accompanied by a change in the context of the display. This stems from the following findings. 1. In young black-headed gulls the oblique display is performed exclusively in a clearly agonistic context when defending the territory or in competition for food and water. Adult gulls perform the very same display in other contexts as well, such as during pair formation, nest relief between partners of a well-established pair, and when calling their young. In all of these situations overt aggression hardly occurs or is completely absent. 2. Young gulls perform the oblique during transitions between running aggressively toward and running away from the opponent, while adult gulls use it during quiet approach or when standing still beside the partner. 3. In contrast to adult gulls, young gulls perform oblique-like display frequently in alternation with overt aggression: the percentage of obliquelike display that is immediately followed by aggressive pecking decreases strongly in the course of ontogeny (Fig. 13A). 4. Adult gulls frequently alternate the oblique and forward postures.
309
ONTOGENY OF SOCIAL DISPLAYS IWU
%
L
i L
60 -
20 0 N= 75
3
4
6 10-12 age (weeks)
ADULT
202
166
119
306
ADUL.T ADULT 4-6 10-12 age (weeks) FIG.13. Percentage of oblique-like postures that is immediately followed by aggressive pecking (A) or forward-like postures (B)in group-reared black-headed gulls in the course of ontogeny .
0-2 0-2
3
However, in young gulls the percentage of oblique-like display that is immediately followed by forward-like display is initially very low (Fig. 13B), despite the fact that these young perform incomplete forward postures very frequently. 5 . Adult gulls frequently perform the oblique-forward sequence synchronously with the performance of these displays by the opponent. For example, adults perform 42% of their oblique postures simultaneously with the oblique display of the opponent. The equivalent is only 15% in 6week-old young. These findings indicate that, in the course of ontogeny, a shift takes place from activation of displays primarily by internal factors to a situation in which the displays are strongly under the control of specific external factors. This suggests that form fixation is accompanied by a change in causation of the display. This may provide the bird with some sort of behavioral routine, a tool which can be used in different behavioral contexts. Except for finding (4), all of these ontogenetic changes in the application of display behavior appeared to be under the influence of social experience. This follows from results of experiments in which gull chicks were reared either in visual isolation from other birds (until the age of about 10 months) or in small groups of 2 to 4 individuals (until the age of 15 weeks). At the time these birds were placed together with conspecifics of the same age, the following results were obtained in relation to the five findings presented above (Groothuis and van Mulekom, 1991).
310
T. G. G. GROOTHUIS
1. Birds reared in isolation always performed the oblique display in association with attack, even when interacting with the other sex. This resulted in failure to establish a pair-bond and to mate. 2. These birds still performed the oblique during erratic aggressive approaches to and escape movements away from the other birds. 3. In both groups of experimental birds, the frequency of aggressive pecking relative to the frequency of oblique display was extremely high for their age, a ratio of about 1.O. This score is 0.5 in normally reared birds of 9 weeks of age and 0.05 in adults. 4. Although highly aggressive, all experimental birds performed oblique-forward transitions like normally reared adults. 5 . Especially when reared in visual isolation, the birds did not adjust their display behavior to that of the opponent. They even performed display on their own, in the absence of any opponent. Furthermore, they did not seem to comprehend the display of conspecifics. This may be illustrated by the fact that they continued to approach the bathing pool or feeding place seemingly without noticing the performance of threat display by another bird at that spot. Normally reared birds would retreat or perform a threat display themselves.
Thus, in the black-headed gull, social experience clearly influences the change in context of display, which normally occurs in the course of ontogeny. Some of the deviations that developed in the isolates also occurred in the small groups. Therefore, these deviations are not just abnormalities caused by a crude manipulation such as complete social isolation. Moreover, birds in the small groups were specifically deprived of agonistic interactions, but not from social interaction in general. Thus, experience with agonistic interactions in particular influences the normal development in context of display behavior. Additional data on the behavior of the birds in the small groups indicate that the amount of experience with display performance during the rearing period before the test influences properties of agonistic behavior during the test. On the basis of this and other data, Groothuis and van Mulekom suggested that both classical and operant conditioning of display take place during ontogeny.
V. FUNCTIONAL ASPECTSOF DISPLAY DEVELOPMENT The way the adult is adapted to the environment will often be based on mechanisms that need to develop in ontogeny. This is obviously so in those cases where functional experience is required in order to adapt the behavior to particular circumstances, such as knowledge of local food
ONTOGENY OF SOCIAL DISPLAYS
311
supply or species-specific song characteristics. But, even in such clear cases, the young organism must be adapted to the environment and to its specific needs in every stage of ontogeny in order to reach maturity, when it may reproduce. Therefore, the concept of behavioral ontogeny as merely a development from imperfect and incomplete behavior toward more adequate adult behavior has rightly been abandoned (e.g., Stamps, 1978; Oppenheim, 1980,1981; Hogan, 1988). Natural selection on the adult stage will obviously influence the mechanisms necessary to develop and this may put restrictions onto the developing animal. But, vice versa, for the developing young to survive, natural selection may provide it with mechanisms that may determine adult properties. Unfortunately, the relationship between causal and functional aspects of behavioral development has hardly been studied. In this section, some suggestions are presented for the functional consequences of each of the three aspects of display development in the black-headed gull that I have discussed in this article: gradual development, form fixation, and change in context. A. GRADUALDEVELOPMENT I N FORM OF DISPLAY If the complete adult displays are present early in ontogeny (as has been shown in Section II), why do gulls that are less than 10 weeks old perform incomplete displays only? There are two functional explanations for this: 1. In the course of the first 2 weeks of ontogeny, the chicks begin to demand so much for food that both parents often have to leave the territory to forage. At the same time, the young become more mobile and often leave the nest site. These changes have two consequences. First, by that time, but not earlier, the young one must have a display at its disposal to signal its location at the moment the parent returns to the nest. At the same time, this display must become an increasingly conspicuous, strong enough stimulus to induce the parent to regurgitate as much food as possible. Both functions are fulfilled with the pumping display, which gradually develops in form and frequency in the course of the second and third week after hatching, and which disappears from the repertoire by the time the young become independent. Second, territorial defense must be increasingly performed by the young one itself. A prerequisite for this is that chicks are able to distinguish siblings and parents from other gulls in the colony, to prevent misdirected aggression. This ability develops at the end of the first week, just before aggressive behavior starts to emerge (T. Groothuis, unpublished observations). However, chicks are vulnerable, especially in the many interactions that occur with older young and adult intruders. By performing long-
312
T. G. G. GROOTHUIS
lasting pronounced display openly in front of the intruder (often an older and thus stronger young one or adult), the chick would provide the opponent ample opportunity to attack. Therefore, instead of displaying, chicks defend their temtory by hiding in the vegetation, performing incomplete choking display. This display, especially the vocalization, may act as a warning to the opponent. If the latter does not retreat, the chick may suddenly jump to its feet, run toward the opponent in an erect obliquelike posture, attack the surprised intruder strongly, after which it suddenly disappears in the vegetation again, crouching in a choking-like posture. Furthermore, siblings never attack each other and agonistic behavior of a young one does not provoke attack by its sibling. This provides the possibility for two or more siblings to attack the same intruder simultaneously. In this way, chicks are often able to win territorial interactions. During the same period in which aggression develops, young gulls need to have a display at their disposal for signaling to their parents and siblings their lack of intention to attack. This function is fulfilled by the incomplete forward displays (called the hunched by Moynihan [ 19551 and Tinbergen [ 1959]), which in form are the opposite of the erect aggressive oblique-like postures. Although all display postures emerge completely in the first 3 months of age, the vocalizations, especially the long call, do not lose their juvenile characteristics before the first summer, when the breeding season has already started. Black-headed gulls hardly ever breed in their first summer, and the juvenile characteristics may signal to adult gulls that these nonbreeders offer no serious threat to them. The reason why juvenile gulls normally do not breed before their second summer is not clear. In our aviaries we found that juveniles are able to reproduce successfully. However, choosing a mate for life, obtaining a central place in the colony (where reproductive success is relatively high), and finding enough food for their young are likely to be difficult tasks. Therefore, in order to gain substantial experience, reproduction may be postponed. 2. The other functional explanation for the gradual development of display is that complete display is triggered by relatively high levels of testosterone. However, testosterone production has some clear disadvantages for the young. First, the production of this hormone is energetically costly. Second, early treatment with testosterone results in rapid growth of the syrinx, which may hamper normal respiration (Groothuis and Meeuwissen, 1992). Third, testosterone may inhibit growth. This follows from the results of implantation experiments in chicks 6 days after hatching. Chicks implanted with pellets of testosterone propionate for 10 days and
ONTOGENY OF SOCIAL DISPLAYS
313
housed together with untreated chicks of the same age in an ad libitum food situation show retardation in weight (see Fig. 14), molt, and skeletal growth after the implantation period (R. Ros and T.G.G. Groothuis, unpublished observations). Obviously, a chick has to invest in growth and this is especially important for black-headed gull chicks. At the end of the breeding period there is a sudden and brief exodus from the colony. In a few days, if left alone, protection against predators becomes ineffective and almost none of the remaining young will survive. Therefore, to be able to leave the colony in time, together with the other birds, rapid growth is of vital importance for the black-headed gull chick. So far, it has been argued that the performance of incomplete displays does not fulfill a function in the development of the complete display. However, by performing incomplete display, the young will enhance their chance of getting involved in agonistic interactions. This may promote three things. First, it may stimulate testosterone production via visual input, leading to the activation of complete display. Second, it may enhance the production of this hormone via behavioral self-feedback (Cheng, 1979);that is, by performing incomplete display the young bird may stimulate its own production of testosterone by proprioceptive feedback, leading to the emergence of complete display. Third, because the performance of complete display has disadvantages, the use of incomplete display may lead the bird to gain the necessary experience that has been shown to be important for the development of normal social behavior.
1
0 weight before implantation (9) FIG.14. Growth in chicks that had been treated with testosterone propionate pellets for 10 days, and in controls of the same age. Weight was measured on the day of implantation (day 6 after hatching) and 10 days later.
3 14
B.
T. G. G. GROOTHUIS
FORMFIXATION
It is generally accepted that the stereotypy of displays is due to selection for motor patterns that promote species recognition and serve to provide communication within the species. Many incomplete forms of display in the black-headed gull show similarities with displays of related gull species (Groothuis, 1989b). Therefore, the occurrence of form fixation of the display in its species-specific form is comprehensible from a functional point of view. The importance of the species-specific form of display also explains why the details of form of these displays were affected only by abnormal reading conditions. However, the deviating displays did show that some plasticity still exists in the form development of display. This fits in with the notion that these displays may serve as vehicles for individual recognition (e.g., Veen, 1980). Indeed, I often had the impression that I could recognize individuals by minor differences in the form of display postures and vocalizations. Displays may also act as subtle vehicles for communication about motivational state and resource holding potential (Beer, 1980; Veen, 1980), which may explain why form fixation was found not to be complete. C. CHANGE I N CONTEXT This concerns two findings: (1) The displays become independent of testosterone in form and frequency; (2) the displays emerge in an agonistic context but are applied by adult birds in other contexts as well. The first finding may be interpreted from a functional point of view as follows. As colonial birds, which have to defend their territory throughout the breeding cycle, black-headed gulls must be able to execute the agonistic displays throughout the period they breed and provide parental care. However, breeding and feeding the young may not be compatible with a high production of testosterone, because these behaviors require the production of other hormones (e.g., Cheng, 1979), while testosterone may inhibit the performance of these behaviors. Therefore, in this species during the breeding period, the causation of display needs to be independent of testosterone. The second finding, the widening of the context of display, is clearly related to the fact that adult gulls must be able to communicate about items other than territorial defense: they have to communicate with their partners and young. Using the displays already available in the repertoire in earlier stages of development seems efficient for this, but it requires a change in the motivational factors affecting the display, as has indeed been found. However, adult birds still need these displays in the agonistic
ONTOGENY OF SOCIAL DISPLAYS
315
context too. In order to prevent confusion in intraspecific communication, two solutions are conceivable. First, the birds may use one subform of display in the agonistic context and another subform in the other context. Evidence for this is provided by data on the oblique display. In young birds all subforms of oblique display are frequently followed by aggression. However, if in adult birds oblique display is immediatelyfollowed by overt aggression, this display is almost always performed with the neck vertical and the bill pointing upward, while in nonagonistic contexts other forms of the display are shown (Groothuis, unpublished data). The second solution is that the receiver of the message that is transmitted by the display is able to understand that message in relation to the context in which the display is performed (see also Manley, 1960). This may be illustrated as follows. If the message of the choking display is “I want to stay on this spot,” it may signal to intruders that the displaying bird is willing to defend that place, inducing retreat in the opponent, and to its partner that it is willing to build its nest at that spot, inducing approach. Context-dependent interpretation of display in the black-headed gull explains easily the occurrence of the same display in different contexts. In conclusion, each of the three main items that have been discussed in this article, form development, form fixation, and change in context, can be explained, at least for the case of display development in black-headed gull, from both a causal and a functional perspective. In Section I1 it was suggested that species-specific differences in the timing of emergence of the complete display are related to the function these motor patterns fulfill for the young animal. As discussed above, the gradual emergence of complete display in the black-headed gull can be satisfactorily explained in this way. Would it be possible to explain from a functional point of view the early presence of complete display in other species? Although we need much more study in this field, there is some evidence for this. For example, Stamps (1978)explained from a functional point of view the form and frequency of early complete display in a lizard species. VI.
A SUMMARIZING SCHEME
The basic properties of the mechanisms underlying the gradual emergence of complete agonistic display in the black-headed gull in Fig. 15. Early agonistic interactions stimulate the production of testosterone (see arrow 1). This production gradually increases in the course of ontogeny, triggering gradually more form elements of the complete display (2). As explained previously, a positive feedback loop may be involved here.
316
T. G. G . GROOTHUIS
SOCIAL INTERACTIONS
II4
PRODUCTION OF TESTOSTERONE
b I I
1
OTHER INTERNAL FACTORS
I
I
ACTIVATION ALREADY COORDINATED MOTOR ELEMENTS
1 FORM FIXATION
I
0
CHANGE IN CONTEXT
I
FIG. 15. Schematic outline of the causal mechanisms underlying the emergence of complete agonistic display in the black-headed gull in the course of ontogeny. Closed arrows indicate causal relations for which good evidence has already been obtained. Open arrows indicate possible causal relations for which hard evidence has yet to be collected.
The performance of incomplete display may in turn enhance testosterone production, either by behavioral self-feedback (3), or because the performance of display provokes agonistic interactions (4). Furthermore, testosterone itself may motivate the bird to initiate more interactions, which in turn may stimulate testosterone production (5). Attempts to obtain evidence for an influence of imitation or practice revealed negative results. The neural coordination mechanisms for the complete display are present very early in ontogeny. These mechanisms can be activated by the proper internal motivation (2), which may in turn be activated by the proper external stimuli. Which mechanism, that is, which display will be activated, depends on motivational factors other than testosterone alone (6), such as the activation of control systems for escape, hiding, or to stay put Social interactions may influence the final form of the display (7): abnormal social interactions have been shown to induce abnormal form elements in the display. Whether normal social reactions influence normal development is not yet clear. Once fully expressed, the complete display becomes fixed in form. As yet the mechanisms underlying form fixation have not been unraveled. Three possibilities that are not mutually exclusive have been discussed and are at the moment the subject of further study in our laboratory. First,
ONTOGENY OF SOCIAL DISPLAYS
317
testosterone itself may induce form fixation (8). Second, the hormone may only be indirectly involved in this process by inducing frequent performance of the motor pattern. Repeated performance of the same pattern may then cause form fixation (9). Third, social reactions of conspecifics to the display performed may be important (10). Form fixation is likely to go hand in hand with a change in causation of display (1 1). Indeed, after form fixation, the display becomes independent of testosterone and is performed in nonagonistic contexts as well. The displays become like subroutines, easily activated and applicable in different behavioral programs. This change in the context of display is influenced by social experience (12), in which operant conditioning may play a role. The model is probably applicable to a variety of cases other than the agonistic displays of the black-headed gull, although the properties of the relevant motivational factors may be different in different cases. The results obtained so far on display development in cichlid fish easily fit in with this scheme. Furthermore, this scheme explains the contradiction that appears in the literature that was discussed at the beginning of Section 11. Both in species in which the adult display is performed very early in ontogeny, and in species in which the complete display seems to develop gradually, the neural coordination mechanism for the complete display is likely to be present early in ontogeny. Species-specific differences in display development do not concern the development of the neural mechanism itself, but the timing of the expression of the complete display. This timing concerns the development or activation of the proper motivational state. As explained in Section V, this timing may be based on its functional consequences. The early presence of a kind of central pattern generator for the complete motor pattern demonstrates a certain similarity between the ontogeny of displays and of many other motor patterns. For walking (e.g., Bekoff and Trainer, 1979; Clark et al., 1988), flying (e.g., Provine, 1981), grooming (e.g., Fentress, 1978), and other behaviours (e.g., Prechtl, 1984), it has been shown that the gross coordination of the patterns develops prior to the time that the motor pattern itself can be observed, and/or without the influence of sensory feedback, as has been reviewed by Fentress and McLeod (1987). And, as was discussed earlier in this article, the occurrence of form fixation has been shown to occur in song development and in the development of stereotypies in farm animals. The early presence of the neural coordination mechanisms for the complete display may bring part of the analyses of display development into the field of experimental embryologists. However, the analysis of the timing and the way by which these mechanisms come to expression, and
3 18
T. G . G . GROOTHUIS
how they may be modified in the course of ontogeny and brought under the control of higher order structures in the CNS, are unquestionably relevant topics and worthwhile for further research by behavioral biologists.
VII. SUMMARY The ontogeny of social displays is of special interest due to its potential as a special case of motor development and may provide insight into the development of social behavior in general. In this article. a synthesis is given of causal and functional aspects of the development of these speciesspecific stereotyped motor patterns. To this end, data from the literature and from several studies of display development in the black-headed gull are integrated. In contrast to most of the studies reported in the literature, the gull studies include a set of coherent experiments. These experiments were designed to test the underlying mechanism of the gradual form development of display which appeared to occur in normal ontogeny in this species. By manipulating social experience, external stimuli, and hormonal conditions, the influence of the following factors was tested: (a) maturation, (b) change in external stimuli, (c) change in internal motivational stimuli, and (d) matching the motor output against a template. In relation to the last mechanism, the influence of imitation and social reactions on display performance has been analyzed. The basic conclusions are summarized in Section VI and Fig. 15. From the literature a difference between species emerged in that in some species display seems to develop gradually, while in others the complete display is present early in ontogeny. It is concluded that these species-specific differences only concern the timing of the complete expression of the display, for which the neural coordination mechanism is present early in ontogeny . This difference may be caused by its functional consequences, which may be different for different species. After the emergence of the complete display, form fixation takes place, which is in turn followed by a change in context and in causation of the displays.
Acknowledgments I thank Gerard Baerends and Jaap Kruijt for their valuable comments on the manuscript. They and the other members of the Ethology group in Haren have stimulated me throughout the research projects reported in this article. I thank Dick Visser for preparing the figures.
ONTCGENY OF SOCIAL DISPLAYS
319
References Andrew, R. J. (1963). Effect of testosterone on the behaviour of the domestic chick. J . Comp. Physiol. Psychol. 56, 933-940. Andrew, R. J. (1966). Precocious adult behaviour in the young chick. Anim. Behau. 14, 485-500. Andrew, R. J. (1969). The effect of testosterone on avian vocalizations. I n ”Bird Vocalizations” (R.Hinde, ed.), pp. 97-131. Cambridge Univ. Press, Cambridge. Andrew, R. J. (1976). Increased persistence of attention produced by testosterone. and its implications for the study of sexual behaviour. I n “Biological Determinants of Sexual Behaviour” ( J . B. Hutchison, ed.), pp. 255-275. Wiley. Chichester. Baerends, G. P. (1975). An evaluation of the conflict hypothesis as an explanatory principle for the evolution ofdisplays. I n “Function and Evolution of Behaviour” ( G .P. Baerends. C. Beer, and A. Manning, eds.), pp. 187-227. Oxford Univ. Press, London. Baerends, G. P. (1991). On spontaneity in behaviour. the model (fixed) action pattern and play. Nerh. J . Zool. 40(4), 565-584. Baerends, G. P., and Groothuis, T . G. G. (1992). The ”Fixed action pattern” concept revisited: An ethological commentary on the papers by Prechtl and Provine. I n “Motor Development in Early and Later Childhood: Longitudinal Approaches” (A. F. Kalverboer, B. Hopkins, and R. H. Geuze, eds.). Cambridge Univ. Press, Cambridge. Baerends van Roon, J. M., and Baerends, G. P. (1979). The morphogenesis of the behaviour of the domestic cat. Proc. R. Nerh. Acad. Sci., Sect. Phys. [ 2 ] Part 72. 1-116. Baptista, L. F., and Petrinovich, L. (1984). Social interactions, sensitive phases and the song template hypothesis in the white crowned sparrow. Anim. Behau. 32, 172-181. Bateson, P. P. G. (1983). Genes, environment and the development of behaviour. Anim. Behau. 3, 52-81. Beer, C. (1980). The communicative behaviour of gulls and other seabirds. I n “Behaviour of Marine Animals’’ ( J . Burger, B. L. Olla, and L. E. Winn, eds.). Vol. 4. pp. 162-206. Bekoff, A., and Kauer, J. A. (1982). Neural control of hatching: Role of neck position in turning on hatching leg movements in post-hatching chicks. J Comp. Phvsiol. 145, 497-504. Bekoff, A., and Trainer, W. (1979). The development of interlimb coordination during swimming in postnatal rats. J . Exp. Biol. 83, 1-1 I . Bottjer, S. W., and Arnold. A. P. (1986). The ontogeny of vocal learning in songbirds. Handb. Behav. Neurobiol. 8, 86-186. Cheng, M. F. (1979). Progress and prospects in ring dove research: A personal review. Adu. Study Behau. 9, 97-129. Clark, J. E., Whitall, J., and Philips, S. J. (1988). Human interlimb coordination: The first six months of independent walking. Deu. Psych. Biol. 21(5), 445-456. Coghill, G. E. (1929). “Anatomy and the Problem of Behaviour.” Cambridge Univ. Press, London. Daanje, A. (1951). On locomotory movements in birds and the intention movements derived from them. Behaviour 3,48-98. de Beer, G. R. (1940). “Embryos and Ancestors.” Oxford Univ. Press (Clarendon). Oxford. de Lannoy, J. (1967). Zur pragung von Instinkthandlungen. Z. Tierpsychol. 30, 162-200. Drachman, D. B.. and Sokoloff, L. (1968).The role of movement in embryonic joint development. Deu. B i d . 14, 401-420. Fentress, J. C. (1978). Mus Musicus. The developmental orchestration of selected movements patterns in mice. I n “The Development of Behaviour: Comparative and Evolutionary Aspects” (M. Bekoff and G. Burghardt, eds.), pp. 321-342. Garland, New York.
320
T. G. G. GROOTHUIS
Fentress, J. C., and McLeod, P. J. (1987).Motor patterns indevelopment. Handb. Neurobiol. 8, 38-97. Field, T. M.. Woodson. R., Greenberg, R., and Cohen, D. (1982). Discrimination and imitation of facial expressions by neonates. Science 218, 179-181. Groothuis, T. (1989a). On the ontogeny of display behaviour in the black-headed gull (Larus ridibundus). Ph.D. thesis, University of Groningen, The Netherlands. Groothuis, T. (1989b). On the ontogeny of display behaviour in the black-headed gull. I. The gradual emergence of the adult forms. Behauiour 109(1/2), 76-124. Groothuis, T. (1989~).On the ontogeny of display behaviour in the black-headed gull. 11. Causal links in the development of aggression, fear and display behaviour: Emancipation reconsidered. Behauiour 110, 161-204. Groothuis, T. (1992). The influence of social experience on the development and fixation of the form of displays in the black-headed gull. Anim. Behau. 43, 1-14. Groothuis, T., and Meeuwissen, G. (1992). The influence of testosterone on the development and fixation of the form of displays in two age classes of young black-headed gulls. Anim. Behau. 43, 189-208. Groothuis, T., and van Mulekom, L. (1991). The influence of social experience on the ontogenetic change in the relation between aggression, fear and display behaviour in black-headed gulls. Anim. Behau. 42, 873-881. Groothuis, T. G. G. (1993a).The ontogeny of display behaviour: the relation between motor development and the development of motivational systems. I n "Causal Mechanisms of Behavioural Development" ( J . A. Hogan and J. J. Bolhuis, eds.). Cambridge Univ. Press, Cambridge. Groothuis, T. G. G. (l993b). A comparison between development of birdsong and development of other displays. J . Neth. Zool., in press. Groothuis, T. G. G., and Ros, R. (1993). Change in context of display in a cichlid fish: Influence of social experience and sex hormones. In preparation. Hailman, J. P. (1967). The ontogeny of an instinct. Behauiour, Suppl. 15, 1-159. Henty, C. J. (1966). Development of a threat posture in young black-headed gulls. Anim. Behau. 14, 581-582. Hinde, R. A. (1%9). "Animal Behaviour." McGraw-Hill. London. Hogan, J . A. (1988). Cause and function in development of behavioural systems. Handb. Behau. Neurobiol. 9, 63-106. Huntingford, F., and Turner, A. (1987). "Animal Conflict." Chapman & Hall, London and New York. Johnston, T. D. (1988). Developmental explanation and the ontogeny of birdsong: Nature/ nurture redux. Brain Behau. 11, 617-663. Kortlandt, A. (1940). Eine ubersicht der angeborenes Verhaltungsweisen des mittelEuropaischen Kormorans (Phalacrocorax car60 sinensis), ihre Function, Ontogenetische Entwicklung und phylogenetische Herkunft. Arch. Neerl. Zool. 4, 401-442. Kruijt, J. P. (1964). Ontogeny of social behaviour in Burmese red junglefowl (Callus gallus spediceus). Behaviour Suppl. U ,1-201. Lehrmann, D. S . (1953). A critique of Konrad Lorenz's theory on instinctive behaviour. Q. Rev. Biol. 28, 337-363. Manley, G. H. (1960). Agonistic behaviour of the black-headed gull. Ph.D. thesis, Oxford University. Marler, P., Peters, S . , Ball, G. F., Dufty, A. M., and Wingfield, J . C. (1988).The role of sex steriods in the acquisition and production of birdsong. Nature (London) 336, 770-772. Martin, P., and Caro. T. M. (1985). On the function of play and its role in behavioral development. Adv. Study Behau. l5, 59-103.
ONTOGENY OF SOCIAL DISPLAYS
32 1
Mason, G. (1991). Stereotypies: A critical review. Anim. Behau. 41, 1015-1037. Meinert, U. (1983). Jugendentwicklung der Lautauserungen beim Birkhun, Tetrix terix. Behauiour 85 (3/4), 242-260. Meltzoff, A. N., and Moore, M. K. (1977). Imitation offacial and manual gestures by human neonates. Science 198, 75-78. Morris, D. (1957). “Typical Intensity” and its relation to the problem of ritualisation. Behauiour 11, 1-12. Moynihan, M. (1955). Some aspects of reproductive behaviour of the black-headed gull (Larus ridibundus L . ) and related species. Behauiour Suppl. 4, 1-201. Moynihan, M. (1959). Notes on the behaviour of some North American gulls. IV. The ontogeny of hostile behaviour and display patterns. Behauiour Suppl. 14, 214-239. Oppenheim, R. W. (1980). Metamorphose and adaptation in the behaviour of developing organisms. Deu. Psychobiol. 13, 353-356. Oppenheim, R. W. (1981). Ontogenetic adaptations and retrogressive processes in the development of the nervous system and behaviour: A neuroembryological perspective. I n “Maturation and Development: Biological and Psychological Perspective” (K. J. Conolly and H. F. R. Prechtl. eds.), pp. 73-109. Lippincott, Philadelphia. Oyama, S. (1985). “The Ontogeny of Information.” Cambridge Univ. Press, Cambridge. Platz, F. (1974). Untersuchingen uber der Ontogenie der Ausdruckbewegungen und Lautauserungen der Kolbenenten (Netta rufina pallas) mit einem Beitrag zur Anatomie des Stimmapparatus. Z. Tierpsychol. 36, 293-428. Plooy, F. X. (1980). The behavioural development of free-living chimpanzee babies and infants. Ph.D. thesis, University of Groningen. The Netherlands. Plooy, F. X. and van de Rijt-Plooy, H. H. C. (1989). Vulnerable periods during infancy: Hierarchal reorganised systems, control, stress and disease. Ethol. Sociobiol. 10, 279-2%.
Prechtl, H. F. R. (1984). Continuity and change in early neural development. I n “Continuity of Neural Functions from Prenatal to Postnatal Life” (H. F. R. Prechtl, ed.), pp. 1-15. Blackwell Scientific Publications Ltd. Oxford. Provine, R. R. (1981). Development of wingflapping and flight in normal and flap-deprived domestic chicks. Deu. Psychobiof. 14(3), 279-291. Provine, R. P. (1990). Natural priorities for developmental study: Neuroembryological perspectives of motor development. I n “Motor Development in Early and Later Childhood: Longitudinal Approaches” (A. F. Kalverboer, B. Hopkins, and R. H. Geuze, eds.). Cambridge Univ. Press, Cambridge. In press. Radesater, T. (1974). On the ontogeny of the orienting responds in the triumph ceremony in two species of gees (Anser anser L. and Branta canadensis L. Behauiour 50, 1-15. Roggenbruck, M. E., and Jenssen, T. A. (1986). The ontogeny of display behaviour in Sceloporus undulatus (Sauria, Inguanidae). Ethology 71, 153-165. Rosenblatt, J. S. (1965). Effects of experience on sexual behavior in male cats. I n “Sex and Behaviour” (F.A. Beach, ed.). Wiley, New York. Rosenblatt, J. S., and Aronson, L. R. (1958). The influence of experience on the behavioural effects of androgen in prepubarally castrated male cats. Anim. Behau. 6, 171-182. Schleidt, W. M. (1970). Precocial sexual behaviour in turkeys. Anim. Behau. 18,760-761. Schleidt, W . M., and Shaker, M. D. (1973). Stereotypy of a fixed action pattern during ontogeny in Coturnix coturnix coturnix. Z . Tierpsychol. 33, 35-37. Schulman, A. H. (1970). Precocial sexual behaviour in imprinted male turkeys. Anim. Behau. 18,758-759.
Stamps, J. A. (1978). A field study of the ontogeny of social behaviour in the lizard Anolis aeneus. Behaviour 66, 1-32.
322
T. G. G. GROOTHUIS
ten Cate, C. (1984).The influence of social relations on the development of species recognition in zebra finch males. Behauiour 91, 263-285. Terkel, A. S., Moore, C. L., and Beer, C. G. (1976). The effects of testosterone and estrogen on the rate of long-calling vocalization in juvenile laughing gulls (Larus atricilla). Horm. Behav. 7,49-57. Tinbergen. N. (1952). “Derived activities”: Their causation, biological significance, origin and emancipation during evolution. Q. Reu. Biol. 27, 1-37. Tinbergen, N. (1959). Comparative studies on the behaviour of gulls: a progress report. Behauiour 15, 1-17. Tinbergen, N. (1%5). Some recent studies on the evolution of sexual behaviour. I n ”Sex and Behaviour” (F. A. Beach, ed.). pp. 1-34. Wiley, New York. van Rhijn. J. G. (1981). Units of behaviour in the black-headed gull. Larits ridihundus L. Anim. Behau. 29, 586-597. van Rhijn, J. G., and Groothuis, T. (1985). Biparental care and the basis of alternative associations among gulls, with special references to the black-headed gull Lurus ridihrmdus. Ardeu 73, 159-174. Veen, J . (1980). On the significance of the Long-call in the little gull (Larus minutus). Behauiour 100, 33-49. Weidmann, U . (1955). Some reproductive activities of the common gull. Larus Canus. Ardeu 43, 85-132. West, M. J., and King, A. P. (1988). Female visual display affects the development of male song in the cowbird. Nature (London) 334, 244-246. Williams, N . J. (1972).On the ontogeny ofbehaviourofthe cichlid fish Cichlasoma nigrofuciatum (Gunther). Ph.D. thesis, University of Groningen. the Netherlands. Wingfield, J . C. (1984). Environmental and endocrine control of reproduction in the song sparrow. I. Agonistic interactions a s environmental information stimulating secretion of testosterone. Gen. Cump. Endocrinol. 56, 417-424. Wingfield, J . C., Newman, A. L.. Hunt, G. L., and Farner. D. S., (1982). Endocrine aspects of female female pairing in the western gull (Larus occidentalis wymani). Anim. Behuu. 30,9-22. Wurdinger. I. (1970). Erzeugung, Ontogenie, und Function der Lautauserungen bei vier Ganze-arten (Anser indicus, A . caerulescens, A . alhifrons. und Branta canadensis). Z. Tierpsvchol. 27, 257-302. Wyman. R. L.. and Ward, J. A. (1973). The development of behaviour in the cichlid fish Etruplus maculatus (Bloch). Z. Tierpsychol. 33, 461-491. Zann, R. (1975). inter and intra specific variations in the calls of three species of grassfinches. Z. Tierpsychol. 39, 85-125.
Index
A Agelenopsis aperia, 104, see also Behavioral
riparian population deviation from expectation, 1 I2 Evolutionarily Stable Strategies, 119-122 payoff components associated with territorial disputes, 119, 121 strategy representations in territorial disputes, I24 temtorial behavior, 112-1 14 Brood parasitism, 89
phenotypes, evolution bird predation, 112 body mass and reproductive success, 104-105, 108, 110 body temperature, 104, 106 desert grassland, NM, 104-108, 110 potential prey, 114-1 15 riparian area, AZ, 107, 109. I 1 1-1 12 Allopreening, parasitism levels, 81 C Antiparasite adaptations, behavioral, 71-73 Antipredator behavior, 135-227 Chimpanzees, male aggression, 19-23 attainment of sucking position, 249, Choking call, 280-283 251-252 Choking posture, 278-280 effect on lamb behavior, 258-260 Competition-for-attention hypothesis, enemy recognition, see Enemy 155-156 recognition Conspecific lamb movement toward udder and dead, antipredator behavior, 181-183.213 counteracting movements of dam, distressed, antipredator behavior, 245-248 178-181, 213 sensory factors mediating activity of fetus Courtship, male aggression toward potential and newborn, 241-243 mates, 20-21 spiders, 116
D
B Behavior, ecotypic variation, 103 Behavioral phenotypes, evolution, 103-133 anti-predator behavior, 116 correlated traits, 117-1 18 dominance mechanism of inheritance of aggression and fear, 118 experimental manipulation of gene flow versus selection, 128-130 foraging behavior, 113-1 16 gene flow, 126-128 phylogenetic inertia, 123-126
Displays, see Social displays, ontogeny Dominance, parasitism and, 78-79 Dummy, use in enemy recognition, 137-140
E Ectoparasites, transmission, 67 Enemy recognition causal aspects, 137-187, 221-223 competition-for-attention hypothesis, 155- 156 323
324
INDEX
context effect. 173-187 dead conspecific. 181-183. 213 distressed conspecific, 178-181. 213 dummy use, 137-140 eye as stimulus. 150-156 generality of multichannel organization, 170-172 identical change of key stimulus in both predators, 164-165 ineffectiveness of zero value stimuli. 148- I49 law of heterogeneous summation, 161 localized versus diffuse key stimuli, 150- I56 mixtures of heterospecific key stimuli. 162-164 multichannel organization, 160- 172 nest concealment hypothesis, 186-187 novelty, 144-149 plumage patterns. 150-153 predator key stimuli. 150-160 proximity to predator. 179 reciprocal habituation. I71- I72 referential signaling hypothesis, 171 risk hypothesis, 175 selective priming through predator experience. 168-170 social context, 176-178 spatial context, 173-176 staying put, 183-187 stimulus coaction rules. 157-159 stimulus-specific habituation of responses. 166- I68 suddenness, 140-144 supernormal predator key stimuli, 160 territorial context effects on responses, I70 two-channel hypothesis, 161-162 unclassifiable risk hypothesis, 159-160 vigilance increases. 143-144 developmental aspects. 187-221, 223225 acquired predator individual characteristics, 206-207 acquired predator species characteristics. 205-206 avoidance adaptiveness. 195- I% conservation relevance of cultural transmission. 221 deprivation experiments on vertebrates, 190-193
differential habituation. 202-205 enemy recognition learning in absence of predator. 2 19-221 habituation, 200-205 innate enemy recognition evidence. 189- I97 learning by others' interactions with predator. 2 15-2 16 multichannel organization. 197 novelty as epigenetic determinant. 197-200 operational definition of innate information on predators. 187-189 perceiving predators, 208-209 population-specific threat. 195 predator behavior learning. 207-208 pursuit and avoidance behavior learning. 209-2 I 1 rarity principle. 197. 200-202. 224. 226 stimulus pattern as a whole. 189-196 stimulus pattern dissection, 196- 197 tutoring others, 218 Evolutionarily Stable Strategies model, 119-122
F Females anestrous, from other communities, chimpanzee male aggression. 2 1-23 primate, see also Male aggression male aggression costs, 9-1 I . 41-42 mate choice. 13-15 social relationships and alliances. 16-18 victims, 40 Fighting, females subject to male aggression, 11-12, 29 Flocks, mixed-species. parasitism, 76-77 Foraging behavior, spiders. 113-1 16
G Gene flow behavioral phenotype evolution effects, 126- I28 manipulation. behavioral phenotype evolution, 128-130 Group. female primate's choice. 15-16
325
INDEX H Habituation as determinant of antipredator behavior. 200-205 differential, 202-205 stimulus-specific. enemy recognition. 166- I68
I Imitation. social display development. 298-299 Infanticide. male aggression. 9-10 Intersexual selection. parasite infection and, 84-85, 85
L Lambs. newborn. see d s o Sucking. newborn lambs olfactory experience. 242-243 prenatal sound experience, 241-242 Law of heterogeneous summation, 161 Long call, 280-283
M Male aggression. 1-50 against females and infants in nonprimate mammals. 24-28 chimpanzees. 19-23 against females from other communities. 21-23 toward potential mates. 20-21 correlation with increased mating success. 37 costs to females. 9-1 I.41-42 during courtship. 7 frequency against females and contexts of occurrence. 4-5 male infanticide. 9-10 males most likely to show aggression, 40 negative evidence, 42-43 nonhuman primates. 3-9
nonprimate mammals costs of. 29 female counterstrategies. 29-3 I "protest" call. 30. 46 similarities and differences with primates. 31 types. 24. 29 presence or absence o f other males. 40-41 primate female counterstrategies. I I fighting back. 11-12 group choice. 15-16 mate choice. 13-15 sexual activity and reproduction timing. 12-13 social relationships and alliances. 16-18 social system form, 18-19 sequelae. 38-40 similarities and differences between primate and nonprimate mammals, 31 terminology. 8-9 variation in. 31-37 female associations with particular males. 35-36 female coalitions. 34-35 male-male alliances. 36-37 male reliance on female political support. 36 one-male and multimale groups. 35 phylogeny. 33 sexual dimorphism, 33-34 victim females, 40 Male-male contest competition. reproductive consequence. 44-46 Mammals. see Male aggression Mating systems. parasites and, 87-88 Migration. parasitism and. 79-80 Multiple mating, parasites, 88-89
N Nest concealment hypothesis. 186-187 Novelty. as epigenetic determinant of antipredator behavior. 197-200
0 Oblique posture. 280 Optimality models, antipredator behavior. I76
326
INDEX
P
5
Parasite-host coevolution. social behavior, 91-93 Parasites. 65-93 abundance and host sociality. 68-71 antiparasite strategies, 81-83 basic concepts. 65-67
Selective priming, enemy recognition, 168-170 Sex hormones, social display. 291-295 Sexual activity, timing and male aggression. 12-13 Sexual coercion concept, 2-3 examples, 6-8 females mating with lower ranking animals, 6 hypothesis evaluation. 37-43 cost to females, 41-42 male aggression correlation with increased mating success. 37 males most likely to show aggression. 40 negative evidence. 42-43 presence or absence of other males and aggression. 40-41 sequelae of male aggression. 38-40 victim females. 40 implications for sexual selection theory, 43-49 nonhuman primates. 3-9 Sexual dimorphism, sexual selection theory, 47 Sexual selection brood parasitism, 89 intersexual selection. 84-85 intrasexual selection. 85 mating systems. 87-88 multiple mating. 88-89 reproduction timing, 89-90 reproductive synchrony. 90 venereal disease in plants, 85-87 Sexual selection theory long-term male-female associations. 47-49 male dominance rank, 46. 48 male-male contest competition, 44-46. 48 male sexual coercion implications. 43-49 sexual dimorphism, 47 Sheep, see also Sucking, newborn lambs factors affecting dam's behavior after birth. 240-241 shaded underbelly of dam, 248 suckling posture, 248-249 Social behavior, parasite-host coevolution. 91-93
behavioral antiparasite adaptations. 7 1-73 dispersal and migration. 79-80 dominance behavior. 78-79 group dispersion, 77-78 host fitness effects, 66-67 host group size variation. 73-76 intermediate host. 68 intersexual selection of hosts, 84-85 intrasexual selection of hosts. 85 mating systems and. 87-88 mixed-species flocks. 76-77 multiple mating. 88-89 optimal group size. 70. 74-75 proximity of conspecific hosts. 75 reproductive synchrony, 90 risk and social factors. 72-73 seasonal variation in host group size. 75 sexual selection and venereal disease in plants. 85-87 transmission and host density, 67-68 Parasitism brood, 89 reproduction timing. 89-90 Phylogenetic inertia. 123-126 Primates. see t h o Male aggression antiparasite strategies. 83
R Rarity principle. 197. 200-202. 224. 226 Referential signaling hypothesis. 174 Refuges. concealment, 185-186 Reproduction parasite effects. 83-84 timing male aggression and. 12-13 parasitism and. 89-90 Reproductive synchrony. parasites. 90 Risk hypothesis. 175
327
INDEX
Social context. antipredator behavior, 176- 178 Social displays, ontogeny. 269-318 aspects of development. 271-272 change in context. 306-310 change from internal to external factors, 308-309 early motor patterns. 306-307 form development mechanisms. 273-302 adult calls in juvenile testerosteronetreated gulls. 293-295 agonistic behavior and testerosterone. 295 choking call and long call. 280-283 choking posture, 278-280 discontinuities, 284 external stimuli. 288-289 fear behavior. 290-291 -frequency changes and regression, 283-284 hypotheses. 286-287 imitation, 298-299 integration and differentiation, 284-285 matching hypothesis. 294-295 methodological issues. 274-278 motivational state development, 289-296 motor output matching, 296-301 motor pattern classification, 275-278 motor side limitations. 288 oblique posture, 280 ontogeny and phylogeny, 285 practice effects, 296-298 proprioceptive feedback, 286-287 sex hormone effects. 291-293 social deprivation effects, 296-298 social relations, 299-301 form fixation, 302-306 independence of oblique display of testosterone. 304 mechanisms. 304-306 reversal of abnormalities. 302-303 functional aspects of development. 3 10-3 I5 change in context, 314-315 first two weeks of ontogeny. 311-312 form fixation, 314 gradual development in form, 31 1-313 incomplete display performance, 3 13 widening of context of display, 314-315 reason for study, 269-270
summarizing scheme, 315-318 central pattern generator, 3 17 form fixation. 317 incomplete display performance. 3 16 Social reactions, display development, 299-30 I Social system. primates. male aggression. 18-19 Spatial context. antipredator behavior, 173-176 Spiders, see Behavioral phenotypes. evolution Startle response, 140-143 Staying put. antipredator behavior. 183-187 Stimulus coaction rules. 157-159 Stimulus compression. 157-159 Stimulus dilation, 157-158 Sucking, newborn lambs, 239-264 circling by dam and ewe. 260-262 developmental aspects of lamb’s response to touch, 158-160 ewe and lamb behavior until lamb stands, 244-245 lamb response to temperature. 254-255 movement patterns in presucking. sucking. and postsucking phases, 260-262 response to touch. 248-253. 262 teat location. 249-250 dam’s odors and. 257 qualities of ewe which aid in. 254258
T Territorial behavior. spiders, 112-1 14 Two-channel hypothesis, 161-162
U
Unclassifiable risk hypothesis. 159-160
V Venereal disease plants. sexual selection and, 85-87 transmission, 67
Contents of Previous Volumes
Genes and Behavior: An Evolutionary Perspective ALBERT0 OLIVER10
Volume U Pavlovian Conditioning of Signal-Centered Action Patterns and Autonomic Behavior: A Biological Analysis of Function KAREN L. HOLLIS
Suckling Isn’t Feeding, or Is It? A Search for Developmental Continuities W. G. HALL and CHRISTINA L. WILLIAMS
Selective Costs and Benefits in the Evolution of Learning TIMOTHY D. JOHNSTON
Volume 14
Visceral-Somatic Integration in Behavior, Cognition, and “Psychosomatic” Disease BARRY R. KOMISARUK
Group Mating in the Domestic Rat as a Context for Sexual Selection: Consequences for the Analysis of Sexual Behavior and Neuroendocrine Responses MARTHA K. MCCLINTOCK
Language in the Great Apes: A Critical Review CAROLYN A. RISTAU and DONALD ROBBINS
Plasticity and Adaptive Radiation of Dermapteran Parental Behavior: Results and Perspectives MICHEL VANCASSEL
Volume 13 Cooperation-A Biologist’s Dilemma JERRAM L. BROWN
Social Organization of Raiding and Emigrations in Army Ants HOWARD TOPOFF
Determinants of Infant Perception GERALD TERKEWITZ, DAVID J. LEWKOWICZ, and JUDITH M. GARDNER
Learning and Cognition in the Everyday Life of Human Infants HANUS PAPOUSEK and MECHTHILD
Observations of the Evolution and Behavioral Significance of “Sexual Skin” in Female Primates A. F. DIXSON
Ethology and Ecology of Sleep in Monkeys and Apes JAMES R. ANDERSON
Techniques for the Analysis of Social Structure in Animal Societies MARY CORLISS PEARL and STEVEN ROBERT SCHULMAN
Volume 15
PAPOUSEK
Thermal Constraints and Influences on Communication DELBERT D. THIESSEN
Sex Differences in Social Play: The Socialization of Sex Roles MICHAEL J. MEANEY, JANE STEWART, and WILLIAM W. BEATTY
328
INDEX
On the Functions of Play and Its Role in Behavioral Development PAUL MARTIN and T. M. CAR0 Sensory Factors in the Behavioral Ontogeny of Altricial Birds S. N. KHAYUTIN
329
Volume 17
Receptive Competencies of LanguageTrained Animals LOUIS M. HERMAN
Food Storage by Birds and Mammals DAVID F. SHERRY
Self-Generated Experience and the Development of Lateralized Neurobehavioral Organization in Infants GEORGE F. MICHEL
Vocal Affect Signaling: A Comparative Approach KLAUS R. SCHERER
Behavioral Ecology: Theory into Practice NEIL B. METCALFE and PAT MONAGHAN
A Response-CompetitionModel Designed to
Account for the Aversion to Feed on Conspecific Flesh W. J. CARR and DARLENE F. KENNEDY
The Dwarf Mongoose: A Study of Behavior and Social Structure in Relation to Ecology in a Small, Social Carnivore 0. ANNE E. RASA
Volume 16
Ontogenetic Development of Behavior: The Cricket Visual World RAYJOND CAMPAN, GUY BEUGNON, and MICHEL LAMBIN
Sensory Organization of Alimentary Behavior in the Kitten K. V . SHULEIKINA-TURPAEVA
Volume 18
Individual Odors among Mammals: Origins and Functions ZULEYMA TANG HALPIN
Song Learning in Zebra Finches (Tueniopygia gurrara): Progress and Prospects PETER J. B. SLATER. LUCY A. EALES, and N. S. CLAYTON
The Physiology and Ecology of Puberty Modulation by Primer Pheromones JOHN G. VANDENBERGH and DAVID M. COPPOLA Relationships between Social Organization and Behavioral Endocrinology in a Monogamous Mammal C. SUE CARTER, LOWELL L. GETZ, and MARTHA COHEN-PARSONS Lateralization of Learning in Chicks L. J. ROGERS Circannual Rhythms in the Control of Avian Migrations EBERHARD GWINNER
Behavioral Aspects of Sperm Competition in Birds T. R. BIRKHEAD Neural Mechanisms of Perception and Motor Control in a Weakly Electric Fish WALTER HEILIGENBERG Behavioral Adaptations of Aquatic Life in Insects: An Example ANN CLOAREC The Circadian Organization of Behavior: Timekeeping in the Tsetse Fly, A Model System JOHN BRADY
The Economics of Fleeing from Predators R. C. YDENBERG and L. M. DILL
Volume 19
Social Ecology and Behavior of Coyotes MARC BEKOFF and MICHAEL C. WELLS
Polytenitorial Polygyny in the Pied Flycatcher P. V. ALATALO and A. LUNDBERG
330
CONTENTS O F PREVIOUS VOLUMES
Kin Recognition: Problems, Prospects, and the Evolution of Discrimination Systems C. J. BARNARD
The Ergonomics of Worker Behavior in Social Hymenoptera PAUL SCHMID-HEMPEL
Maternal Responsiveness in Humans: Emotional, Cognitive, and Biological Factors CARL M. CORTER and ALISON S. FLEMING
"Microsmatic Humans" Revisited: The Generation and Perception of Chemical Signals BENOIST SCHAAL and RICHARD H. PORTER
The Evolution of Courtship Behavior in Newts and Salamanders T. R. HALLIDAY Ethopharmacology: A Biological Approach to the Study of Drug-Induced Changes in Behavior A. K. DIXON, H. U. FISCH, and K. H. MCALLISTER Additive and Interactive Effects ofGenotype and Maternal Environment PIERRE L. ROUBERTOUX, MARIKA NOSTEN-BERTRAND, and MICHELE CARLIER Mode Selection and Mode Switching in Foraging Animals GENE S. HELFMAN Cricket Neuroethology: Neuronal Basis of Intraspecific Acoustic Communication FRANZ HUBER Some Cognitive Capacities of an African Grey Parrot (Psitfacus erirhacus) IRENE MAXINE PEPPERBERG Volume 20
Social Behavior and Organization in the Macropodoidea PETER J. JARMAN The r Complex: A Story of Genes. Behavior. and Populations SARAH LENINGTON
Lekking in Birds and Mammals: Behavioral and Evolutionary Issues R. HAVEN WILEY
Volume 21
Primate Social Relalionships: 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 Responses to 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 MORALf 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
This Page Intentionally Left Blank
