Myth of the Typical Primate

Transcription

1 YEARBOOK OF PHYSICAL ANTHROPOLOGY 37: (1994) Myth of the Typical Primate KAREN B. STRIER Department of Anthropology, University of Wisconsin-Madison, Madison, Wisconsin KEY WORDS Cercopithecines, Typical primates, Kinship, Dispersal, Aggression, Dominance, Sex, Reproduction ABSTRACT Anthropological interest in nonhuman primates as models for human behavioral evolution has tended to focus on a relatively small number of species. This emphasis, coupled with a search for unifying principles that explain behavior, has led to a widespread perception of the semiterrestrial cercopithecines as typical, and therefore characteristic of most other primates. The prevalence of male-biased dispersal and female philopatry, the use of aggression to establish and maintain hierarchical relationships, and the occurrence of sex for exclusively reproductive purposes have been challenged repeatedly, but the cercopithecine model of primate behavior has nonetheless persisted in much of the anthropological literature. This review incorporates accumulating data on a diversity of primates to examine the myth of the typical primate. The roles of kinship, aggression, and sex in mediating primate social relationships are far less uniform across primates than the myth has implied, raising questions about the generality of models of primate social systems derived from typical primates. Acknowledging existing diversity and encompassing it in more accurate portrayals of primate behavioral ecology requires consideration of the interacting effects of phylogenetic, demographic, ontogenetic, and physiological variables. o 1994 Wiley-Liss, Inc. In the last two decades, a growing number of anthropologists have begun to follow nonhuman primates out of the Old World savannas and woodlands into what remains of the world s tropical forests. Data on species that were once considered peripheral to questions about human behavioral evolution are now challenging many long-standing perceptions of comparative primate behavioral ecology. Yet, mainstream anthropology has been slow to incorporate behavioral findings from these newly studied species into its models. The anthropocentric currents of primatology run deep, and appear to have been resistant to change. Part of this resistance may be rooted in biases dating back to the first primate field studies in the 1930s, when psychologist Robert Yerkes sent his students to investigate the naturalistic behavior of nonhuman primates (Carpenter, 1934). By the mid 1950s, Japanese primatologists, influenced in part by Carpenter s work, and in part by Kinji Imanishi s belief that monkeys resemble human beings more than they resemble other animals (Asquith, 1991:91), initiated field studies on macaques (see Fedigan and Asquith, 1991). Soon afterward, American anthropologists began to focus on other Old World semi-terrestrial monkeys in an effort to understand the social correlates of adaptations to life on the ground (Washburn and DeVore, 1961; Dolhinow, 19721, and paleontologist Louis Leakey promoted field studies on the great apes because of their phylogenetic relatedness to humans. Unlike many anthropologists, primatologists from disciplines such as psychol Wiley-Liss, Inc.

2 234 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 Descriptive, Fig. 1. Waves of primate field studies. ogy and zoology have never limited their research to particular species or geographic areas that were obvious candidates for inferences about human behavioral evolution. For psychologists such as Carpenter, whose pioneering field study was on arboreal, New World howler monkeys, and a number of zoologists, who subsequently developed long-term field studies on arboreal New World and Old World monkeys alike, understanding primate adaptations has been more important than a particular species phylogenetic position or ecological parallel with humans. But, despite the broad interdisciplinary appeal of primates, anthropologists have tended to treat primates as species apart from other animals (Richard, 1981). Only recently, as disciplinary boundaries have blurred, have anthropologists begun to focus on primates as subjects for addressing questions in comparative behavioral ecology rather than as human or hominid analogs (Kinzey, 1986). How accurate are contemporary depictions of primate behavior in the anthropological literature? How do these depictions reflect the shifting perspectives behind primate field studies? What are the consequences of expanding our views of primate behavior by incorporating new data from diverse species into our models? In cultural anthropology, recognition of such diversity has led to relativistic approaches that emphasize the uniqueness of different human societies (Boas, 1973). How can anthropologists retain their search for unifying principles about primate behavior while simultaneously acknowledging the diverse social systems in their study subjects? These fundamental questions have strongly influenced anthropological perspectives of the typical primate, and will be considered in the final section of this review. First, however, it is appropriate to examine the myth of the typical primate within the context of evolving research paradigms. Evidence for much greater variability in primate societies than the myth implies is provided by comparative data on primate social relationships, including kinship, aggression, and sex, and by a brief evaluation of some ecological models of primate social systems. ORIGIN OF THE MYTH Methods and standards, as well as the questions asked in primate field studies, have changed over the years, reflecting a succession of distinct but overlapping waves as disciplinary perspectives have converged (Fig. 1). The first of these waves, from the late 1950s through the 1960s, was basically descriptive, adhering to the anthropological tradition of ethnographic reports and to the zoological tradition of natural histories. These studies were rich in contextual details, but it was difficult to compare descriptions from different studies because there were few common denominators. Many observations from this period (e.g., the importance of coalitions; the prominence of affiliative relationships) clearly anticipated later, more quantitative findings, but their impact was limited by the lack of a uniform methodology and comparative and theoretical framework. In the 1960s and early 1970s, primatologists from all disciplinary backgrounds began to employ systematic methods of behavioral sampling that could facilitate

3 Strier] MYTH OF THE TYPICAL PRIMATE 235 quantitative comparisons both among primates and between primates and other animals (e.g., Hinde, 1973; Altmann, 1974; Dunbar, 1976). The coincidental incorporation and application of evolutionary and ecological theories, including sociobiology and optimality models, further standardized the types of quantitative data that were collected (Richard, 1981). Consequently, by the mid 1970s, the second wave of primate field studies had become increasingly focused on specific questions pertaining to the functional, or evolutionary, significance of behavior. By the early 1980s, the availability of comparative data from enough different species permitted the development of general explanatory models relating ecological variables, such as food distribution and predation pressure, to social variables, such as group size and mating systems (e.g., Wrangham, 1980; van Schaik and van Hooff, 1983; Terborgh and Janson, 1986). The antecedents of these models were based on early correlations between ecological, morphological, and behavioral traits in primates (e.g., Hall and DeVore, 1965; Crook and Gartlan, 1966; Eisenberg et al., 1972; Clutton-Brock and Harvey, 1977) and comparative behavioral ecological analyses of bats (Bradbury and Verhencamp, 19771, birds (Emlen and Oring, 1977), and mammals (Crook et al., 1976). Primatologists of the 1980s took the predictions generated by these evolutionary ecological models into what became the third wave of field studies. Predictions could be tested through diachronic analyses on a few well-studied species, such as macaques, baboons, and chimpanzees, and through synchronic analyses on species that had not been studied previously, or had been studied only cursorily and were included in the general models incorrectly. At the same time, research on diverse species was facilitated by changing global politics that made many primate habitat countries, and the diverse primates in them, more accessible to foreign researchers. The results of third wave efforts to test synthetic models of primate behavioral ecology have been mixed. Some ecological generalizations, such as that predicting a relationship between food patch size and feeding group size, have been supported in various studies of Atelines and apes, which exhibit more flexible grouping patterns than most other primates (e.g., Leighton and Leighton, 1982; Chapman, 1988; Symington, 1988a; White and Wrangham, 1988; Strier, 1989). Others, such as that between body size and diet, have not fared so well against comparative data from New World monkeys (Ford and Davis, 1992; Strier, 1992a) and lemurs (Richard and Dewar, 1991). A number of other behavioral generalizations, particularly those pertaining to dispersal and kinship, dominance relations and aggression, and sex and reproduction, were also challenged. Today, generalizations in these fundamental areas of primate sociality are confounded by exceptions, meriting a closer look at the contradictory observations permeating the field. The 1990s signal the beginning of a fourth wave of primate field studies. Methodologically, the fourth wave is already distinguished by the development of noninvasive tools including DNA analyses from hair follicles and buccal cells obtained from discarded food wadges (Higuchi et al., 1988; Li et al., 1988; Takasaki and Takenaka, 1991; Morin et al., 1993; Takenaka et al., 1993) and fecal steroid assays (Wasser et al., 1988; Strier and Ziegler, 1994). These methods not only permit an integration of what have become standardized methods of behavioral sampling with new insights into genetic and physiological processes, but they have also followed the lead of captive primate studies in extending the interdisciplinary nature of field primatology beyond the behavioral sciences. Theoretically, contemporary studies have also begun to explore some of the inconsistencies that emerged from third wave models by focusing on distinctions between intra- and intergroup dynamics (e.g., van Schaik, 1989; Isbell, 1991; Cheney, 1992; van Hooff and van Schaik, 1992; Strier, 1994), and on a revived interest in ontogenetic, demographic, and phylogenetic variables (e.g., Altmann and Altmann, 1979; Dunbar, 1979; Snowdon, 1990a; Fleagle, 1992; DiFiore and Rendall, 1993). It is not yet clear, however, whether more comprehensive comparative models will be robust enough to encompass these new perspectives and escape from established perceptions of the typical primate.

4 236 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 The typical primate? It is only natural that three of the longest and best-studied primate taxa, the baboons, macaques, and chimpanzees, figure prominently in portrayals of primate social behavior. But it is also the case that underlying assumptions about the relevance of these primates to human behavioral evolution have contributed to their prominence in the anthropological literature. While such simplification may be acceptable in an introductory curriculum, it is disturbing to discover how frequently it is carried over into more technical articles and books that review existing knowledge. The fact that baboons, macaques, and chimpanzees differ in many fundamental respects both from one another, and from within the genera, further illustrates the arbitrary processes behind such conservative referential approaches (Fedigan, 1982; Tooby and DeVore, 1987). Savanna-dwelling baboons, like rhesus and Japanese macaques, live in multimale, multifemale polygamous troops. The troops are cohesive, and comprise related matrilines with male-biased dispersal. Males and females are highly dimorphic in both body and canine size; larger males equipped with more elaborate weaponry are individually dominant over females. Dominance hierarchies are relatively stable among females because young females inherit the ranks of their mothers. Among males, however, dominance relationships are routinely challenged and reigning alpha males are regularly overthrown by successors. Dominance hierarchies, and the aggressive interactions that reflect and lead to hierarchical relationships, together with affiliative interactions, such as grooming and coalitions among kin, form the basis of baboon society. Relationships among related females are more stable than those among unrelated males, and savanna baboons have come to represent the typical, female-bonded primates (Wrangham, 1980). Chimpanzees superficially resemble savanna baboons in their multimale, multifemale polygamous societies and in the highly visible sexual swellings that signal female reproductive condition, but they are markedly different in nearly every other respect. Chimpanzee parties are fluid, with heterosexual aggregations occurring only when large patches of preferred fruits are available. In contrast to baboons, chimpanzee communities comprise related males with female-biased dispersal (Morin, 1993). The strongest associations, beyond those between mothers and their offspring, exist among males. Males compete amongst themselves for dominance status, but males also cooperate with one another in intercommunity aggression. Females appear to have weak dominance relations, although the degree to which they associate with one another is highly variable between populations. The pronounced differences between the multimale, multifemale polygamous societies of savanna baboons and chimpanzees also demonstrate the limitations of relying on superficial characteristics such as group composition to generalize about social dynamics. Indeed, these differences have been used to justify distinctions between chimpanzees, as exceptional primates, and savanna baboons and other well-studied, female-bonded cercopithecines, as more typical primates. Yet, even among the ecologically similar semiterrestrial cercopithecines, such as baboons, vervet monkeys, patas monkeys, and macaque species, social relationships differ markedly (e.g., Cheney and Seyfarth, 1983; Harding and Olson, 1986; Rowel1 and Chism, 1986; de Waal and Luttrell, 1989). Similarly, there are significant differences in the societies of common chimpanzees and the closely related bonobos (Furuichi, 1989; Ihobe, 1992). When data from an even wider variety of species, particularly the Malagasy lemurs and the New World monkeys, are considered, it becomes apparent that many behavioral traits shared among the cercopithecines are actually unique to them. The diversity of social systems now known to exist across primates leaves the status of baboons and macaques as typical primates in a highly dubious state.

5 Strier] MYTH OF THE TYPICAL PRIMATE 237 Deconstructing a myth The myth of the cercopithecine model of a typical primate is based on at least three erroneous but persistent assumptions. First, male dispersal and female philopatry continue to be described as the pattern that characterizes the primates as well as other mammals (Greenwood, 1980; Pusey, 1987). Chimpanzees and bonobos, along with a few other species (red colobus, hamadryas baboons, and howler monkeys), have long been regarded as exceptions to this pattern, but the number of exceptional cases has increased in recent years, challenging the assumptions that a typical primate dispersal pattern exists (see Moore, 1984, 1992). Second, early emphasis on the use of aggressive competition to mediate primate social relationships has prevailed despite repeated efforts to demonstrate the limitations of such arguments (Rowell, 1974; de Waal, 1989a,b; Silverberg and Gray, 1992). Is the absence of strong dominance hierarchies and overt aggressive interactions in many atypical primates due to the failure of observers to detect their occurrence, or is it the case that these behavioral systems are less uniformly prevalent across primates than among the cercopithecines? When other variables, such as the relationship between male-male competition and female mate choice and distinctions between intra- and intergroup aggression and affiliation, are examined, the primacy of aggressive competition even among cercopithecines becomes less obvious. Simultaneously, greater attention has been paid to the importance of coalitions and reconciliations (de Waal, 1986, 1989a) and other more subtle, nonaggressive forms of competition including sperm competition in male chimpanzees (Harcourt et al., 19811, muriquis (Milton, 1985a; Strier, 1992b,c), and savanna baboons and rhesus macaques (Bercovitch, 1992), and ovulatory inhibition (Wasser and Barash, 1983) in female talapoin monkeys (Bowman et al., 1978), gelada baboons (Dunbar, 1980, 19841, and callitrichids (Abbott, 1989). When viewed collectively, these alternatives suggest that a typical primate competitive strategy does not occur. Finally, the link between sex and reproduction in nonhuman primates has endured despite the fact that it was effectively debated more than a decade ago (Hrdy, 1981). Clarification of the relationship between sex and reproduction has been elusive because of the difficulties inherent in inferring reproductive success from mating success (reviewed by Gray, 1985); it is an important relationship to clarify, nonetheless, because one of the purported benefits of sociality is the opportunity to enhance reproductive success and inclusive fitness. Yet, if reproduction is only one of the functions of sex in nonhuman as well as human primates, then by extension we must reconsider the suggestion that social structures and mating systems are not the same things (Cords, 1987:107; see also Melnick et al., 1984; Richard, 1985a; and review in Moore, 1992). The prevalence of female matings with extragroup males in Barbary and Japanese macaques (Mehlman, 1986; Small, 1990; Sprague, 1992) as well as several other primates (e.g., lemurs: Richard, 1985a; Richard and Dewar, 1991; Sussman, 1992; patas monkeys: Harding and Olson, 1986; Rowell and Chism, 1986; forest guenons: Cords, 1987; muriquis: Strier et al., 1993; Strier, 1994) may have profound consequences for the ways in which the function of primate social systems have traditionally been modeled from ecological and evolutionary principles. Questions about the generality of female philopatry, aggression, and sex for exclusively reproductive purposes were raised years ago and in some cases, repeatedly, in both empirical and theoretical publications. But, the strength of the typical primate model has overpowered the impact that many of these original challenges have had on the field (e.g., Glezer and Kinzey, 1993; Janson, 1993; Snowdon, 1993). With more abundant data on newly studied species, on species that have long been in the literature but are only now beginning to yield longitudinal data, and the ongoing accumulation of data from well-studied species, it is no

6 238 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 longer possible to accept the myth of the typical primate uncritically, or to generalize from baboons and macaques, which are themselves highly variable (de Waal and Luttrell, 19891, to most other primates. SOCIAL RELATIONSHIPS Dispersal and kinship Theoretical obsessions Kinship has occupied a central position in efforts to understand primate social relations and social systems during the methodological and theoretical waves that have swept primatology. Part of this tenacity may be attributed to the tradition in social anthropology in which kinship, whether biologically or culturally defined, has been viewed as a ubiquitous organizing principle in human societies (Sade, 1991; Quiatt and Reynolds, 1993). With the adoption and application of evolutionary theory in primatology, the importance of biological kinship was further elevated. Kin selection and inclusive fitness theory were invoked to explain seemingly altruistic acts that ran contrary to what selfish individuals should be selected to do (Hamilton, 1964). Consequently, knowledge of the genetic relatedness between individuals has become critical to interpretations of primate social relations, In many cases, however, such knowledge remains largely inferential. Evolutionary theory permits the formulation of predictions about how different individuals should behave toward one another and about why interindividual relationships may vary. Because individuals share a greater proportion of their genes with kin than with nonkin, selection pressures should favor beneficent behavior toward kin as long as the genetic benefits through inclusive fitness outweigh the costs to individual fitness. Armed with this theoretical model, primatologists could both describe and explain the occurrence of nepotistic behavior among their study subjects. Efforts to discriminate between beneficent and selfish behavior have produced many detailed analyses of social relations that confirmed and advanced the theoretical predictions. For example, Kurland (1977) found that female Japanese macaques spent more time in proximity, grooming, and in agonistic interactions with kin than with nonkin, and that among kin, the degree of relatedness was positively correlated with higher frequencies of interaction among close relatives. Yet, while proximity and grooming were expected to be stronger among kin than nonkin, agonistic interactions were expected to be less frequent. These incongruent results were reconciled with kin selection theory in a second level of analysis: when the frequency of agonistic interactions was calculated relative to the frequency of proximity between dyads, aggression between kin was proportionately less frequent than expected from the time they spent in proximity. Similarly, Seyfarth and Cheney (1984) observed that vervet monkeys were more likely to assist kin than nonkin, unless nonkin had recently groomed one another. These findings were interpreted by combining the predictions of both kin selection and reciprocal altruism, another powerful sociobiological principle ( rivers, 1971). Such conclusions, and the analyses that predicated them, could not have been reached prior to the adoption of systematic, quantitative methods of behavioral observation. Similarly, biological relatedness among primates could not have been determined without the accumulated data from long-term studies in which identified mothers could be associated with identified offspring. As successive offspring matured, maternal relatedness among siblings and ultimately, adults, could be calculated. However, kinship through the paternal lineage, particularly but not exclusively in polygamous primates, continues to elude the most exacting observational regimes. Indeed, despite some claims that the increased focus on female primates was introduced by feminist primatologists in the 1970s (Haraway, 1989), the importance of female kin groups had already been recognized in the long-term studies of the Arashiyama Japanese macaques (Fedigan and Asquith, 1991). It is possible that these renewed emphases on female primates were a consequence of

7 Strier] MYTH OF THE TYPICAL PRIMATE 239 the coincidental emergence of kin selection theory and its requisite documentation of genetic relatedness, which could only be accurate for females. Female-bonded primates: A cercopithecine phenomenon? Accumulating knowledge of female kinship relations among the Old World cercopithecines permitted primatologists to understand some of the complexities of these primates societies. Hierarchically ranked females in matrilines interact with hierarchically ranked females in other matrilines; troops fission along matrilines; and members of matrilines ally themselves against other matrilines and against unrelated males (Kawai, 1965; Samuels et al., 1987; Cheney, 1992; reviewed in Quiatt and Reynolds, 1993). Thus, the influence of females in their own groups, in intergroup dynamics, and in terms of male group membership and mating success has been widely documented (Hrdy, 1981; Smuts, 1987). Furthermore, the primacy of the mother-daughter bond came to represent more than a descriptive element of primate socialization practices because it was embedded in a larger social and kinship network involving other mother-daughter bonds (Nicolson, 1991). If one sex is philopatric, then, according to traditional views pertaining to inbreeding avoidance, the other sex presumably must disperse (Packer, l975,1979a, 1985; Greenwood, 1980). Knowledge of dispersal patterns was thus thought to provide indirect insights into the kinship structure of a group. And, because determining kinship lineages remains impractical in short-term studies of slowmaturing species such as primates, documenting sex-biased dispersal has become a widely employed shortcut for inferring sex-biased philopatry and kinship within groups. However, as Moore (1984, 1992) has repeatedly argued, coupling malebiased dispersal and female-biased kinship is misguided for two essential reasons. First, although routine dispersal by both sexes is limited to a relatively small number of primates, there are numerous reports of occasional dispersal by females in primates with male-biased dispersal systems, and by males in primates with female-biased dispersal. Even a low proportion of dispersal events can have profound implications for relatedness among group members because of the relatively small size of most primate groups and because of the relatively long lifespan of most primates (Chepko-Sade et al., 1987). Second, there is debate over whether inbreeding avoidance is, in fact, the primary force for sex-biased dispersal systems in primates (Moore, 1984; Moore and Ali, 1984; but see Pusey and Packer, 1987). Without a thorough understanding of what constitutes negligible levels of sexbiased dispersal and why dispersal occurs at all, the behavioral significance of philopatry remains obscure. Inferences about nepotistic behavior based on the male-biased dispersal and female philopatry found in many cercopithecine primates are further confounded when accumulating data from a more diverse set of species are considered (Fig. 2). Among the cercopithecoids, dispersal tends to be less biased toward males among the colobines than among the cercopithecines (McKenna, 1979; Moore, 19841, and even among congeneric cercopithecines, such as the macaques, there is extensive variability in the degree of male-biased dispersal (Moore, 1984, 1992). When the comparison is extended to include other anthropoids, it is evident that none of the hominoids exhibit this pattern, and among the New World monkeys, only some capuchin monkeys adhere to it. Male-biased dispersal and female philopatry is not a typical primate pattern; at most it is a pattern among the prosimians (Richard and Dewar, 1991; Kappeler and Ganzhorn, 1993) and the cercopithecines. Yet, it has persisted in being the default expectation (Moore, 1992:369) in primates, despite the fact that examples in which females disperse and males remain in their natal groups are found across all haplorhine families except cercopithecines. These include chimpanzees (Goodall, 1986; Nishida et al., 1990), red colobus (Struhsaker, 1975; Marsh, 19791, spider monkeys (Symington, 1988b), woolly monkeys (Nishimura, 1990), muriquis (Strier, 1991a), and Costa Rican (but not Peruvian) squirrel monkeys (Boinski,

8 240 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 Dispersal Patterns in Anthropoid Primates 6 5 Male-biased Both Female-biased 2 4 al E d r 0 3 L a, n 5 2 z 1 0 I I c I I I I Cercopithecines Colobines Apes New World Monkeys Papio Colobus Pan Cebus Macaca Nasalis Gorilla Alouatta Theropithecus Presbytis Pongo Saimiri Erythrocebus Pygathrix Lagothrix Cercopithecus Ateles Brachyteles Fig. 2. Dispersal patterns in anthropoid primates. Sources from Moore (1984, 19921, Pusey and Packer (19871, and Strier (1990). 1987; Mitchell et al., 1991). These examples do not refute the claim that kinship can be a powerful organizing principle of social relations in some primates. Rather, they imply that in a number of primates, kin-biased behavior may be evident among males rather than females. More compelling, however, is the growing number of examples in which both sexes disperse from their natal groups. These include members from all haplorhine taxa representing a diverse array of social systems, such as, but not limited to, gibbons (Leighton, 19871, mountain gorillas (Harcourt, 1978; Stewart and Harcourt, 1987), hamadryas baboons (Abegglen, 1984; Phillips-Conroy et al., 1992), proboscis monkeys (Bennett and Sebastian, 19881, howler monkeys (Glander, 1980, 1992; Crockett and Eisenberg, 1987; Crockett and Pope, 19931, and marmosets and tamarins (Sussman and Garber, 1987). Even when comparisons are restricted to just the polygynous or polygamous genera, fully 50% exhibit dispersal by both sexes (Fig. 2). This widespread phenomenon severely challenges the assumption that kinship is an ubiquitous organizing principle in all primate societies. Implications for understanding primate societies Why is there such variation in dispersal patterns across haplorhine primates, and what are the implications for interpretations of social behavior when dispersal

9 Strier] MYTH OF THE TYPICAL PRIMATE 241 by both sexes might preclude the occurrence of strong kinship among members of some primate groups? Efforts to decipher why any primate disperses from its natal group remain highly speculative due to difficulties in distinguishing between alternative mechanisms such as inbreeding avoidance, expulsion due to resource competition by same-sexed group members, avoidance of resource competition with kin, and the search for greater reproductive opportunities elsewhere (Greenwood, 1980; Moore, 1984; Moore and Ali, 1984; Packer, 1985; Pusey and Packer, 1987). The preponderance of similar dispersal patterns within taxonomic groups, such as male-biased dispersal in the prosimians and cercopithecines, female-biased dispersal in the New World atelins, and dispersal by both sexes in most apes and other ceboids, has led to the proposition that dispersal systems may have phylogenetic, as well as ecological or reproductive, components that correspond to primate evolutionary histories (Strier, 1990; Kappeler and Ganzhorn, 1993). In the absence of obvious and robust explanations for why sex-biased dispersal occurs in some primates, it may be useful to rephrase the question from why a primate might disperse to why primates might benefit by staying with their kin. Ecological models have suggested that female philopatry should only occur when food resources are distributed in such a way that females benefit by having related allies available to cooperate in defending food from other groups of related females (Wrangham, 1980; van Schaik, 1989) or in avoiding predators (van Schaik and van Hooff, 1983). According to these models, females should disperse only when the costs of competing with female kin for food or reproductive opportunities outweigh the benefits derived from cooperative resource or predator defense (Wrangham, 1982). Social models have also postulated that female philopatry should be favored when females require reliable allies to protect themselves from aggression from larger, more individually dominant males (Dunbar, 1984; Smuts, 1987; Strier, 1990; Smuts and Smuts, 19931, just as male philopatry is thought to facilitate cooperation among male chimpanzees and spider monkeys in defending community females from other groups of related males (Goodall, 1986; Symington, 1990). Comparative models developed in birds (Emlen and Vehrencamp, 1983) and bats (Bradbury and Verhencamp, 1977) support the hypothesis that the occurrence and patterning of sex-biased dispersal and philopatry in nonhuman primates is an outcome of the compromise between intra- versus intergroup competition, whether it is for food resources or protection in the case of females or for female resources in the case of males (Wrangham, 1980,1982; Moore, 1984; van Schaik, 1989; Isbell, 1991; Cheney, 1992; van Hooff and van Schaik, 1992). The evidence for greater diversity in patterns of dispersal and philopatry across the primates has not diminished interest in the importance of kinship. Rather, it has led to increasing efforts to understand the determinants and behavioral and genetic consequences of sex-biased philopatry when it occurs. From the perspective of population genetics, sex-biased dispersal should lead to greater homogeneity within the philopatric sex than within the dispersing sex, and groups in which one sex is philopatric should be more genetically homogeneous than groups in which both sexes disperse (Gouzoules, 1984; Chepko-Sade, et al., 1987). Until recently, however, there has been little concern for the fate of emigrants (but see Glander, 1992; Crockett and Pope, 1993), in part because many long-term field studies have focused on single study groups instead of local populations. Indeed, the tendency to assume that disappearances from a study group represented dispersal, without confirmation that missing individuals had, in fact, immigrated into other groups, has had a significant impact on how quantitative and anecdotal dispersal data have been interpreted (Moore, 1984). In the few studies in which local populations, rather than single study groups, have been monitored, a number of confounding findings have begun to emerge. First, many individuals which leave their natal groups, whether male or female, experience a long delay before they succeed in immigrating into other groups. In marked Costa Rican mantled howler monkeys, where 79% of males and 96% of

10 242 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 females dispersed from their natal groups, males maintained solitary lives for up to 4 years and females for up to 1 year (Glander, 1992). In Venezuelan red howler monkeys, extratroop individuals accounted for 6-9% of approximately 500 censused animals (Crockett and Pope, 1993). Second, if dispersing individuals leave their natal groups together, and subsequently join the same group, or establish their own group, then the average relatedness in the new groups may be comparable to or greater than the relatedness in groups comprising philopatric individuals (Moore, 1992). Male vervet monkeys often transfer to the same groups as those that males from their natal groups have previously joined, presumably for allies (Cheney and Seyfarth, 1983). Male ringtailed lemurs generally disperse in cohorts, possibly for protection against predators, but may respond to unfavorable sex ratios in their new groups by subsequent emigrations (Sussman, 1992). Related red howler monkey males that emigrate together achieve longer tenures than unrelated males in multimale troops, although mating opportunities may differ depending on their relative ages (Crockett and Pope, 1993). Finally, the absence of genetic paternity data from most field studies means that estimates of relatedness are limited to matrilines. Genetic relatedness within groups and within populations will be higher if some males father a disproportionate number of offspring (e.g., Pope, 19901, if dispersal is strongly sex-biased and males tend to migrate to the natal groups of their fathers (Kuester et al., 1992), or if stochastic demographic processes result in skewed infant sex ratios that ultimately affect dispersal patterns and adult sex ratios of groups (Dunbar, 1979, 1984). Variation in the degree of relatedness within primate groups necessitates a reevaluation of the consequences of kinship for predicting social relations. While kinship may facilitate cooperation between individuals, it is not a necessary condition for the formation of cooperative alliances (Kummer, 1978; Wrangham, 1982). Even among typical cercopithecine primates, long-term coalitions have been observed between unrelated individuals that benefit from cooperation either immediately due to mutualism, or over the long-term due to reciprocity (e.g., Packer, ; Smuts and Watanabe, 1990). It is likely that familiarity and reliability are the mechanisms by which primates evaluate potential allies; familiarity with kin, or long-term coresidence with unrelated individuals, may be similarly effective in promoting reciprocal alliances (Kummer, 1978; Gouzoules, 1984; Small, 1993). Kinship does not always lead to the expression of cooperation among related individuals. Among the three atelin genera, for example, there are pronounced differences in the degree of cooperation between philopatric males. In both spider monkeys and muriquis, male kin cooperate in intergroup contests over access to females (Fedigan and Baxter, 1984; Symington, 1990; Strier, 1992c; Strier et al., 1993). In woolly monkeys, by contrast, there is no evidence of cooperation among male kin (Nishimura, 19901, probably because greater cohesion among females and more parous adult sex ratios reduce intergroup competition among males or mates (Strier, 1994; see below). Similarly, there is no evidence of cooperation among philopatric female lemurs (Kappeler and Ganzhorn, 1993). It is equally difficult to make broad inferences about social relationships, even among primates exhibiting similar patterns of dispersal and philopatry. Kinship may be associated with stable hierarchical relationships among female baboons and macaques, unstable hierarchical relationships among male chimpanzees, or egalitarian relationships among male muriquis and bonobos. Variability in these features of primate societies deviate from expectations based on typical primates. Thus, just as there is evidently a need to reassess the assumptions inherent in traditional perceptions of kinship and dispersal systems in primates, there is also a need to reassess the assumption that primate social relationships are organized around hierarchies mediated by aggressive competition.

11 Strier] MYTH OF THE TYPICAL PRIMATE 243 Dominance, aggression, and competition Theoretical origins The widely held premise that aggressive competition is a central component of primate social relationships owes its origins to the visible drama of displays of aggression and to a preoccupation with the origins of human warfare and aggression during the years following World War I1 when primate field studies were gaining momentum (de Waal, 1992; Silverberg and Gray, 1992). Early field primatologists devoted considerable efforts to developing ethograms for aggressive and submissive behaviors, and to constructing dominance hierarchies based on consistent aggressive interactions between winners and losers. The typical primate society was characterized as one in which group members could be linearly ranked, both individually, based on the outcome of dyadic interactions, and dependently, based on the outcome of interactions involving coalition partners (De Vore, 1963). In these typical primates, adult males are larger than females in both body size and canine size, and are individually dominant over them. Males and females each vie aggressively amongst themselves for status within their respective hierarchies, although aggression among females was considered more subtle and less likely to escalate into canine-flashing fights that might injure themselves or their infants (Smuts, 1987). The more egalitarian societies and lower levels of sexual dimorphism in chimpanzees and bonobos set them closer to the egalitarian nature of human hunter-gatherers than to the hierarchical typical primates, further justifying the distinction of these apes as exceptional among nonhuman primates. Yet, aggressive competition among related males is even rarer in bonobos than in common chimps (Ihobe, 1992), suggesting that even exceptions to the typical primate patten are themselves deviant. The discovery of a striking degree of variability in dominance styles among different macaque species further illustrates how comparative data have undermined the assumption of a typical cercopithecine primate from within (de Waal and Luttrell, 1989). Functional explanations for aggressive competition have focused on the importance of obtaining priority of access to limited resources that affect reproductive success (Bernstein, 1981). These critical resources should differ for males and females because of fundamental biological sex differences (Clutton-Brock and Harvey, 1978; Wrangham, 1979, 1982). In primates, as in other mammals, female reproductive success is constrained by the time and energetic demands of gestation and lactation, which are affected by nutritional condition. Data from captive and field studies alike indicate that better-fed females begin reproducing at an earlier age, produce healthier offspring, have shorter interbirth intervals, and live longer to reproduce (Dittus, 1979; Mori, 1979; Small, 1981; Whitten, 1984). Thus, the most pervasive resource limiting female reproductive success is food, particularly high quality, high energy food, and females should compete with one another for access to the best food and feeding sites. Male reproductive success, by contrast, is constrained primarily by access to fertile females, whose inherently greater investment in reproduction via gestation and lactation is limiting to males (Rivers, 1972). Consequently, males should compete with one another for access to mates. The frequency and intensity of aggressive competition should vary both interand intraspecifically according to diet and to seasonal and annual fluctuations in food availability for females (McKenna, 1979) and to the number of receptive females and the degree of female reproductive synchrony for males (see below). Frugivorous female primates should compete more than folivores for access to their higher quality, more sparsely distributed fruits, and in general, females should be more competitive when preferred foods are scarce. In many species, however, female behavior may not be entirely consonant with these generalized predictions. In the frugivorous spider monkeys and chimpanzees, for example, females rarely compete overtly with one another for access to food, and females avoid feeding

12 244 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 Competition by avoiding one another unless large patches of fruit are available. Thus, rather than leading to aggressive relations among females, the high costs associated with direct competition apparently favor fluid, fission-fusion patterns of association that minimize opportunities for direct contests in these frugivores (Klein and Klein, 1977; Wrangham and Smuts, 1980; Chapman, 1988; Symington, 1990; but see Chapman and LeFebvre, 1990). Conversely, although leaves and other herbaceous vegetation may be more widely available than fruit, there are differences in the quality of these abundant foods (Glander, 1978). These qualitative differences should lead to competition between females for access to the highest quality items (Watts, 1985). Yet, aggressive contests for these foods may be inhibited by the energetic limitations associated with a low-energy diet (Milton, 1984). Polygynous males should compete more than monogamous males due to a greater variance in reproductive opportunities, and among polygynous primates, competition between males should be greater when female reproduction is asynchronous rather than synchronous. However, efforts to identify a positive relationship between male dominance rank and reproductive success have met with only limited success for at least three interrelated reasons. First, it has become increasingly evident that inferring male reproductive success from observed mating success or copulatory frequency is inappropriate (Hausfater, 1975). Data from studies on a diversity of primates reveal that a substantial proportion of matings occur at times in a female s cycle when she is not ovulating, and therefore not likely to conceive (reviewed in Martin, 1992). Differences in sperm quantity and quality may also lead to variation in male fertilization success (Smith, 1984; Parker et al., 1990; Curtsinger, 19911, further confounding the accuracy of inferences about male reproductive success from mating success. Paternity tests are ultimately necessary to establish how male mating behavior corresponds to male reproductive success because all copulations are not equally responsible for conceptions. Similarly, more detailed knowledge of female reproductive biology is necessary to evaluate the diverse relationships between sex and reproduction (see below). Closer scrutiny of male dominance relationships has also revealed that hierarchies constructed from the cumulative outcomes of dyadic interactions do not necessarily reflect dominance relationships among males in particular contexts. A male may routinely submit to others at feeding or resting sites, but nonetheless consistently win contests over access to sexually receptive females (Popp and De- Vore, 1979). Even when the outcomes of aggressive interactions between males are differentiated by the contexts in which they occur, a male s position in the hierarchy changes repeatedly throughout his lifetime in response to shifts in his competitive ability, opportunities for establishing reliable coalitions with other males, and demographic factors that may alter the competitive pressures he faces (Hausfater, 1975). Accurate measures of male lifetime reproductive success are essential to evaluating the effects of male rank, yet such measures are difficult to calculate even with paternity tests because primate lifespans may exceed researchers careers. A final confounding factor involves the growing recognition that in many species, males may employ subtle, nonaggressive forms of competition to secure fertilizations. The effectiveness of these alternative strategies, which include winning female mate choice (Strum, 1982; Smuts, 19851, manipulation of coalitions and alliances with females and other males (Packer, , and sperm competition (Harcourt et al., 1981; Smith, 19841, may be independent of or inversely related to a male s ability to compete aggressively (Popp and DeVore, 1979). Females also engage in subtle forms of competition, including their preference for mating with particular males that may provide resources or protection for themselves and their infants (Smuts, 1985, 1987), the manipulation of coalitions and alliances with other females as well as males (Kummer, 1967; Hrdy, 1981), and in some species, through pheromonal and/or behavioral inhibition of ovulation in other females (Wasser and Barash, 1983; Dunbar, 1984; Abbott, 1989). The use of nonaggressive competitive strategies may reflect the high costs of

13 Strier] MYTH OF THE TYPICAL PRIMATE 245 direct contests between individuals, particularly when the benefits of cooperation in between-group competition inhibit the expression of aggression among members of the same groups (Vehrencamp, 1983; Wrangham, 1980; van Schaik, 1989; van Hooff and van Schaik, 1992; Strier, 1992b, 1994). Thus, most primate social dynamics can be interpreted as a set of compromises between divisive intragroup competition and the benefits of cooperation among group members during intergroup competition, whether among females over food or among males over mates, and in terms of the value of social partners (Kummer, 1978; de Waal, ). Consequently, the relative importance of aggressive and nonaggressive tactics is expected to vary both intra- and interspecifically with ecological and demographic variables (Wrangham, 1982; van Schaik, 1989; van Hooff and van Schaik, 1992). The costs of aggressive tactics may also vary among species and among individuals. For example, the risks of fighting may be greater for large bodied primates in arboreal habitats than in the terrestrial ones occupied by most typical primates (Strier, 1992b). Similarly, while males in their reproductive prime may be more able, and therefore more willing, participants in aggressive competition (Popp and DeVore, 1979), females may be more willing to risk injury toward the end of their reproductive careers (Hrdy, 1981). Thus, habitat and individual life histories, as well as population density and diet, affect the expression of aggression and alternatives to aggression across primates. Because nonaggressive competitive strategies are often quite subtle, they were not as obvious to early primatologists. Recent data from longitudinal studies of both typical and atypical primates demonstrate that broad generalizations about the importance of dominance and aggression are as species- and context-specific as those between dispersal and nepotism. Aggressive competition, like kinship, continues to be one of the ways in which the social relations of some primates can be understood. However, social skills and the ability to manipulate the behavior and in some instances, the physiology, of competitors may be equally important to characterizing primate social relationships. In their social interactions and social relationships, primates are proving to be more diverse both within and between species than implied by the myth of the typical primate. Female-female dynamics Nearly all cercopithecine primates living in matrilineal societies associate in cohesive groups. Females form the core of these groups, whether they are multimale or single-male. Female membership in these groups is stable, and female hierarchical relationships are usually, but not always, influenced by inherited rank reinforced by coalition support (Walters, 1980; Altmann et al., 1985; Chapais, 1985; Hausfater et al., 1987; Mori et al., 1989; also in female-bonded capuchins: O Brien and Robinson, 1993). Wrangham (1980) linked female cohesive kin groups, stable affiliative relationships, and relatively stable (compared to males ) hierarchical relationships to the advantages of cooperation in intragroup feeding competition (Fig. 3). According to this model of female-bonded primates, females benefit by stable, kin-mediated relations when the advantages of cooperation in intergroup feeding competition outweigh the costs of intragroup feeding competition. If competition among group members is greater than that between groups, females should avoid competing with their kin by dispersing (Wrangham, 1982). Extreme examples of avoiding such high intragroup interference competition may result in the female dispersal and fluid grouping patterns found in common chimpanzees and spider monkeys. Female dispersal in muriquis, however, cannot be explained by high intragroup feeding competition because muriquis feed at large patches of preferred fruit, consume substantial quantities of abundant leaves when fruit is scarce, and do not compete directly for food or feeding sites (Strier, 1989, 1991b). The proximate or phylogenetic causes of female dispersal remain undocumented in each of these species. van Schaik (1989) further extended the distinctions between intra- and intergroup competition for categorizing female primates by distinguishing between

14 246 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 WRANGHAM S ( MODEL OF FEMALE-BONDED PRIMATE GROUPS FOOD DISTRIBUTION, Preferred foods not patchy or defendable - OR occur in small patches Preferred foods occur in large, defendable patches Uabundant subsistence foods eaten when preferred foods are scarce I NOT FEMALE-BONDED FEMALE-BONDED Females can Females disperse Territorial Nonterritorial I be herded I SINGLE-MALE MULTI-MALE SINGLE-MALE MULTI-MALE, (males cooperate) (males compete) Fig. 3. Schematization of Wrangham s (1980) model of female-bonded primates. contest and scramble types of competition. He predicted that female bonding should occur when the costs of within group contest competition are offset by the benefits of cooperating with female kin in between group contest competition. Among such female-bonded groups, however, patterns of affiliative interactions suggest that although matrilines may cooperate with one another in intergroup competition, they otherwise remain strongly differentiated (Cheney, 1992). When within group contest competition is stronger than between group competition, as is assumed to be the case in specialized frugivores, females should split up, thereby avoiding direct competition with female kin and precluding the formation of strong afiliations and stable, long-term relationships with one another, as Wrangham (1980) proposed. Alternatively, within or between group feeding competition may be of the scramble type due to a dietary reliance on abundant and evenly distributed foods such as leaves, grass, and herbaceous vegetation. In these cases, there should be few benefits to cooperative strategies and the pressures favoring female bonding should be relaxed. Gelada and hamadryas baboons are the principal cercopithecine exceptions to this model for strikingly different reasons (Dunbar, 1986). The diet exploited in the arid habitat occupied by hamadryas baboons is believed to preclude the formation of female-bonded groups. Instead, hamadryas baboons have a multilevel society (Abegglen, 19841, unusual among nonhuman primates (Rodseth et al., 1991; but

15 Strier] MYTH OF THE TYPICAL PRIMATE 247 see also Robinson et al., 19871, in which male-male competition determines female patterns of association. Gelada females, by contrast, conform to the social criteria of female-bonded primates despite their dietary reliance on abundant, herbaceous vegetation. Female bonding in gelada baboons may be a secondary strategy employed for social rather than dietary purposes: by bonding together, gelada females can increase group size in response to high predator pressure (Dunbar, 1986; see below). In primates in which either females or both females and males routinely disperse, hierarchical relationships tend to be based on demographic factors such as length of residency in the group, female age, or female reproductive condition (Hanuman langurs: Hrdy, 1977; mantled howler monkeys: Jones, 1980) rather than kinship. Furthermore, in some nonfemale-bonded species such as hamadryas baboons and mountain gorillas, females may associate, at least in part, as a result of male efforts at herding them together (Wrangham, 1980). When males are experimentally removed or die of natural causes, female associations may disintegrate (but see Stammbach, 1978). In other species, female relations are egalitarian rather than hierarchical (e.g., muriquis: Strier, 1990; squirrel monkeys: Baldwin, 1992). Resources for these females are either not limited, or else the benefits of establishing and maintaining priority of access to resources are offset by high energetic or other constraints (Milton, 1984; Strier, 1992b,c). Competition for access to preferred foods is only one way in which females can maximize their reproductive opportunities. Unrelated females form alliances to prevent new females, and thus potential food and reproductive competitors, from immigrating into their group (howler monkeys: Sekulic, 1982; Crockett, 1984; Glander, 1992; Peruvian squirrel monkeys: Mitchell et al., 1991; muriquis: Strier, 1992~). Furthermore, females may compete directly for access to preferred mates which will invest in them or their infants (Smuts, 1985) or for infant care by inhibiting ovulation in subordinates (Abbott, 1989). Such helpers have been considered to be essential to relieve the high energetic costs on mothers, particularly among callithrichids which routinely give birth to twins (Goldizen, 1987, 1990). However, there is evidence that males may provide more infant care than nonreproductive females (reviewed in Snowdon, 1990a). Inhibiting their own reproduction while helping their mothers to rear siblings could be perceived as an extreme example of cooperation among female primates, although it is more likely that it is a case of making the best of a bad situation. If opportunities for dispersing and founding their own reproductive groups are limited, daughters may benefit their inclusive fitness by remaining in their natal groups and assisting their mothers in the rearing of siblings (Emlen and Vehrencamp, 1983; Goldizen, 1987; Snowdon, 1990a; see below). Less ambiguous forms of cooperation among reproductively active females have, however, been documented in many other primates. These cooperative alliances tend to be strongest among the female-bonded primates, where females routinely intervene on behalf of their kin against unrelated females and against males (Waiters, 1980; Smuts, 1987). However, in both matrilineal and nonmatrilineal societies, female alliances are effective at influencing male residence or associations with female groups in single-male polygynous (e.g., langurs: Hrdy, 1977) and multimale polygamous societies (e.g., Japanese macaques: Packer and Pusey, 1979; capuchins: O Brien, 1991; muriquis: Strier, 1992c; bonobos: Furuichi, 1989; Ihobe, 1992) and at defending food resources during encounters with other groups of females (e.g., vervet monkeys: Cheney, 1987; Peruvian squirrel monkeys: Mitchell et al., 1991; muriquis: Strier, 1992~). Strong female social bonds may also occur when females are unrelated and exhibit weak dominance relationships. In bonobos, for example, females engage in frequent genital-genital, or g-g, rubbing, a behavior that has been attributed to regulating tension under potentially stressful situations (de Waal, 1987). The expression of conciliatory interactions, like that of aggression, is highly variable both between distant taxa and across closely related species (de Waal, 1989a).

16 248 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Val. 37, 1994 The occurrence of strong female affliative relationships, cooperation, and reconciliation among both female-bonded and nonfemale-bonded primates does not imply that females are more passive or less aggressive than their male counterparts. Females may be more likely than males to avoid direct confrontations that increase the risk of injury to themselves or their infants (Smuts, 1987), particularly in species where males are larger and more equipped to inflict such injuries. Forming alliances with other females may be an effective strategy for protecting themselves from male aggression when males are individually dominant (Smuts, 1987; but see Packer and Pusey, 1979), but the risk of male aggression, and consequently the advantages of such alliances, are minimal in species in which females are dominant over, or codominant with, males (Strier, 1990; Kappeler and Ganzhorn, 1993). Male-male dynamics Female mate choice can have profound consequences for the outcome of malemale competition over access to females, but identifying what traits females favor in males has remained elusive (Small, 1989). Both female choice and male-male competition directly affect male reproductive success, but they are interrelated processes that cannot be easily distinguished. In a captive study, female hamadryas baboon preferences for particular males were perceived and respected by other males, although the bases for these mate choices were unclear (Bachmann and Kummer, 1982). Similarly, although dominant male olive baboons and chimpanzees may be able to aggressively interfere with copulations by subordinates, females are nonetheless highly successful at maneuvering themselves into mating consorts with preferred male associates (Tutin, 1979; Strum, 1982; Smuts, 1985). Males may solicit favoritism by maintaining proximity with a female, grooming her regularly, and providing protection and defense for both her and her infant. Establishing these associations appears to be a strategy employed both by new immigrant males as a means of achieving acceptance into a group (Strum, 1982) and by mature males which possess the sophisticated social skills required to gain a female s trust (Smuts, 1985). Yet, despite the importance of such affliative competitive strategies, less than 60% of male friends were possible fathers of infants born during one study of olive baboons (Smuts, 1985). The fact that high ranking males may be able to achieve substantial mating success without investing in friendships suggests that aggression may be a more effective strategy for males that are able to outcompete their opponents in direct contests. Because their competitive abilities fluctuate over their lifetimes, males may shift between aggressive and nonaggressive strategies as they mature and their relationships to both females and male competitors change. Aggressively competing with other males and establishing affliative relationships with females to obtain female choice need not be mutually exclusive strategies. Indeed, switching tactics in response to changing demographic and social conditions is common in many animals (Milinski and Parker, 1991). The ability to win overt contests-and all that winning implies about a male s ability to defend the resources females need or females themselves-may also be one of the criteria that some females use in choosing their mates. In brown capuchin monkeys, for example, females preferentially solicit copulations with the alpha male in their group, presumably because of the greater protection alpha males can provide females and their infants (Janson, 1984). In Costa Rican squirrel monkeys, males exhibit low levels of aggression except during the brief period when females are sexually receptive (Baldwin, 1992), and during one breeding season, the largest male accounted for 70% of all copulations observed (Boinski, 1987). Male-male aggression outside of the breeding season is also rare in black and white ruffed lemurs, where females appear to mate preferentially with familiar rather than unfamiliar males (Morland, 1993). Thus, whether females mate with male associates or dominant males at times when they are most likely to conceive appears to be highly variable both within and between species.

17 Strier] MYTH OF THE TYPICAL PRIMATE 249 As in females, the frequency and intensity of male-male aggression within multimale societies varies across species, ranging from the hostility displayed by many cercopithecines, to the mixed aggressive and affiliative interactions observed in chimpanzees and spider monkeys, to the seasonally restricted aggressive interactions in squirrel monkeys and lemurs, to the high levels of tolerance exhibited by bonobos and muriquis. This spectrum of male-male relationships is related to the reproductive pay-offs of aggression, which are related, in turn, to how easily females can be monopolized. Male strategies appear to reflect a compromise between competition for access to groups of females, or between group competition, and competition for access to individual females, or within group competition. Several variables have been invoked to differentiate the strength of between group competition, including dispersal patterns, group size, female grouping patterns, and the ratio of reproductive-aged females to males, or the socionomic sex ratio (van Hooff and van Schaik, 1992; Strier, 1994). If males disperse from their natal groups, they must first gain entrance to a group containing females, which often requires a combination of rebuffing antagonism from resident males and insinuating themselves into the group by establishing friendships with group residents. Once tolerated in a group, they must then begin to work their way up the male hierarchy through aggressive interactions or develop female support, as is the case in olive baboons (Strum, 1982, 1983; Smuts, 1985), or by transferring and maintaining coalition support with male kin in some macaques (Melnick and Pearl, 1987). In Hanuman langurs, males may cooperate with one another in ousting a resident male, and only afterward do they begin fighting amongst themselves for exclusive access to the female group. Once a single male has succeeded in monopolizing a group of females, he must still defend his position in between group competition. The killing of infants sired by the previous male following a take-over to bring females into estrus as early as possible during a new male s own tenure in the group may be a final extension of within group competition (Hrdy, 1977; but see Bartlett et al., 1993), but apart from this, obtaining access to a group of females may be close to the equivalent of obtaining access to individual females. In species where males generally remain in their natal groups, such as chimpanzees, spider monkeys, and muriquis, defending access to fluid groups of females from other groups of males may require extensive cooperation because it is difficult for males to track females that do not always associate together. This cooperation may be facilitated by kinship among philopatric males, but kinship does not necessarily imply that male kin will always cooperate with one another. Male philopatry occurs in both bonobos and woolly monkeys, yet, for different reasons, between group competition does not appear to be strong enough to promote male cooperative alliances in either case (Furuichi, 1989; Nishimura, 1990). van Hooff and van Schaik (1992) have suggested that group size and female grouping patterns are important determinants of male-male cooperation in between group competition. However, among the patrilineal New World atelin monkeys, female grouping patterns and the socionomic sex ratio appear to be more important than group size in determining how easily groups of females can be monopolized (Strier, 1994). Cohesive groups with relatively low female-to-male sex ratios in woolly monkeys may be more easily monopolized in between group competition, reducing the benefits of cooperative male alliances, than fluid groups with high female-tomale sex ratios in spider monkeys and muriquis, which are more difficult to defend without cooperation. The importance of between group competition to male relationships and reproductive opportunities is based on the assumption that primate social groups are the equivalent of closed breeding groups (Melnick et al., 1984; Richard, 1985a; Cords, 1987; Moore, 1992). In fact, although most copulations occur within groups, many female primates also copulate, and may conceive, with extragroup males (ringtailed lemurs: Sussman, 1992; sifaka: Richard, 1985a; patas monkeys: Rowell and Chism, 1986; Harding and Olson, 1986; forest guenons: Rowell and Chism, 1986;

18 250 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 Cords, 1987; Barbary macaques: Mehlman, 1986; Small, 1990; Japanese macaques: Sprague, 1992; muriquis: Strier, 1994). Sexual access to females may still be the primary reason why males associate in heterosexual groups, but such associations may not be as effective at monopolizing access to female groups as is generally thought (Moore, 1992). The importance of sexual access to particular females within groups is more clear-cut, because while a male that does not belong to a heterosexual group may still have opportunities to fertilize females, a male that is unable to mate will not. The degree of competition among males for sexual access to ovulating females may be most strongly affected by the ratio of estrous females to males at any particular time, or by the degree of female reproductive synchrony (Andelman, 1986; Caldecott, 19861, and the degree to which males can dominate females (Budnitz and Dainis, 1975; Strier, 1990, 1994). It should be more difficult for a single male to monopolize copulations as the number of females ovulating at any time increases (Berenstain and Wade, 1983; Cowlishaw and Dunbar, 1991). Thus, aggressive competition throughout the year may be less pronounced in species with tightly synchronized breeding seasons than in those in which female receptivity is asynchronous. Males may compete for access to dominant females, older females that have already demonstrated their success at motherhood, or young females that have not yet conceived (Stephenson, 1975; Lindburg, 1983) but the potential variance in male reproductive success, and consequently, the degree of within group competition, should be lower when there are too many estrous females for a single male to monopolize. In strongly seasonal breeders, such as lemurs and squirrel monkeys, males rarely engage in aggressive interactions when females are not receptive (Richard, 1974; Richard and Dewar, 1991; Boinski, 1987; Baldwin, 1992). Similarly, the tolerant social relationships among male bonobos, which contrast with the aggressively mediated hierarchical relationships of common chimpanzees, have been attributed to the more prolonged period of sexual receptivity of female bonobos (Furuichi, 1989). Ecological factors that affect female reproductive cycles, and physiological factors that affect female receptivity, play important roles in the degree of male-male aggressive competition. Monopolizing receptive females requires that females accept the outcome of male-male competitive efforts. In typical primates, in which males are dominant over females, females may associate and mate with preferred subordinate males, but dominant males can still interfere with female efforts to exercise choice. Not all primates are typical, however. Muriquis provide an extreme example of the consequences that female codominance with males may have on male social relationships and reproductive competition (Strier, 1990, 1994). Codominance may provide female muriquis with greater opportunities to express their mate choices, effectively overriding any benefits of male-male aggressive competition. If males cannot harass females into copulating, and females do not favor aggressive males, a male muriqui s best strategy may be to tolerate male allies for their support in competition with other groups of male kin, and compete for fertilizations through more subtle means, such as sperm (Milton, 1985a; Strier, ) or ejaculate plugs (Strier, 1992~). Sperm competition is just one of many alternatives to aggressive competition exhibited by male primates, and it may be a form of competition that females exploit or incorporate into their own reproductive strategies (Small, 1988). It is thought to occur in those species where the benefits of male-male aggression are offset by the necessity of cooperative alliances (Harcourt et al., 1981) or by female codominance (Strier, 1990, 1992b). Paradoxically, there is little evidence among lemurs for sperm competition, at least as measured by testes size, despite female dominance over males (Kappeler and Ganzhorn, 1993). Among some primates, such as yellow baboons and Barbary macaques, males may use infant care to establish affiliative relationships with females (Stein, 1984; Small, 1990). Among howler monkeys, Hanuman langurs, yellow baboons, and mountain gorillas, by contrast, males may commit or threaten to commit infanti-

19 Strier] MYTH OF THE TYPICAL PRIMATE 251 cide to secure access to estrous females (Hrdy, 1979; Smuts and Smuts, 1993; but see Bartlett et al., 1993). In any species in which social relationships are hierarchical and males are dominant over females, females are vulnerable to attacks directed by other females or males toward them and their infants (Smuts and Smuts, 1993). Protection from such aggression may a resource that males in these species can offer females in exchange for mating opportunities. Female-male dynamics The assumption that male aggression toward females and their young is an important dynamic in heterosexual relationships is based on the fact that the typical male primate is larger in body size and canine size than the female. Traditional sexual selection theory has explained the widespread occurrence of sexual dimorphism in terms of the advantages of size and weaponry in male-male competition for mates (Alexander et al., 1979). Although sexual dimorphism is prevalent among anthropoids, the degree of dimorphism tends to vary with the degree of male-male aggressive competition and other ecological constraints such as seasonally and spatially limited food and female availability (e.g., Popp, 1983; Rodman, 1984). In the lemurs, by contrast, males and females are more closely monomorphic despite radical differences in their social systems (Richard and Dewar, 1991). Greater similarity in body and canine size appears to be associated with greater equity between the sexes. Females are dominant over, or codominant with, males in the relatively monomorphic callitrichids (Sussman and Garber, 1987), and muriquis (Milton, 1985b; Rosenberger and Strier, 1989), as well as the lemurs (Kappeler and Ganzhorn, 1993). Energetic costs of gestation and lactation may limit how large females can become (Demment, 1983), and females may have to rely on alternatives to brute force to assert themselves. It is possible, for example, that the formation of cooperative female kin groups is a strategy to counteract the effects of sexual asymmetry in size, weaponry, and dominance (Packer and Pusey, 1979; Smuts, 1987; Strier, 1990) as well as for intragroup competition over access to food resources (Wrangham, 1982). Despite numerous efforts to identify consistent relationships between levels of sexual dimorphism and intrasexual competition (e.g., Kay et al., 1988; Rosenberger and Strier, 1989; Plavcan and van Schaik, 19921, explanations for the interacting effects of phylogeny, ecology, morphology, and behavior remain controversial. Persisting questions Discussions of primate aggression have traditionally revolved around the effects of aggressive competition on reproductive success. The accumulation of examples of alternatives to aggression has led to a better understanding of how primates compete, but they have not yet resolved outstanding questions about why primates compete. Captive and field studies have demonstrated that female reproductive success varies with nutritional condition, but we still lack detailed data on how nutrition of female primates varies in the wild (Strum and Western, 1982; Moore, 1984). How frequent are droughts and food shortages in nature? Can unpredictable ecological crises exert strong enough pressures to select for the long-term maintenance of complex social relationships? Conversely, the assumption that male reproductive success is highly variable in all but monogamous primates dates back to early considerations of sexual selection theory (Trivers, 1972). Yet, how much do most males really vary in their lifetime reproductive success (Hausfater, 1975)? How does variation in male ability to compete aggressively or form affiliative alliances ultimately affect which males females chose to father their offspring? We will be unable to answer these questions, or interpret the significance of the answers, until newly developed, noninvasive methods of paternity testing are more widely applied (Morin et al., 1993; Takenaka et al., 1993). It is important to note, however, that such data will be limited unless they are obtained at the level of local populations rather than just within single study groups, particularly if there

20 252 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 is any indication that extragroup males copulate with estrous females (Melnick et al., 1984). Behavioral responses to demographic fluctuations in primate groups and populations are as important to understanding aggression and competition as are fluctuations in ecological and life history variables. Long-term data from different primates reveal divergent responses to increases in population density, ranging from increased aggression and the splitting up of established groups to the formation of larger, more tolerant aggregations (Samuels et al., 1987; Strier et al., 1993). We know even less about the effects of shifts in adult sex ratios on inter- versus intragroup aggressive competition (Altmann and Altmann, 1979; Dunbar, 1979; Strier, 1994). Lastly, it is evident that competition among female and male primates may be mediated by their reproductive physiology. Whether through sperm competition or ejaculate plugs among males, or ovulatory inhibition among females, we still know very little about the proximate mechanisms by which reproductive physiology can be manipulated. Understanding primate reproductive physiology is essential to interpreting primate sexual behavior, especially in those cases in which a substantial amount of primate sexual activity occurs at times other than ovulation. Sex and reproduction Historical perspectives Interest in the relationship between sex and reproduction in nonhuman primates grew out of efforts to understand human sexual behavior from a comparative and evolutionary perspective. Early models focused on the social implications of concealed ovulation and continuous female receptivity, traits that were thought to be uniquely human (e.g., Morris, 1967; Alexander and Noonan, 1979; Ember and Ember, 1984). Scenarios differed in their emphases, which included among others the role of sex in securing male provisioning to enhance the survival of altricial young, and the importance of sex to maintaining a long-term pair bond. In many primates, however, ovulation is not advertised through visual cues and females copulate at times in their cycles when conception is unlikely, or, in the case of post-fertilization matings, when additional conceptions are impossible. In addition, females in a number of polygamous taxa copulate with many more partners than are necessary for conception (Hrdy, 1981; Small, 1988). These comparative findings clearly indicate that sex and reproduction are decoupled in many nonhuman primates, and that the human difference is therefore quantitative, not qualitative (Wolfe, 1991; Martin, 1992). This raises questions about the function of nonreproductive or extrareproductive sexual behavior and the origins of situation-dependent female receptivity (Hrdy, 1981). Hypotheses pertaining to nonreproductive sexual behavior can be grouped into three broad categories: 1) female strategies to confuse male confidence of paternity and thus increase male investment andlor reduce male interference in potential offspring (Hrdy, 1981; Harcourt, 1981; Hamilton, 1984; Wallis and Englander- Golder, 1992); 2) female strategies to regulate tension and thus decrease the risk of male aggression (de Waal, 1987; reviewed in Smuts and Smuts, 1993); and 3) female strategies to acquire a range of partners, permitting them to assess male quality and, in the case of primates with sexual swellings, to incite male-male competition (Clutton-Brock and Harvey, 1976). These hypotheses are not necessarily mutually exclusive (Small, 1988; Wallis and Englander-Golder, 1992). For example, confusing paternity has been invoked as one possible explanation for promiscuous mating behavior by female baboons, which exhibit visual signs of ovulation (Hausfater, 19751, as well as to account for nonreproductive matings with new immigrant males in species such as Hanuman langurs, in which ovulation is concealed and new males are potentially infanticidal (Hrdy, 1979). Examples of female sexual behavior to regulate tension include females soliciting sex

21 Strier] MYTH OF THE TYPICAL PRIMATE 253 with males that may direct or redirect aggression toward them (reviewed by Smuts and Smuts, 19931, particularly in contexts of elevated excitement (de Waal, 1987). Indeed, extended sexual swellings and prolonged female receptivity in bonobos have been linked to the low levels of aggressive competition displayed by males (Mori, 1984; Furuichi, 1989; Ihobe, 1992). Nonetheless, in all three sets of hypotheses, the implicit assumption is that nonreproductive sex has evolved as one of the counterstrategies females employ to offset the significant risks male aggression may pose for female reproductive success and to exert choice over males that are individually dominant to them (Hrdy, 1981; Smuts and Smuts, 1993). Evaluating these hypotheses about the function of nonreproductive sexual activity has been difficult due to the coincidental occurrence in many typical primates of a suite of interrelated and interacting traits: 1) agonistically established hierarchical relations among males; 2) male dominance over females due to sexual dimorphism in body and/or canine size; and 3) the predominance of male-biased dispersal systems. The absence of visible sexual swellings signaling female ovulatory state in the majority of primates (Dixson, 1983) further confounds observers efforts to correlate sexual behavior with female hormonal and reproductive condition. Visual concealment may not, however, confound male detection of female ovulatory condition, particularly when olfactory communication is employed (Ziegler et al., 1993; Converse et al., 1994). Promiscuous or opportunistic females? Species differences in sexual behavior are believed to correspond to differences in social systems. Promiscuity, or mating with numerous males, is a widespread occurrence across taxonomic groups whether females live in single-male and multimale groups, exhibit sexual swellings or concealed ovulation, or experience seasonal or aseasonal breeding. But, in most cases, even promiscuous behavior results in an uneven distribution of copulations by males. Females in single-male groups copulate with extragroup males during attempted take-over attempts (e.g., langurs), and females in both single-male and multimale groups may copulate with transient males during the breeding season (e.g., patas; Barbary macaques; Japanese macaques; lemurs). If such copulations are nonreproductive, however, distinctions between social and breeding groups are less critical than if they result in conceptions (see above; Moore, 1992). Various functions have been attributed to promiscuous behavior, ranging from female efforts to confuse paternity among males, to female efforts to avoid male aggression directed toward themselves, to female efforts to ensure fertilization. Confusing paternity may be important to ensure infant safety in species with infanticidal tendencies (Hrdy, 1981), but it may also increase infant caretaking by males in primates such as callitrichids. Accepting or soliciting male sexual advances may be less dangerous to females, particularly in highly dimorphic species where male aggression may lead to serious physical injury (Smuts and Smuts, 1993) or constant harassment may lead to interrupted feeding opportunities (e.g., gorillas: Wrangham, 1979). Promiscuity has been carried to extremes in two species, the bonobo and the muriqui. High frequencies of sexual activity have been associated with prolonged sexual receptivity in female bonobos (Furuichi, 1989). In muriquis, by contrast, sexual receptivity is more seasonal (Strier, 1987; Strier and Ziegler, 1994). Promiscuous mating in this species has been associated with egalitarian relationships between males and females (Strier, 1990; Strier, , which may be due to the fact that the sexes are monomorphic, or nearly so, in both body and canine size (Milton, 1985b; Kay et al., 1988; Rosenberger and Strier, 1989; Lemos de Sa and Glander, 1993). Male muriquis do not threaten or care for infants, and it is still unclear whether or not females mate with multiple partners throughout their ovulatory cycles and whether they do so for reproductive or social advantages.

22 254 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 Seasonal versus aseasonal breeders Field reports indicate that some type of birth clustering may be common in the majority of primates (Lindburg, 1987). The extent of such reproductive seasonality may be correlated with ecological, demographic, and social variables, and can have strong effects on the dynamics of primate social and mating systems (Jolly, 1967; Baldwin, 1970; Kavanagh, 1983; Nash, 1983). Tight reproductive seasonality, and therefore reproductive synchrony, affects the degree of male-male competition because as the ratio of estrous females to males rises, females become more difficult for individual males to monopolize (Cowlishaw and Dunbar, 1991; Strier, 1994; see above). When matings occur aseasonally, individual females become potentially defensible resources, but when reproduction is strongly synchronized, male-male competition tends to be weakest and opportunities for female mate choice rise as is the case in capuchins (Janson, 1984) and squirrel monkeys (Boinski, 1987). Female dominance in lemurs and female codominance in muriquis may be related to their seasonal reproduction as well as to their sexual monomorphism and high energetic costs (Young et al., 1990; Richard and Dewar, 1991; Strier, 1991a, 1994; Richard, 1992). Reproductive seasonality may simultaneously limit the degree to which females can use sex to manipulate their social relationships. Nonetheless, promiscuous mating during the breeding season can be effective at confusing male confidence of paternity, thereby reducing the risk of males harming potential offspring. When male infant care is important to female reproductive success, however, there may be advantages to actual or apparent fidelity. Parental care of infants All female primates, like all other mammals, bear the energetic burden of gestation and lactation. Yet, strong variability exists in the degree to which other group members participate in infant care. In cercopithecine primates, males may be protective of infants either to protect their reproductive interests if they are possible fathers, or to gain female trust and subsequent mate choice if they are not possible fathers (Whitten, 1987; Smith and Whitten, 1988). Similarly, male infant carrying has been attributed to both male infant care and male exploitation of infants as agonistic buffers (Stein, 1984). Male infant care is most widely observed among the callitrichids, which exhibit an array of mating systems ranging from monogamous to single-male polygynous to multimale polygamous to polyandry (Goldizen, 1987). Pronounced examples of male infant care in callitrichids, as well as other monogamous New World primates, include males carrying infants up to 90% of the time (Wright, 1990). Traditionally, male parental investment was attributed to paternity certainty in monogamous and single-male polygynous species, and to inclusive fitness benefits in polyandrous species, where strong associations have been found between the number of males and infant survivorship (Sussman and Garber, 1987). Yet, the fact that estrous females may mate with extragroup males, even among monogamous species, implies that male parental care may occur even in the absence of paternity certainty. High levels of male infant care have also been attributed to high metabolic demands of small-bodied female primates (Leutenegger, 1980; Wright, 1984,1990). Small (1990) found high levels of male alloparenting in the polygamous Barbary macaques, a species that may also experience metabolic stress due to seasonally low temperatures. However, nonparental caretakers may benefit directly, either by gaining essential experience that will increase their skill when they become parents themselves, or by enabling them to remain in a group where they may ultimately inherit reproductive positions (Snowdon, 1990a). Whether metabolic or social demands are responsible for male parental care in different taxa is still unclear. Nonetheless, the fact that males in some species care for infants that are evidently not their own further emphasizes the necessity of

23 Strierl MYTH OF THE TYPICAL PRIMATE 255 distinguishing behavior with potential future reproductive pay-offs from that with immediate ones. This distinction, like that between group membership or the use of sex for social or reproductive purposes, has important implications for the way that primate social systems have been modeled. MODELS OF SOCIAL SYSTEMS The myth of the typical primate has influenced efforts to classify primate social systems in much the same way that it has influenced characterizations of primate social relationships. The ecological models derived from these classificatory systems aim to be predictive as well as explanatory: If the models are sufficiently robust, it should be possible to accurately predict the social systems of primates from a clearly defined and quantifiable set of ecological variables. Yet, such predictions have been limited due to the combined difficulties inherent in identifying and measuring relevant ecological variables, and in accounting for stochastic ecological and demographic events and the effects of phylogeny on physiology, ontogeny, and behavior. Ecological models Early efforts to identify the ecological correlates of primate social systems focused on simple ecological variables, such as diurnal versus nocturnal and terrestrial versus arboreal habits, and on simple descriptions of group composition, such as monogamous pairbonds, single-male polygyny, age-graded polygyny, and multimale polygamy (DeVore, 1963; Crook and Gartlan, 1966). Dietary classifications were subsequently appended, distinguishing between insectivory, frugivory, folivory, and omnivory (Clutton-Brock and Harvey, 1977). Anthropocentrism figured prominently in many of these early models: ecological variables most closely resembling those to which hominids were believed to have evolved were inevitably associated with more complex social systems. Thus, the age-graded polygynous or multimale polygamous groups of typical diurnal, semiterrestrial, omnivorous primates were believed to represent the most derived, human-like condition, while the solitary or single-male polygynous groups of nocturnal, arboreal, insectivores primates represented the most primitive condition. As data accumulated and theoretical perspectives expanded, it became evident that such simplistic ecological and social classifications failed to characterize important variability among and between species. Closely related species, or even different populations of the same species, exhibit markedly different social systems, while distantly related species may exhibit strikingly similar organizations (e.g., prosimians: Richard, 1978; Tattersal, 1978; Harcourt and Nash, 1986). Several socioecological analyses have attempted to evaluate the relative importance of ecology and phylogeny in interspecific comparisons (lemurs: Sussman, 1977; cercopithecines: Struhsaker, 1969; mangabeys: Waser, 1984; atelines: Rosenberger and Strier, 1989; hominoids: Wrangham, 1987). Until recently, however, the role of phylogeny has been largely usurped by ecological models which have focused on two basic questions: Why do most primates live in groups; and why do primates live in the groups that they do? Group living is presumably advantageous for three reasons: improved predator detection and defense; improved food detection and defense; and improved access to mates. Differences in the social systems among the majority of group living primates, as well as more solitary species, are attributed to variability in predation pressure and fine-grained differences in the distribution and abundance of food resources. Thus, primates such as galagos, tarsiers, and orangutans are generally solitary except for the period when infants are dependent on their mothers and when males and females come together to mate. In the case of the nocturnal galagos and tarsiers, solitarity is attributed to cryptic predator avoidance (Nash, 19931, while in orangutans, it is attributed to the combination of immunity from predators due to their large body size and avoidance of feeding competition for access to preferred fruit (Rodman, 1984). That orangutans differ socially from the

24 256 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 ecologically similar chimpanzees has been attributed to the mediating effects of morphology. The costs of locomotion in orangutans are thought to be higher for the larger, more sexually dimorphic male orangutans than male chimpanzees, accounting for their failure to form cooperative patrols to defend female communities like male chimpanzees (Rodman, 1984). The role of predation Group living confers several potential advantages in primates that are too large to hide effectively from predators. Groups contain additional eyes and ears to detect predators, reducing the need for constant vigilance by each individual. Alarm calls may be highly specific to particular classes of predators, enabling an individual to respond in an appropriate way without having independently seen the danger (Seyfarth et al., 1980). Larger groups may be able to mount more effective defenses against predators, such as mobbing, than an individual could alone, and the presence of other possible victims may reduce the probability for any one individual to be taken as prey, a phenomenon described as the selfish herd (Hamilton, 1971). Indeed, the benefits of detecting and escaping from predators are thought to increase with group size until the costs of feeding competition become prohibitive; the optimum group size should reflect the compromise between these benefits and costs (Terborgh and Janson, 1986). Despite the advantages of group living to predation pressures, the role of predation in shaping primate sociality is highly debated. Some primatologists regard it as minimal (e.g., Wrangham, 1979), particularly for large bodied primates and primates inhabiting areas where human activities have eliminated naturally occurring predators (Strier, 1992~). The latter may reflect relatively recent events, however, raising the question of how rapidly primate behavior can adapt to changing ecological conditions. Even in less disturbed habitats where natural predators and primates coexist, the intensity of predation on primates, and its significance remain difficult to quantify. Successful predation events may be witnessed infrequently (e.g., Stelzner and Strier, 1981), particularly if the presence of human observers inhibits the approach of unhabituated predators (Stanford et al., 1994). However, high levels of predation have been documented in Costa Rican and Peruvian squirrel monkeys (Mitchell et al., 1991), and in ringtailed lemurs, where male dispersal in cohorts instead of individuals is thought to be a response to high predator pressure (Sussman, 1992). Observations of leopard predations on chimpanzees in the Tai National Forest (Boesch, 1991) and the discovery of chimpanzee hair in the feces of lions (Inagaki and Tsukahara, 1993) indicate that large bodied primates, as well as arboreal ones (Terborgh, 1983), are vulnerable prey. Primates as predators. Even if predation events are more common than previously thought, what percentage of all mortalities must predation account for before it can be regarded as a serious selective force? Recently, analyses of 9 years of data on chimpanzee predations on red colobus monkeys at Gombe National Park, Tanzania, indicate that the chimps have killed at least 350 red colobus, accounting for a substantial percentage of mortality in this species (Stanford et al., 1994). Gombe chimpanzees exhibit higher predation rates than do other populations (Wrangham and van Zinnicq Bergmann Riss, 19901, and the social organization of red colobus monkeys at this site is believed to be influenced by chimpanzee predation pressures (Busse, 1977). The evidence indicating that chimpanzees can be highly successful predators is significant not only because of its potential role in the social adaptations of primate prey species, but also because of the importance attributed to meat eating in the course of human evolution. The transition from a vegetarian diet supplemented by invertebrates to one involving the exploitation of large vertebrates was believed to be a critical distinction between nonhuman and human primates. Yet, in their

25 Strier] MYTH OF THE TYPICAL PRIMATE 257 determined, coordinated hunting tactics, their sharing of kills, and the male-bias in hunting activity, chimpanzees exhibit many of the behavioral traits that have been associated with cooperation, reciprocity, and the division of labor in humans (McGrew, 1979, 1981; Boesch and Boesch, 1989). Whether the proportion of meat in chimpanzee diets is high enough to merit comparisons with the role of meat in human diets remains controversial. The question provides, nonetheless, an extreme example of the persisting difficulty of characterizing primate diets and the effects of dietary variables on social behavior. Characterization of primate diets Annual proportions. Primate diets have traditionally been characterized by calculating the average proportion of feeding time devoted to different food types, which for most primates is some combination of fruits, leaves, flowers, seeds, and insects or other invertebrates (Hladik, 1981). Species have been classified as insectivorelfrugivores, frugivorelfolivores, folivorelfrugivores, or omnivores based on the predominant food types in the annual diet (Richard, ). These dietary classifications have been correlated with morphological traits, including body size, dentition, and gut specializations (Kay, 19841, although recent analyses indicate that taxonomy is a stronger predictor of diet than body size in many New World monkeys (Ford and Davis, 1992; Strier, 1992a) and lemurs (Richard and Dewar, 1991). Dietary type has also been linked to behavioral variables including day range length, home range size, and the degree of intra- versus intergroup feeding competition (e.g., Milton and May, 1976; Clutton-Brock and Harvey, 1977). Despite the utility of such classificatory systems, there are numerous limitations to such simplifications (Rosenberger and Strier, 1989). First, proportions of feeding time on different food items fail to consider the significance of handling and search times, absolute food weights, caloric content, or nutritional value (Richard, 1985b). In a study of red howler monkeys, Gaulin and Gaulin (1982) found that the importance of fruits and leaves in the diet differed markedly depending on which measure was used. Second, annual averages fail to take into account the importance of seasonal or year-to-year variations in food availability and, consequently, diet. From an evolutionary perspective, ecologically stressful periods are likely to play a highly significant role in selecting for morphological specializations (Rosenberger and Kinzey, 1976). Pronounced seasonal shifts in food availability have been identified in nearly all studies where phenological data have been collected, and primates respond to these fluxes in preferred food availability by either shifting their diet to more abundant foods or by shifting their behavior, including ranging and grouping patterns (Wrangham, 1980). Although most researchers regard such dietary or behavioral shifts as examples of adaptive responses, one result is that inferences about food preferences generated from morphology may be inconsistent with direct observations of feeding behavior at any particular time (Rosenberger and Kinzey, 1976). Finally, distinguishing primate diets by the predominant food type may lead to inconsistencies in the predicted relationship between diet and behavior. For example, frugivorous primates have been described as following a strategy that maximizes energy intake, in contrast to the strategy of minimizing energy expenditure followed by folivores (Milton, 1980). Frugivores spend less time resting and travel longer distances than more folivorous primates, presumably because fruit is both higher in energy and more patchy in distribution than leaves. Yet, among the New World ateline primates, which include the frugivorous spider monkey and the folivorous howler monkey, there is substantial overlap in the annual proportion of feeding time devoted to fruits and leaves between seasons and between habitats (Strier, 1992a). Muriquis fall within the range of folivory documented for howler monkeys, yet in nearly every feature of their behavior, including day range length,

26 258 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 home range size, group size and composition, and group cohesion, muriqui behavior more closely resembles the energy maximization strategy of spider monkeys. Such comparisons among closely related species avoid the potentially confounding effects of phylogeny on behavior (Glutton-Brock and Harvey, 1984). They emphasize the limitations of predicting behavior from broad dietary categories based on annual feeding times alone, and suggest that, if dietary data are the only information available, then the most meaningful interspecific comparisons are likely to be restricted to sympatric primates confronting similar ecological pressures at particular times (e.g., Strier, 1992a; Tutin and Fernandez, 1993). Inconsistencies in the predicted relationship between diet and behavior have also been documented in comparisons between Costa Rican capuchin monkeys and African redtail monkeys, further illustrating the difficulties of generalizing about social behavior from dietary categorizations (Fedigan, 1993). Despite similarities in the proportion of different food types in the diets of these primates (Robinson and Janson, 19871, Fedigan (1993) found that capuchin intersexual relations deviated substantially from those observed in redtail monkeys and predicted from the ecological analogy. She suggests that a more informative description of capuchin monkey foraging strategies, opportunistic, extractive foraging, would be more appropriate to understanding their behavioral ecology than the proportion of fruits, insects, and leaves in their diets. Distribution in time and space. Efforts to evaluate the effects of food distribution on primate behavior have distinguished food types by whether they occur in discrete patches of limited size, such as fruiting trees, or in abundant, even distributions, such as grass and many leaf sources (Wrangham, 1980). Patchy foods are potentially defensible, with the benefits of such defense depending on the correspondence between patch size and group size. Fruit is also regarded as a preferred food for most primates because it is higher in readily available energy than leaves (Wrangham, 1980). Consequently, the size, distribution, and abundance of patchy fruit resources should determine the degree of intra- and intergroup feeding competition. How primates, especially females, respond to seasonal fluctuations in the availability of fruit patches should determine their social options (Wrangham, 1980; van Schaik, 1989). When large fruit patches are scarce, females should either fission into smaller feeding parties to avoid within group contest competition with one another, or remain together and cooperate in defending whatever large patches may occur in between group contest competition. In the latter case, it is also necessary that they can shift their diets to less preferred but more abundant, evenly distributed foods to avoid the high costs of intragroup feeding competition. The physiological ability to accommodate dietary shifts to lower quality foods, as well as the relative availability of preferred foods, should determine which of these strategies females adopt. While useful in principle, dichotomizing primate diets into patchy, high quality fruits versus evenly distributed, low quality leaves is somewhat misleading. Differences in leaf quality can be as pronounced as those between fruits and leaves, and the distribution of leaves that are low in digestion-inhibiting tannins or other secondary compounds may be as patchy as that of many fruits (Glander, 1978). Furthermore, although there is evidence suggesting that protein and other nutrients, as well as carbohydrates, play important roles in primate food preferences, we still know remarkably little about the digestive physiology and nutritional requirements of the vast majority of primates, on the one hand, and the chemical composition of most primate foods, on the other (Oftedal, 1992). Demography, as well as social systems, may be strongly affected by disease as well as the spatial and temporal availability of primate foods (Coelho et al., 1977). Sharp population declines have been documented after extended periods of drought in many Old World monkeys (e.g., yellow baboons: Altmann and Altmann, 1970;

27 Strierl MYTH OF THE TYPICAL PRIMATE 259 olive baboons: Sapolsky, 1986; toque macaques: Dittus, 1979; vervet monkeys: Wrangham, 19811, and disease has periodically swept through the Gombe chimpanzees (Goodall, 1986) and Panamanian howler monkeys (Collias and Southwick, 1952; Smith, 1977). In addition, human habitat disturbance and poaching have fragmented many primate populations and decimated their numbers (Mittermeier and Cheney, 1987). Understanding behavioral responses to both naturally occurring and human-induced fluctuations in group and population size and composition may ultimately provide critical insights into the determinants of primate social systems (Neville, 1968; Durham, 1971; Anderson, 1983). Even with such attention to demographic and phylogenetic variables, the question of whether primate social systems can be modeled in a predictive or deterministic way remains controversial (Rowell, 1993; see below). Categorical versus continuous variation across primates Disagreements over the relative importance of predation pressures or food availability and distribution in the evolution of primate social systems, like nearly every feature of primate social behavior reviewed thus far, illustrate the limitations of imposing discrete categorical alternatives on complex phenomena that are actually continuous variables (Clutton-Brock and Harvey, 1984). Primates classified as frugivorous eat foods other than fruit, and even reproductive success, the common currency in all evolutionary theories, is a relative term. While categorical classificatory systems may be useful as a first approximation in ordering primate behavioral diversity, they risk obscuring important similarities and continuities. Similarly, there has been a tendency to interpret correlations between behavioral and ecological variables as evidence of causality (Clutton-Brock and Harvey, 1984). For example, primate day ranges may decrease as the degree of folivory increases, but the reason for this apparent relationship is not clear. Are leaves more densely distributed than other food types, or do folivores tend to live in smaller groups with lower feeding requirements? Potentially confounding variables, such as group size, are not always so obvious and they may affect different species to different degrees. Indeed, deterministic models of behavior are particularly problematic when ecological and phylogenetic variables are treated as partially, but not fully overlapping sets (Fig. 4). Comparisons between sympatric species and between populations of the same or closely related species occupying different habitats can help to tease apart the dynamic, interacting effects of ecology and phylogeny on social behavior (e.g., Mitchell et al., 1991; Fedigan, 1993; Kappeler and Ganzhorn, 1993). Without such appropriate comparisons, efforts to develop and expand comprehensive models of primate behavior risk being overwhelmed by the diversity of primate adaptations. Intra- versus interspecific variation Similarities in the social systems of distantly related species, such as chimpanzees and spider monkeys (Symington, 1990) or capuchin monkeys and cercopithecines (Robinson and Janson, 1987; O Brien, 1991; Fedigan, 1993), have been interpreted as evidence of behavioral convergence in response to similar ecological pressures. Differences between populations of the same or closely related species, such as muriquis from Minas Gerais and Sao Paulo (Strier, l989,1992a), Peruvian and Costa Rican squirrel monkeys (Mitchell et al., 1991), red and mantled howler monkeys (Glander, 1992; Crockett and Pope, 1993) or De Brazza s monkeys (Brennan, 1985) by contrast, have been interpreted as evidence of divergent responses to local ecological differences. Yet, by focusing on the ways in which ecology affects behavior, we have remained remarkably ignorant about phylogentically conservative traits and the interaction between phylogeny and ecology, on the one hand, and ecology and demography, on the other. In addition, proximate mechanisms, such as individual developmental experiences and physiology, that affect life histories, may be correlated with phylogeny and must be incorporated into our comparative models (Harvey and Purvis, 1991).

28 260 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 ( Phylogeny) (-) (-) b. (Gz-)->(-) \ d C d. P hy 1 ogeny Ecology em ography Fig. 4. Alternative views of the relationships between ecology, phylogeny, demography, and behavior. a,b Hierarchical effects with no demographic factors included. c: Phylogenetic and ecological effects on behavior are mediated by and influence demographic variables. d: Interactive effects between phylogeny, ecology, demography, and behavior are hierarchical and unidirectional; e: Interactive effects of phylogeny, ecology, demography, and behavior are nested in a dynamic feedback system. For example, is male-biased dispersal the ancestral primate condition, retained among extant lemurs and most cercopithecines, but lost among all apes and all but one New World monkey, or is it a derived condition among both lemurs, perhaps due to high metabolic requirements in these sexually monomorphic primates, and cercopithecines, as a way to counteract the effects of male dominance in these sexually dimorphic primates when ecological conditions permit? Models of primate behavioral ecology have begun to consider the role of phylogeny, and to incorporate the growing body of comparative data on diverse taxa (Wrangham, 1987; Strier, 1990; Fleagle, 1992; DiFiore and Rendall, 1993). How facultative are dispersal and other behavioral systems within primate species? Phylogenetic considerations may offer few insights into the dynamics of intraspecific or intrageneric behavioral variability (but see Harvey and Purvis,

29 Strierl MYTH OF THE TYPICAL PRIMATE ). Rather, demographic variables such as sex ratios and birth rates, which may fluctuate widely over relatively brief timespans, must be considered. Newton (1988) and Stephen (1989) have emphasized the importance of demography for interpreting variability in the social systems of Hanuman langurs and tamarins, respectively. The effects of demography on social relationships have also been demonstrated in long-term studies, not only of cercopithecines (e.g., yellow baboons: Altmann and Altmann, 1979; gelada baboons: Dunbar, 19791, but also of prosimians (e.g., ringtailed lemurs: Sussman, 1992) and New World monkeys (e.g., mantled howler monkeys: Glander, 1992; muriquis: Strier et al., 1993). As longterm data accumulate from a wider diversity of primates, it may be possible to identify patterns in behavioral responses to demographic events, and to evaluate more thoroughly the interrelationships between ecology, phylogeny, and demography that have affected both nonhuman and human primate behavioral evolution (Fig. 4). REVISIONIST PERSPECTIVES FOR PRIMATOLOGY Within anthropology The study of complex societies Primatologists and social anthropologists share the study of complex and highly variable societies. Yet, their approaches to studying the behavior of nonhuman and human primates have tended to diverge in at least two important respects. It is appropriate to consider these differences, and the consequences that incorporating new knowledge of diversity may have for primatologists and anthropological perspectives on primates. Primatologists are in two senses reductionists, at least methodologically. First, the implicit assumption that behavior can be quantified necessitates reducing complex social aggregations and interactions into their individual components (Hinde, 1976). These components, or variables, are constantly being refined and revised, but do we miss important relationships between different variables in the process? Critics of reductionist approaches regard society or culture as an epiphenomenon, a whole that is greater than the sum of its parts, and may find hierarchical or dialectical analyses of individual behavior and relationships within society too limiting (see Hinde, 1987; Quiatt and Reynolds, 1993; Rowell, 1993). Yet, without the quantitative data obtained from reductionist methods, primatology would revert to the descriptive accounts that characterized the first wave of studies, and we would lose whatever comparative ground we have gained over the years. Rather, by extending behavioral ecological models to include phylogenetic and demographic variables, we may be able to identify patterns across diverse and dynamic behavioral systems. At the same time, however, we must incorporate the more traditional definition of reductionism, in which complex phenomena, such as social behaviors, are understood in terms of lower level processes involving proximate mechanisms. Primatologists working with captive primates have historically examined behavior at multiple levels (Snowdon, 1990a); the continued development of noninvasive techniques to measure proximate variables that affect behavior will provide additional insights for field primatologists as well. As evolutionary theorists, primatologists also tend to be populationists, interested in individual variability, rather than typological norms that tend to disregard most surrounding variation (Mayr, 1966). However, primatologists have succumbed to the problem of extrapolating from individual cases to generalized models, resulting in overly simplified myths, such as that of the typical primate. The challenge of incorporating individual diversity, whether between individuals, populations, and species, or across primates, resulted in the search for unifying principles that govern behavior and that can explain variability. These principles have been modified and expanded as new, contradictory data emerged, as can be seen in the development of theories of kin selection and reciprocal altruism in

30 262 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 37, 1994 sociobiology, or stochastic dynamic programming models in behavioral ecology (Mange1 and Clark, 1988). Without such principles, primatologists would be forced to adopt a sort of group relativism, similar to the cultural relativism employed by many contemporary social anthropologists. Primatologists must acknowledge the coexistence of alternative behavioral strategies, such as that of aggressive versus affiliative forms of competition among males, which may occur in a population as a frequency-dependent trait. Rowell (1993: 136) suggests that we lack evidence that individuals have in any sense decided on an appropriate social system.... Rather, animals respond to impinging stimuli and we perceive social systems. If social systems are not emergent properties, then, as Rowell proposes, efforts to fit observed variation across primates into simple classificatory systems may detract from, rather than advance, our understanding of behavior. Yet, as long as the pursuit of unifying explanations and testable hypotheses about behavior remains a priority, primatology will continue to be more closely, and appropriately, aligned with behavioral ecology than with other subfields of anthropology. The role of primate models in studying human behavioral evolution If primatologists are methodologically and theoretically more closely aligned with behavioral ecologists than with other anthropologists, are nonhuman primates more appropriately viewed as other animals rather than as human relatives? Social carnivores may provide better models for cooperative hunting (Schaller and Lowther, 19691, cetaceans may provide better models for complex, multilevel societies (Moore, 1992), and birds may provide better models for the ontogeny of vocal communication (Snowdon, 1990b). But if, for example, we would like to know how humans evolved their vocal tracts, nonhuman primates, and in particular, our closest panine relatives, are clearly the most suitable study subjects. While general principles that apply to nonprimates, nonhuman primates, and humans alike are useful in addressing questions of convergence, it is primates we must look toward in addressing questions of homology (de Waal, personal communication). General principles that explain some of the diversity of extant primate behavioral adaptations can provide insights into that of extinct primates, including hominids (Tooby and DeVore, 1987), but it is important to recognize the limitations of such inferences. For example, comparative data from nonhuman primates indicate that while those with monogamous mating systems are sexually monomorphic in body and canine size, some sexually monomorphic primates, such as muriquis, mate polygamously (Milton, 1985b; Rosenberger and Strier, 1989; Strier, 1987, ; Lemos de Sa et al., 1993). We might infer, therefore, that sexual dimorphism among fossil hominids was associated with polygynous or polygamous mating systems, but we could not conclude that sexually monomorphic hominids were necessarily monogamous. Recognizing that not all principles have transitive properties is as essential to avoiding inappropriate inferences between nonhuman and human primates as is the fit between our choice of study subjects and the types of comparative and evolutionary questions we ask (Harvey and Purvis, 1991). Comparative behavioral ecology Apart from their phylogenetic relationship to humans, do nonhuman primates differ from other animals? Or, as Daly (1992:425) has provocatively asked, Why does primatology exist? According to Daly, The principal effect of this disciplinary boundary seems to be a slowed diffusion of advances from behavioral ecology and other biological disciplines. Yet, long-term studies of long-lived, socially manipulative individuals have provided some of strongest examples of the range of behavioral diversity within and between species (Cheney et al., 1987). Indeed, primatologists were among, if not the first, behavioral ecologists to recognize and individually name their study subjects (Asquith, 1991). Insights into the ways in which social behavior can respond to and compensate for ecological fluctuations

31 Strier] MYTH OF THE TYPICAL PRIMATE 263 are likely to become more instructive as phylogenetic, demographic, and proximate-level factors are increasingly considered. The merging of phylogeny and demography with behavioral ecology and physiology can provide a context for interpreting behavioral diversity, but it will be limited unless the communities in which primates occur are also understood. Understanding interspecific competition or mutualistic associations both among primates and between primates and other animals is essential to understanding the contexts in which primate behavioral adaptations have evolved. Conservation biology Is the liberation of primatology from its anthropological biases an oxymoron? As long as primatologists continue to search for patterns and principles that may be relevant to questions about human behavioral evolution, nonhuman primates will continue to be important anthropological subjects. Yet, primate studies have acquired another, more urgent agenda. Increasing human pressure through hunting and habitat disturbance over the past century has led a number of primates to the verge of extinction. Of some 240 species of primates recognized today, nearly onehalf are threatened and nearly one-third are endangered, meaning they will become extinct unless drastic measures are taken to protect them. Habitat preservation is an obvious form of protection, and primates are obvious flagship species to generate public and political support for conservation efforts. In addition, because they are high on the food chain, primates serve as good indicators of the degree of habitat degradation (Mittermeier and Cheney, 1987). Many of the data that field primatologists routinely collect during their scientific studies are invaluable to informed conservation management efforts. For example, data on mating patterns and paternity of both group and nongroup members can provide critical insights into the genetics of endangered populations, while data on dispersal patterns can help determine which sex might be the most appropriate to move in translocation projects (Strier, 1992~). Similarly, understanding the relationship between sex and reproduction, and the interactions between reproduction and ecological and demographic variables, will be critical to monitoring the viability of populations, and by extension, tropical ecosystems. The expansion of primate field studies throughout the tropics has led to the discovery of new species and the rediscovery of species that had been thought extinct. It has also led to the discovery of greater diversity in primate behavior. Incorporating this diversity into more comprehensive primatological models will facilitate our ability toward preserving it, without undermining the importance of primates within anthropology. ACKNOWLEDGMENTS This review benefitted from support from NSF grant BNS , and discussions with Irv DeVore, Jon Marks, Jim Moore, and Chuck Snowdon over many years. I am especially grateful to Jim Moore, Jon Marks, Chuck Snowdon, Frans de Waal, and two anonymous reviewers for their critical reading and comments on an earlier draft of this manuscript, and to Ted Steegmann for his patience and encouragement. LITERATURE CITED Abbott DH (1989) Social suppression of reproduc- Evolutionary Biology and Human Social Behavtion in primates. In V Standen and RA Foley ior. North Scituate, Mass.: Duxbury, pp (eds): Comparative Socioecology: The Behav ioural Ecology of Humans and Other Mammals. Alexander RD, Hoogland JL, Howard RD, Noonan Oxford Blackwell Scientific, pp KM, and Sherman PW (1979) Sexual dimor- Abegglen JJ (1984) On Socialization in Hamadr- phisms and breeding systems in pinnipeds, unguyas Baboons. Cranbury, N.J.: Associated Univer- lates, primates, and humans. In NA Chagnon sity Presses. and W Irons (eds.): Evolutionary Biology and Hu- Alexander RD, and Noonan KM (1979) Conceal- man Social Behavior: An Anthropological Perment of ovulation, parental care, and human so- spective. North Scituate, Mass.: Duxbury, pp. cia1 evolution. In NA Chagnon and W Irons (eds.):

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