ADVANCES IN THE STUDY OF BEHAVIOR, VOL. 37

Coexistence in Female‐Bonded Primate Groups S. Peter Henzi*,{ and Louise Barrett*,{ *school of psychology, university of kwazulu‐natal durban 4041, south africa { department of psychology, university of lethbridge lethbridge, alberta t1k 3m4, canada

I. INTRODUCTION With few exceptions, diurnal primates are distributed in large social groups that are spatially and temporally coherent. The goal of primate socioecology since 1960s has been to understand what drives and structures this distribution. Whereas initial syntheses (Crook and Gartlan, 1966; Eisenberg et al., 1972) focused on males, this emphasis gave way during the 1970s to an increasingly articulated representation of primate sociality that was centered on females and their responses to the world (Dittus, 1977; Hinde, 1983; Seyfarth, 1976; Wrangham, 1980). This shift, to a large degree, was fueled by the coincidence of an accelerating number of detailed field studies and the emergence of sociobiological theory, including the recognition that females were the ‘‘ecological’’ sex (Emlen and Oring, 1977; Wilson, 1975). The former pointed to well‐differentiated relationships within groups, while the latter shifted the analytical emphasis from groups to individuals and promoted kin selection as the likely solution to the reproductive consequences of cooperation and coexistence (Hamilton, 1964, 1972). Given that this fieldwork concentrated on Old World monkey species (Cercopithecoidea) in which females predominantly remain in their natal groups—and hence are ‘‘female‐bonded’’ (Wrangham, 1980; where the term indicates both female philopatry and strong bonds between females)—subsequent empirical and theoretical attention was directed to the nature of the associations of female kin. Despite a well‐administered corrective to the uncritical assumption that the results of all this effort speak to the ‘‘typical’’ primate (Strier, 1994), instead of being phylogenetically circumscribed (Di Fiore and Rendall, 1994), interest in the social dynamics of female‐bonded (FB) primates 43 0065-3454/07 $35.00 DOI: 10.1016/S0065-3454(07)37002-2

Copyright 2007, Elsevier Inc. All rights reserved.

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remains strong. There are many reasons for this. Although not representative of most primate societies, FB groups are certainly much more common within the Old‐World monkeys (and the New‐World genera, Cebus and Saimiri), compared to other families (as well as other mammals in general), and this is a distinction that promotes elaboration. There is also a well‐ developed body of socioecological theory, which has emerged from the study of FB groups and that has now developed its own impetus and connects to other central primatological concerns such as the ‘‘social intelligence’’ hypothesis (Barrett et al., 2007). Finally, a good deal of effort continues to go into field studies of FB species, generating both long‐term data from single populations, as well as comparative information across different populations of the same species, both of which allow for much richer analyses than are possible with any other primate group. Our aim here is to review these data, highlighting the strengths, insights, and shortcomings of current theoretical views of FB groups. In doing so, we hope to make a case for a more nuanced framework in which to situate studies of primate sociality and cognition.

II. KINSHIP AND COMPETITION FB societies remain interesting in their own right because they pit the explanatory power of kin selection against the understanding that, other things being equal, individual animals will behave selfishly. What then happens in a world where relatives must coexist? This question, which guides most of the work on social dynamics in FB primate groups, has derived its power primarily from the demonstration that while the advantages of group life accrue in relation to their ability to reduce predation risk, and where larger groups are therefore better, they are coupled to reproductive costs associated with local resource competition, where larger groups, consequently, are worse, at least for some group members (Dunbar, 1988; van Schaik, 1983). These demonstrations that birth rates decline with group size negate the original presumption that FB groups are primarily cooperative, in the sense of being selected in the context of defending resources against other FB groups (Wrangham, 1980). This, then, has been the springboard for everything that follows because it sets up the idea that female relatives are obliged to compete, in one way or another, for resources within a social group that they cannot readily leave. While there have been rumblings recently that this emphasis on within‐group competition discounts the generally cooperative basis of social engagement (Sussman et al., 2005) it is likely to stand, at least until the alternative is more comprehensively fleshed out (Koenig et al., 2006) and some synthesis achieved.

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In the meantime, the question of how females respond to the ‘‘inevitability’’ of competition has produced a cascading set of neat, interlocking responses. These have served as powerful organizing principles for data collection and interpretation (Barrett et al., 2007) and have additional resonance because they point directly to a particular view of primate cognition (Dunbar, 1998). In this view, the canonical structure of FB social dynamics is derived from the following strategic responses displayed by females: 1. In order to defend resources against competitors within groups, it is advantageous for females to form cooperative coalitions and alliances (Harcourt and de Waal, 1992; Wrangham, 1987), where a coalition is defined as an event in which one individual aids another by actively joining forces against a third during an on‐going aggressive encounter, and where an alliance represents an enduring cooperative relationship involving repeated coalition formation. 2. Allogrooming, insofar as it provides a service to others, is used by females to persuade valuable (e.g., high‐ranking) partners to participate in coalitions (Seyfarth, 1977). Females form strong, enduring relationships with each other, which they service by grooming, as a means of ‘‘ensuring unstinting mutual support’’ (Dunbar, 1998) from their coalition partners over time, either by the exchange of grooming for support in a reciprocal fashion (Cheney and Seyfarth, 1984) or by using grooming as a signal of mutual trustworthiness (Dunbar, 1998). 3. Where such valuable relationships are damaged (e.g., by aggression between alliance partners), females will act to repair this damage via a process known as reconciliation (de Waal, 1989), so that they can continue to reap the benefits of coalition formation over time. This is, to some extent, a caricature of a more nuanced framework that also includes the effects of resource dispersion (Sterck et al., 1998; van Schaik, 1989), where these processes, associated with nepotism, are more predictive of species encountering clumped, defensible resources. Nevertheless, it is true to say that this broad structure receives support from Di Fiore and Rendall’s phylogenetic analysis (Di Fiore and Rendall, 1994) and that their results are perhaps themselves a product of the fact that most researchers have either concentrated their work on these topics or framed their analyses in this way (see, as two examples, Matsumura, 1998; Silk et al., 2003). In addition, further implicit acceptance for this focus is evinced by the widely embraced ‘‘social brain’’ hypothesis (Dunbar, 1998), which extends these premises to account for the general increase in relative brain size among the anthropoid primates relative to other mammalian groups. Here, the prospective need to predict the actions of others and to

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track and service valuable relationships in order to sustain coalitions (that is, the qualitative demands of social engagement with others), all place cognitive demands on females that have selected for increased brain size; these selection pressures are assumed to have been stronger in species that, for ecological reasons, must live in larger groups, producing a quantitative component to relationship monitoring, which further selects for increased brain size. In other words, the social brain hypothesis provides the mechanistic, cognitive underpinnings that are required to sustain the long‐term, strategic relationships that structure FB groups in ways that are relevant from a functional, evolutionary perspective. In this view, therefore, the assumption being made is that females have an overt, cognitive understanding of their own relationships that they actively strive to sustain, protect, and repair over time. This framework and its corollaries are very compelling, both because the components fit together seamlessly and because they are congenial to a view of ourselves that, at least in part, helps validate research on primate sociality (Barrett et al., 2007). While there is no doubt that it has been a very powerful driver of some very good research, it is, in a sense, at the mercy of its own success. Our general argument has been that the congeniality of the argument is not matched by the data it has produced (Barrett and Henzi, 2005, 2006; Henzi and Barrett, 1999), and that there is now an opportunity—easily met, we think—to reconfigure it. In the sections that follow, we look at each of the behaviors linked to theories of female coexistence. We illustrate how each can be seen as an independent, contingent response to current need rather than as interlocking components of an overall female strategy to cultivate and enhance relationships in the long term. Having done so, we then suggest that the concept of a relationship may itself benefit from a fresh, and less anthropomorphic, assessment.

III. ORGANIZING PRINCIPLES A. COALITIONS Coalitions among adult females against other adult females of the same group provide the keystone for this conceptualization of long‐term relationships: if coalitions are not the key mechanism by which females alleviate the negative effects of competition on their reproductive success, then there is no immediate need to consider the formation and conservation of valuable long‐ term partnerships. Coalitions and alliances sprang to prominence with the rising interest in primate social cognition because they suggested a capacity to track third‐party relationships, which, at the time, appeared to be

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beyond the capability of non‐primates (Harcourt and de Waal, 1992). More recent research, however, has shown that other species such as hyenas display similar abilities despite relatively smaller brains (Holekamp, 2007; Holekamp et al., 2007). What is interesting is the extent to which the deployment of coalitions as the primary means by which females achieve their competitive goals has been an article of faith for primatologists in the face of relatively little evidence that they serve such a function (Henzi and Barrett, 1999). Savannah baboons, for example, live in typical FB groups and, in some populations, experience strong within‐group competition that has clear consequences for participants. At Mkuzi in South Africa, at a time when predation pressure was particularly high, rates of female–female aggression were among the highest recorded for baboons and were a consequence of attempts to shift other females to the periphery of the group where they were more vulnerable to predation (Ron et al., 1996). Despite this, and under circumstances where one might readily imagine the advantages of conjoint action, coalitions were conspicuously absent. Similar results were obtained from another very different chacma baboon (Papio hamadryas ursinus) population (Silk et al., 1999) and the possibility has been mooted that the absence of coalitions among females might be a feature of this subspecies, since it also lacks the male–male coalitions recorded from other subspecies (Henzi and Barrett, 2003). However, subsequent data from yellow baboons (P. h. cynocephalus) indicate, too, that coalitions are a feature of only 3% of female–female aggression (Silk et al., 2004). More recently, it has been suggested that the apparent paucity of baboon coalitions does not take into account the formation of ‘‘vocal alliances’’ that obviate the need for more physical support (Wittig et al., 2007). Such alliances occur when one female gives a threat vocalization to signal the likelihood that she will intercede on another’s behalf if the dispute does not end quickly. Even with the inclusion of such vocal alliances, however, females supported each other on only 10% of occasions (dropping to 4.4% for physical coalitions alone). This suggests that, no matter how they are configured, coalitions remain rare. In addition, no observational data were presented on the actual effectiveness of these alliances in terminating aggression. The experimental playback evidence provided by Wittig et al. (2007) is also inconclusive, partly because the experimental design involved playing a threat grunt to a female who had just been threatened by another animal. While threatened females responded more strongly to calls and avoided contact with the signaler and its kin, the fact that these experimental females had been the victims of aggression means that we cannot infer that these calls have the potential to stop aggressors in their tracks. It is also hard to exclude the possibility that victims were in a state of

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Genus

arousal that led them to avoid the aggressors and their relatives (who may, in any case, have been in close spatial proximity—see below) generally and not as a response to these particular calls. A stronger design, where aggressors were played the threat grunts of kin of the animal under attack, and assessing whether this terminated aggression more quickly than under control conditions, where no such vocalization was played, could perhaps provide stronger support. Admittedly, it would be much more difficult to implement since most conflicts are of short duration. This, in itself, questions the effectiveness of providing a signal of potential intervention, given that, in the time taken to produce a call, the incident is likely to have ended anyway. A larger comparative sample from the literature (Fig. 1) generates much the same impression that coalitions are not common (see also Schino, 2001, p. 270). These data are greatly constrained by the precision with which details on coalitions are reported and should be taken primarily as being illustrative; it is particularly difficult to find actual rates of coalition formation reported, to derive them from published accounts, or to determine the exact targets of coalitionary behavior. We know from Seyfarth’s otherwise comprehensive analysis (Seyfarth, 1980, p. 809) of vervet monkeys, Chlorocebus aethiops, for example, only that females form coalitions, but not how often, against whom, or to what ends. Clearly, then, vervet female–female coalitions may be underrepresented in Fig. 1, but, even so, it is not likely that they are common (see Fig. 4 in Seyfarth, 1980), an interpretation

Colobus Cercocebus Procolobus Papio Cercopithecus Presbytis Macaca Chlorocebus Erythrocebus Saimiri Cebus Ateles 0

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corroborated by the recent estimate that coalitions occur in only 3% of aggressive interactions between females (reported as unpublished data in Wittig et al., 2007). At the same time, general reference to coalitions obscures the fact that many female–female coalitions do not target other adult females as predicted by socioecological theory. Family members, for example, assist immature offspring (Chapais, 1992; Cheney, 1977), maximizing the possible adult rank of the supported juvenile, or, as is the case for vervets or blue monkeys, Cercopithecus mitis (Henzi and Lawes, 1987; Seyfarth, 1980), females may cooperate successfully in attacks on adult males. In the case of the vervets (Fig. 2), this constitute 70% of recorded coalitions (Seyfarth, 1980). Nevertheless, it is striking that, first, the highest rates of coalitions are reported for the South American genera, for which grooming and group size do not correlate (Dunbar, 1991) and where one (Ateles) includes no FB species. Second, it is likely that some of the reports reflect captive conditions, where animals are less capable of distancing themselves from conflict. For example, wild Presbytis (now Semnopithecus entellus, the hanuman langur) appear to make little use of coalitions (Koenig, 2000). At the same time, data from free‐ranging capuchin monkeys, Cebus capucinus, show a role for coalitions in status maintenance among females that may belie their relatively low representation here (Manson et al., 1999). The data in Fig. 1 indicate, perhaps above all else, that female–female coalitions, especially when directed against other females, are generally uncommon. However, there is a difference between the importance of coalitions and their ubiquity. The fact that female–female coalitions are mostly rare in FB groups (and those against female targets even rarer) speaks to their conception as an organizing principle for current socioecological theories,

FIG. 2. The photograph shows two female vervet monkeys cooperating to keep a male at bay.

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FIG. 3. The photograph illustrates an example of coalition formation in chacma baboon females. The context is as follows: B and C are sisters and, at the time (2002), the first and third ranking females, respectively. D is the older—and A the younger— daughter of B. Just prior to this photograph, C had threatened B who responded by attacking her. While they were fighting, D approached and threatened B (her mother); that is, she entered the dispute by supporting C. B then threatened D while C, instead of persisting with the coalitionary attack on B, joined her in threatening D. This new coalition was augmented by the arrival of the juvenile A. In the photograph, D is looking toward the male who is her consort partner but who does not get involved. The consequence of this episode is that the ranking B > D > C shifts to B > C > D and, later, B > A > C > D (whereas, without intervention and youngest ascendancy, it would have been B > A > D > C). The anecdote draws attention to the contingent nature of presented opportunities (Barrett and Henzi, 2005), while the photograph itself highlights the importance of spatial coherence in conjoint action (see also Fig. 2).

not to their contingent value in the lives of the individual animals that participate in such events. There is little doubt that coalitions can sometimes be very valuable for particular participants. Figure 3 shows two adult females and one immature female baboon combining forces against a fourth. The consequence of this, pursued over several days at our De Hoop study site in South Africa, was the maintenance of rank by one of the adults and the rise in rank of the immature, both at the expense of the attacked female. Despite the significance of such acts for the participants, we have seen only two such episodes in 10 years at the site. Interestingly, both were characterized by similar relative age‐ and rank‐based configurations of mothers and daughters. This suggests that some of the rarity of coalitions may be ascribed to a corresponding rarity in the combination of circumstances that allow a positive payoff for each of the participants.

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In other words, demonstrating that some females in some populations sometimes engage in coalitionary behavior is not good evidence that coalitions themselves have been selected as the evolutionary response to competition, as current theory assumes. Instead, it suggests that coalitions are one element in a suite of possible responses, and it is this plasticity of response that represents the evolutionary adaptation. Instances where females do not form coalitions deserve greater empirical and theoretical emphasis because this will shed light on the full range of tactics that females can and do pursue and, as importantly, help predict more accurately the circumstances under which coalitions are expected to occur. B. GROOMING To the extent that coalitions are rare, grooming is unlikely to serve as an insurance against unpredictable future need, as postulated by some forms of the social brain hypothesis (Dunbar, 1998). Individuals would need to invest large amounts of time and effort in grooming for perhaps very little or no return, especially as coalitions are more likely to occur when both participants gain an immediate benefit rather than just the individual that needs support (Silk et al., 2004; see below for further discussion of these results). Moreover, any mutualistic coalition formation immediately obviates the need for any prior investment in a partner in order to secure support. Even from a solely evolutionary perspective, the costs of social investment would seem to outweigh the limited benefits likely to accrue. In addition, the cognitive demands of coalition formation would seem to be beyond the limited time horizons of monkeys (Barrett and Henzi, 2005; Hampton et al., 2005; Roberts, 2002). At present, we have no good evidence to show that monkeys can engage in true anticipatory planning: that is, that they can form detached representations of their future needs (Ga¨rdenfors, 1995). For example, monkeys often throw food from their cages when satiated, seemingly unable to recognize that they will be hungry again at a later point (Roberts, 2002). More rigorously, Hampton et al. (2005) found that while rhesus macaques showed robust memory for the type and location of a food reward in an open‐field test, there was no evidence that they could remember when an event occurred; as this kind of episodic‐like memory is argued to be linked causally to the ability to engage in ‘‘mental time travel’’ (Tulving, 1983), the inability to recall the temporal sequence of past events suggests that monkeys also cannot project a sequence of events into the future. We should therefore expect to find that grooming is traded either for something immediately obtainable or which does not require overt monitoring of checks and balances over time (such as tolerance around high‐quality resources). Observational data on baboons support

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the notion that many social decisions are made on the basis of current need in this way rather than on the anticipation of their future needs: female–female grooming patterns tend to reflect contingent events like infant births and seasonal shifts in foraging competition (Henzi and Barrett, 2002; Henzi et al., 2003). In part, this absence of evidence may reflect only the paucity of research on anticipatory planning and the need to distinguish it carefully from immediate planning for current need (where the presence of relevant stimuli and/or the organisms’ internal state can cue behavior). It is, of course, entirely possible that further study will reveal that such abilities do exist. Nevertheless, it is telling that there is so little evidence given that the assumption that monkeys can anticipate their future social needs is central to the construction of current socioecological and, more pertinently, sociocognitive views of monkey life. Nevertheless, even if we cannot argue for the anticipatory use of grooming, it may be used more generally to cultivate dominant animals, if only to maintain spatial proximity and improve opportunities for access to resources in the vicinity of such individuals (Seyfarth, 1977, 1980). If grooming serves this purpose, we would expect to find both direct and indirect competition for access to high‐ranking females (Seyfarth, 1977). Delineating the discrepancy between intended and achieved grooming allocation is the subject of Seyfarth’s influential model (Seyfarth, 1977), and it stipulates not only that the observed allocation will be biased toward adjacently ranked females, as a consequence of competition for access, but also that the ratio of grooming received to that given will, for similar reasons, be rank related. Seyfarth’s own results (Seyfarth, 1976, 1980) together with a meta‐ analysis (Schino, 2001) provide support for grooming up the hierarchy (i.e., where high‐ranking females receive more grooming than low‐ranking females) and a bias toward grooming individuals of adjacent rank as the model predicts. In terms of the formal model, though, which is about the allocation of grooming in relation to rank, the appropriate datum for each female is really the ratio of grooming received to that given (see Henzi et al., 2003; Seyfarth, 1977), and this should be biased by rank (high‐ranking females should receive proportionately more than they give). Here the results are not as clear‐cut. A reanalysis of Seyfarth’s data indicates that while a trend is evident, there are no statistically significant correlations between this ratio and rank in his three vervet groups (data from Seyfarth, 1980, Table II. Group A: rs ¼ "0.62, N ¼ 8, NS; Group B: rs ¼ "0.5, N ¼ 7, NS; Group C: rs ¼ "0.57; N ¼ 8; NS; Fig. 4). Schino’smeta‐analysis, similarly, indicates that high‐ranking females not only receive more grooming but also give more than low‐ranking ones (Schino, 2001).

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A detailed application of Seyfarth’s model to chacma baboons (Henzi et al., 2003; see also Sambrook et al., 1995 for olive baboons) found the same pattern of high‐ranking females both receiving and giving more grooming, while also failing to find, contrary to the model’s predictions, any effect of resource competition on grooming allocation. Specifically, during a period of high resource competition (externally imposed by habitat changes), both female grooming clique size (the number of other individuals that a given female grooms) and partner diversity (in terms of the identity and rank of grooming partners) were higher than during a period of low competition. These findings are contrary to the model’s predictions because competition over access to high‐ranking females would reduce clique size due to the exclusion of low‐ranking females by those higher in the hierarchy, and, as a consequence, result in a lower rank‐related diversity of grooming partners. The absence of such an effect suggests that grooming decisions are not driven by competition for high‐ranking partners, and that grooming ratios should not, therefore, be expected to vary by rank. In fact, given the unavoidable confound of kin and rank (adjacent ranks are likely to be occupied by close relatives), these results are as likely to indicate that high‐ranking animals, who can forage more efficiently, simply

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have more time for grooming, which they provide preferentially to their close kin. Since the value of one’s rank to another individual is relative, not absolute, we expect rank distance to be more influential than high rank per se (Barrett et al., 1999) and, supporting this, Schino (2001) found no effect of rank on the intensity of preference for kin. The real issue here is not only whether Seyfarth’s model describes an accurate, intrinsic modus vivendi for females but also whether there is the expected uniformity within FB species. Our argument has been that there is too much variability to be able to conclude that this is the case (Henzi and Barrett, 1999). Some capuchin monkey species groom up the hierarchy sometimes, but show differences between populations (C. capucinus; Manson et al., 1999), while others groom down the hierarchy in both the wild (C. olivaceous, O’Brien, 1993; C. apella, Di Bittetti, 1997) and captivity (C. apella, Parr et al., 1997). Free‐ranging bonnet macaques, similarly and unusually for macaques, groom down the hierarchy (Sinha, 1998). Blue monkeys, like vervets, compete for access to grooming partners (16% of aggressive interactions) and groom up the hierarchy, but they neither form coalitions nor compete intensely for resources (Payne et al., 2003). Baboons, which often compete over resources, do not compete, directly or indirectly, for grooming partners (Henzi et al., 2003). They do, however, adjust their patterns of grooming in relation to resource competition and the manner in which they do so offers another way to configure the role of grooming. As noted above, Seyfarth’s model predicts that when resource competition increases, and if these resources are clumped and defendable (van Schaik, 1989), we should see a decrease in the grooming partner diversity of high‐ranking animals as females jockey for access to valuable partners. We find, instead, that high‐ranking chacma baboon females at De Hoop experience an increase in grooming partner diversity as food becomes more clumped and levels of aggression increase (Barrett et al., 2002; Henzi et al., 2003). High‐ranking females, in other words, are groomed by more partners when resource competition increases (Fig. 5). We explain this by reference to the theory of biological markets (BM) developed by Noe¨ and Hammerstein (1994, 1995). The goal of market theory is to explain the emergence of cooperation that evolves under the pressure of partner choice. We expect partner choice to be able to keep cooperating animals honest. For this to be so, cooperation must be tied up in the exchange of commodities, where participants have a choice of trading partners and where the value of the commodities relative to one another is set by the law of supply and demand. Allogrooming is an excellent example of a dynamic market of this kind because, as Seyfarth (1977) himself noted, grooming has intrinsic value. Since no animal is sufficiently dexterous to be

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able to groom its entire surface area efficiently (Barton, 1985), allogrooming is a service that can be exchanged either for itself or for some other commodity such as tolerance at a feeding site. According to this interpretation, the observed increase in grooming diversity is a consequence of increased demand, by more females of lower rank, for greater tolerance around other females when food is clumped (Henzi et al., 2003). This is a demonstration of partner choice in operation and, instead of reflecting the shoring up of valuable relationships in case of future need, is a response by females who need to trade grooming in the here and now (Barrett et al., 2002). That is, while this short‐term contingent cultivation of partners may end up having long‐term positive benefits, there is no need to posit the latter as the proximate driver of females’ social choices in the here and now; an explanation in terms of current need is

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sufficient to explain the patterns in the data. In corroboration, we have found that as demand for high‐ranking tolerance increases, so too does the price that low‐ranking females are prepared to pay; there is a significant increase in the relative amounts of time for which high‐ranking females are groomed (Fig. 6). More specifically, there is a strong positive correlation between the difference in ranks between two partners and the relative allocation of effort by the lower ranking of the two (Barrett et al., 2003). With similar results in other contexts (Barrett et al., 1999; Henzi and Barrett, 2002) and from other species (Manson et al., 2004; Payne et al., 2003), it is possible to advance the idea that grooming is a tool whose social deployment is both geared to current need and sensitive to circumstance rather than used to signal the level of mutual support once individual can expect from another. C. RECONCILIATION The term ‘‘reconciliation’’ has been used to label selective affiliative contact between individuals previously involved in an aggressive conflict. This contact can take the form of specific behaviors that signal the occurrence of reconciliation such as ‘‘kissing’’ and ‘‘embracing’’ in chimpanzees, Pan troglodytes (de Waal and van Roosmalen, 1979), but may also consist of general affiliative behaviors such as lipsmacking, contact‐sitting, and grooming (see Aureli and de Waal, 2000; Aureli et al., 2002 for a review). This behavior has been interpreted as a means by which individuals can alleviate the costs of unavoidable aggression, particularly for animals that live in permanent social groups (Aureli and de Waal, 2000). Conflict resolution fits into a view of social life which is essentially cooperative, but where aggression is seen as both inevitable and necessary for the negotiation of individual interests among nonlinguistic animals. Post‐conflict affiliative behavior is therefore crucial to ensure that the positive benefits of group life (e.g., protection from predators) are not lost due to the dispersive effects of aggression on social interaction (de Waal, 1986). However, with respect to primates in particular, the argument has been taken much further than this such that post‐conflict behavior is predicted and explained on the basis of the ‘‘valuable relationship hypothesis’’ (Aureli et al., 2002; de Waal and Aureli, 1997). This argues that when a conflict disrupts the usual pattern of interaction between individuals, it damages the relationship between them and, consequently, jeopardizes the benefits associated with it (Aureli et al., 2002). According to this hypothesis, individuals engage in post‐conflict behaviors in order to preserve the integrity of their relationships with particular individuals; post‐conflict behavior then serves to ‘‘repair the damage’’

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FIG. 6. The impact of rank effects on timed grooming bout contributions when (A) resource competition is high (Period 1) and (B) when it is low (Period 2). The data come from female baboons at the De Hoop Nature Reserve (Barrett et al., 2002; Fig. 4 reproduced with permission from Elsevier). The x‐axis represents the rank distance between the individual participants in a grooming bout. The y‐axis represents residuals from a regression of A’s contribution on B’s contribution to a given grooming bout. The designation of Individual A was conventionally assigned to the first individual to groom in a bout, irrespective of rank. Deviations from zero indicate that one partner groomed significantly more (positive deviations) or less (negative deviations) than the other during a bout. During Period 1, extreme residual values were associated significantly with large rank distances, indicating that low‐ranking females contributed more to grooming bouts than did high‐ranking females, indicating that low‐ranking females invest more in grooming high‐ranking females under conditions of high competition. During Period 2, there was no association between the deviation from grooming equality and rank distance, indicating that rank‐related variation in grooming value was absent under conditions of low competition.

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caused by aggression and leads to ‘‘reconciliation.’’ The reduction in stress‐ related, self‐directed behaviors (e.g., scratching) following reconciliation in both aggressors and victims is related to the restoration of the social bond and the associated reduction in uncertainty regarding the future of the relationship that conflict created (Aureli et al., 2002). Only the relationship repair hypothesis, it is argued, can account for why the aggressor’s, as well as the victim’s, stress‐related behavior increases after conflicts and is reduced following post‐conflict affiliation. As the former were not exposed to aggression in the same manner as the victim, it can only be the uncertainty associated with relationship status that leads them to engage in high levels of stress‐related behaviors. We show below, however, that this is not the only plausible mechanism that can account for the aggressor’s behavior. Since de Waal and van Roosmalen’s groundbreaking study (de Waal and van Roosmalen, 1979), the subject has generated a large literature in which species differences in conciliatory tendency (the probability that a particular conflict will be reconciled) have been widely documented and related to differences in the relatedness and dominance rank of individuals (Aureli and de Waal, 2000; Aureli et al., 1989, 1997; Demaria and Thierry, 2001; de Waal and Ren, 1988), as well as factors such as the intensity of aggression, the decisiveness of conflict outcome, reproductive season, and the presence of infants (Aureli et al., 2002; Call et al., 1999; de Waal, 1993; Kappeler and van Schaik, 1992; Silk, 1996). More recently, the issue of how this relates to the negotiation and functioning of individual interactions over time has been addressed, and a framework for predicting the occurrence of post‐conflict behavior has been developed (Aureli et al., 2002). As mentioned above, this framework is based on the notion that post‐ conflict behavior serves to repair damaged relationships. Consequently, the argument put forward is that post‐conflict reunions are necessary under conditions where individuals will suffer a post‐conflict loss of benefits from a relationship with their former opponents and where within‐group aggression undermines a relationship that is perceived as valuable by both partners (Aureli et al., 2002, p. 336). As a result, post‐conflict reunions should occur more often after aggressive conflicts between individuals with more valuable relationships (Aureli et al., 2002, p. 336). Observational data provide some support for the idea that animals that engage in more positive social interactions overall (taken as the measure of ‘‘value’’) also show higher rates of conflict resolution (see Aureli et al., 2002 for a review). A small number of experimental studies help establish the causality of this relationship. For example, Cords and Thurnheer (1993) manipulated the value of individuals to each other experimentally by training pairs of long‐tailed macaque females to cooperate on a task that required mutual tolerance to obtain a food reward. Reconciliatory tendencies within

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pairs increased following this training, suggesting that females were more likely to reconcile following aggression when the opponent was more valuable to them. Despite this body of evidence, however, there are some outstanding issues that are not fully accounted for within this framework. For example, only a small proportion of all conflicts are actually reconciled. The ‘‘conciliatory tendency’’ ranges from 14% for rhesus macaques, Macaca mulatta, to a maximum of 41% for stump‐tailed macaques, M. arctoides (see also Kappeler and van Schaik, 1992). This means that, even among those species designated as showing a high conciliatory tendency, the majority of fights are not reconciled. Equally, while a number of studies have shown that kin reconcile at much higher rates than non‐kin, it is nevertheless the case that kin rarely reconcile any more than 50% of all disputes (Kappeler and van Schaik, 1992). This raises the question of how important reconciliation actually is to the repair and maintenance of relationships. Second, in those studies in which the context of aggression was recorded (Aureli, 1992; Castles and Whiten, 1998), the majority of reconciled conflicts were those where the observer was not able to determine any apparent context. As it seems unlikely that animals would waste time and energy attacking each other without cause, it is reasonable to assume either that we are missing something important in these interactions or, perhaps, simply looking at them in the wrong way. This suggests, in turn, that a sharper focus on the period prior to aggression, in tandem with a greater theoretical emphasis on the goal of such aggression, may help at least as much as the post‐ conflict period in identifying the underlying motivation for conflicts and their resolution. Silk (2002a), for example, has argued that ‘‘random acts of aggression and senseless acts of intimidation’’ have been selected for in social groups as a means of asserting and maintaining dominance relationships: random, unpredictable aggressive attacks exert the maximum stress on the subordinates to which they are directed, while keeping stress on the aggressor relatively low. Aggression causes the victim to mount a physiological stress response that has adaptive short‐term benefits but carries severe longer‐ term costs, including reduced fertility, if the response becomes chronic. The lack of predictability, in terms of the timing of attacks and their duration, creates these chronic conditions and can explain why selection would favor such behavior on the part of dominant animals. If this can explain patterns of aggression, at least partly, then the idea that post‐conflict behavior serves to repair valuable relationships damaged by aggression is called into question. Aggression used in this manner is, by definition, not damaging a valuable relationship, but establishing and maintaining the boundaries of

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particular dominance‐related relationships. Any subsequent reconciliation under these circumstances is therefore difficult to incorporate into the relationship repair hypothesis, according to Silk (2002a). Finally, there is inconsistency in the literature as to whether the ‘‘aggressor’’ or the ‘‘victim’’ makes the first peaceful contact after conflict (de Waal, 1993; de Waal and Ren, 1988; Judge, 1991; Kappeler, 1993). This is true both between and within species. Although in the majority of cases the victim tends to make the first move (Kappeler and van Schaik, 1992), there are a number of species in which the aggressor is statistically more likely to do so, and at least one species (P. hamadryas) in which both victim and aggressor are equally likely to attempt reconciliation (Castles and Whiten, 1998; Petit and Thierry, 1994). These findings raise two interesting questions. First, if reconciliation is a straightforward act that repairs a damaged relationship, why should there be this variation? Second, and related to this, if it is the act of aggression that damages the relationship, why should the victim of aggression be more likely to reconcile? Aureli et al. (2002) suggest, on the one hand, that a more nuanced assessment of the costs and benefits of particular kinds of interactions may well account for some of this variation and, on the other, that certain relationships are so critical to social functioning that they need not be reconciled (among cooperative breeders, like tamarins, e.g., Schaffner et al., 2001). An alternative view, however, is that reconciliation may not be tied to the repair and protection of valuable relationships. Silk (1996, 1997, 2000, 2002b) has proposed that post‐conflict behaviors are ‘‘signals of benign intent.’’ These inform the recipient that the current conflict is over and that the actor’s intentions are no longer aggressive. She argues that such signals may be favored by natural selection because they enable former opponents to coordinate their interactions (Silk, 1997). This is a return to the idea that post‐conflict behaviors function to preserve the cohesion of social groups rather than repair and protect particular valuable relationships. In other words, Silk’s reading of the available data (Silk, 2002b) is that post‐conflict behavior is a contingent response to current circumstances, allowing animals to achieve short‐term objectives (e.g., access to resources, tolerance by preferred partners) and does not require a long‐term, relationship‐based component. The rise in stress‐related behavior by aggressors, for example, can be explained as a result of increased arousal following aggression and need not be associated with relationship uncertainty. The fact that redirected aggression toward uninvolved third parties can reduce self‐directed behavior as effectively as post‐conflict affiliation with a former opponent is consistent with this view (Silk, 2002b).

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Silk’s proposals can also account for low rates of post‐conflict affiliation because, if these are needed only to reduce short‐term uncertainty, other tactics (e.g., increasing distance from an aggressor) can be equally effective. If the aggressor is far away, further aggression is much less likely and uncertainty reduced in equal measure. Silk (2000) also argues that the relatively higher rates of post‐conflict affiliation between kin are better explained by her benign intent hypothesis than by the relationship repair hypothesis. The latter predicts that post‐conflict affiliation should occur most often within dyads that value a relationship more and for whom damage to a relationship is more costly. This in turn is argued to be a function of how ‘‘secure’’ the bonds are between individuals. Consequently, as Silk (2002b) argues, kin should show low rates of reconciliatory behavior because, according to the relationship repair hypothesis, although equally valuable, their bonds are less likely to be damaged by conflict due to their greater security (Cords, 1988). This security is at least partly attributed to the benefits that accrue through kin selection. The fact that kin actually engage in post‐conflict behavior at equivalent, or even higher rates, than non‐kin is not good support for the relationship repair hypothesis, but does fit with the notion that individuals are signaling an end to aggression. Kin‐based reconciliation is then more common not because of a greater need to salvage damaged relationships but because, as we go into below, kin may be more strongly motivated to remain in close spatial proximity. They therefore have an active need to signal an end to hostilities and cannot use alternative responses to manage and cope with the post‐conflict period such as maintaining distance or avoiding former aggressors. The apparent lack of context of many aggressive disputes and the tendency of aggressors as well as victims to reconcile are also accommodated more satisfactorily by the benign intent hypothesis because, in Silk’s view, reconciliation is an antidote to random, intimidating aggression. Individuals subject to random attacks may be (understandably) wary of former attackers since they cannot predict the nature of any particular interaction. Reconciling reduces this short‐term uncertainty in interactions for both aggressors and victims, enabling aggressors to engage in behaviors that serve new goals (e.g., a former aggressor may now want grooming from a subordinate). Support for this comes from the findings that, among baboons, females tend to reconcile selectively with females that have young infants whom the conciliatory female goes on to ‘‘handle’’ (i.e., engage in various forms of physical contact; Silk et al., 1996). Furthermore, rates of reconciliation track rates of infant handling by non‐mothers, and females also reconcile more frequently with the mothers whose infants they are most eager to handle. All of this suggests that it is the short‐term

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goal of handling infants that drives conciliatory behavior not the value or quality of the relationship with the infant’s mother (Silk, 2000; Silk et al., 1996). Silk (2002b) also points out that even those studies, like Cords and Thurnheer’s (1993), that have been taken as compelling evidence of the relationship repair hypothesis are open to an alternative interpretation. Cords and Thurnheer’s experiment (Cords and Thurnheer, 1993) assumed that the value of the social bond between two animals had been manipulated but, strictly speaking, it was the value of a partner with respect to an individual’s own success on an instrumental task that was manipulated, not the value of a social bond as such. In the cooperative feeding task, monkeys could only feed if their partner was tolerant of their presence. If one monkey was intolerant or wary, and left the feeding station, then neither monkey was able to obtain the food reward. It is possible, under such circumstances, that animals learned to use reconciliation instrumentally: females became more conciliatory because this enhanced their own success at the task rather than because they valued their relationship with their partner more highly (Silk, 2002b). As such, signals of benign intent would enable animals to communicate their intentions to behave peaceably around their partner. It has been suggested that the benign intent hypothesis, rather than being an alternative, is complementary to the relationship repair hypothesis (Cords and Aureli, 1996; de Waal, 2000). In this view, it is simply an explanation of the proximate motivation for the resumption of contact between former opponents. Ultimately, however, females are motivated to resume contact because repairing valuable relationships contributes positively to long‐term reproductive success. Silk’s counter (Silk, 2000, 2002b) is that the long‐term consequences stemming from short‐term post‐conflict behaviors do not mean that natural selection has favored the evolution of reconciliatory behaviors because they enhance long‐term social bonds. The selection pressures acting on signals of benign intent may be quite different from those that shape social bonds between females. It is, of course, possible that long‐term benefits do accrue from post‐conflict behaviors—this is, after all, the reasoning behind Grafen’s ‘‘phenotypic gambit’’ (Grafen, 1984)—but the benign intent hypothesis is complete in itself and sufficient to account both for the observed patterns and to explain the evolution of reconciliatory behaviors. In the absence of any additional explanatory power, Silk regards it as unnecessary to add an extra, long‐ term, relationship‐related benefit. Why, then, are so many researchers persuaded by the relationship repair hypothesis?

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Silk’s suggestion (Silk, 2002b) is that it is because reconciliation is an anthropomorphic concept, deriving originally from a direct analogy with human conflict (de Waal and van Roosmalen, 1979). Consequently, the relationship repair model is a compelling one because it fits so well with our own folk model of how and why we resolve conflict (p. 38). This is something that we have argued is also true of the relationship concept itself (Barrett et al., 2007). In Section IV, we show how a reconsideration of the concept of a primate ‘‘relationship’’ is a logical extension of Silk’s proposition that reconciliation is a short‐term signal of benign intent (Silk, 2002b).

IV. RELATIONSHIPS Hinde’s original proposition (Hinde, 1976, 1983) was that relationships between animals could be abstracted from the frequency, quality, and patterning of individual social interactions. This further implied that, as emergent, irreducible phenomena, relationships were greater than the sum of their parts. Consequently, although relationships are, at base, quantitative measures of overt behavioral patterns such as grooming, proximity maintenance, coalitionary support, and post‐conflict behavior, a sense has developed that these behaviors are not constitutive of the relationship itself. They are, instead, only the surface reflection of a deeper underlying bond. For example, Cords (1997) states: ‘‘Validation of grooming and proximity measures as indicators of social bond strength comes from correlations between them and other types of behavior’’ (p. 27; our emphasis), before going on to admit that ‘‘there is little direct evidence that grooming is used to cultivate valuable social bonds’’ (our emphasis). Similarly, Strier (1999) writes, ‘‘Female kin in these cohesive, matrilineal groups form affiliative bonds that are expressed through proximity, grooming, and agonistic support. . .’’ (p. 300; our emphasis). Here, then, we have a clear separation between the relationship itself and the behavioral measures used to identify and assess it. Note, too, that the focus of these articles is neither on the nature of relationships per se nor are these statements presented as definitions; the existence of relationships is taken to be axiomatic and a springboard for the elaboration of primate social complexity. This reification of relationships turns them into a much more anthropomorphic construction, akin to the concept of friendship in humans. This, as Silk (2002c) suggests, following Hinde (1983), is something that we define by the kind of emotional bond that exists between individuals, and not merely by the kinds of things they do together. As Silk (2002c) points out, this makes it difficult to identify whether anything like human friendship can objectively be identified in other species, since we cannot easily gain

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access to another animal’s emotions. The same applies, in our view, to current notions of all primate relationships: if a bond or relationship is constituted by something other than the behaviors used to quantify it, how do we get at the relationship itself? What would constitute good evidence to suggest that such bonds exist? A related problem is that the abstraction of relationships from a series of interactions introduces a temporal component that may also reflect our own folk‐psychological constructions rather than those of the animals themselves. The notion of grooming as something that ‘‘cultivates’’ or ‘‘maintains’’ a social bond is based on the assumption that the function of relationships is to ensure unstinting mutual support (Dunbar, 1998) from coalition partners at unknown, unpredictable future dates. This introduces a prospective element to relationships that motivates females to maintain bonds with a set of familiar, valuable partners. While an evolutionary account does not require females to make any cognitive assessment or have any conscious awareness that this is what they are doing, it is also true that this prospective element has been incorporated into the social brain hypothesis of increased brain size. There is, therefore, an assumption that females’ grooming decisions derive from cognitive assessments of the likelihood of future need. Whiten (2000), for example, in an exploration of the kinds of social complexity that would select for enlarged brains, suggests that this complexity is inherent in the fact that primate relationships vary in stability, creating a pressure to track their status, so that there is a consequent pressure to ‘‘pick up information that might not be vital at the time, but which may be utilized adaptively later on.’’ Similarly, Aureli et al. (2002) suggest that the reason why both aggressors and victims display post‐conflict anxiety is that they have some overt recognition of future costs. They argue that it is difficult to explain the stress response in former aggressors in terms of Silk’s hypothesis (Silk, 1996, 2002b) because aggressors actually face a very low risk of renewed attack. Instead, Aureli et al. (2002) state that it is the uncertainty about the future of their relationship, and the potential loss of future benefits, that creates an additional source of post‐conflict anxiety that affects aggressors as well as victims. It is difficult to construe this as a purely evolutionary argument, with no overt, cognitive component, because it suggests that aggressors understand that they have put their future relationship at risk and are not simply mounting a physiological response to the stress of aggression (which is all that a functional, evolutionary account—and the benign intent hypothesis—requires). In these examples, then, relationships are assumed to reflect ‘‘propositional knowledge’’ (Cheney and Seyfarth, 2005) on the part of the animals: the individuals concerned ‘‘know that’’ they have relationships with others (i.e., possess a declarative, explicit knowledge),

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and are also assumed to know that such relationships require ongoing maintenance in order to provide benefits, and that aggression puts this at risk. The costs of conflict are therefore construed as future, rather than current, costs. Moreover, the formulation by Aureli et al. (2002) requires this prospective ability in order to distinguish it from Silk’s hypothesis: remove the temporal component (the uncertainty about the future of the relationship), and the argument reduces to the benign intent model, where animals act to reduce current uncertainty (which may or may not have long‐ term consequences). There is, therefore, a distinction to be maintained between an evolutionary account of relationships in terms of their fitness‐ enhancing properties and an evolutionary account of relationships as a selective force shaping primate cognitive capacity. As these examples illustrate, that distinction is often blurred, so that evolutionary and proximate explanations become mutually reinforcing. There is no doubt that certain individuals in FB groups—most notably close kin such as mothers, daughters, and sisters—show higher levels of affiliation than others, that they do so flexibly and contingently, and that consistent patterns of affiliation can often be detected over time. There is also recent evidence to suggest that sociability has positive fitness effects: Silk et al. (2003) have demonstrated, for female yellow baboons at Amboseli, that more sociable females rear a greater number of offspring to the age of 1 year. The unanswered question in all such studies, however, is whether females can abstract across successive interactions in a way that allows them to construe their engagement with others in terms of their relationships and then reason prospectively about how to cultivate, manage, and protect them. This, as we argue elsewhere (Barrett et al., 2007), is not something for which we currently have any good evidence. There are, on the other hand, data to suggest that short‐term, contingent, and instrumental choice of partners is common in FB primate groups. At De Hoop, measures of grooming and proximity indicate marked inconsistency across years in the degree to which females were ranked as another’s primary partner, where changes in preference were associated strongly with reproductive events (Barrett and Henzi, 2002). This, by itself, might explain why more sociable females are more reproductively successful: females with young infants attract significantly more social attention than non‐ lactating females (Altmann, 1980; Henzi and Barrett, 2002; Silk et al., 2003), with the result that those females who give birth more often experience increased levels of social interaction. If so, causality may run in the opposite direction to that assumed for Amboseli (Silk et al., 2003). There is also evidence that individuals groom and maintain proximity to others on the basis of short‐term concerns, such as access to infants, tolerance around food and water resources, access to ‘‘skilled’’ individuals and avoidance of

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aggression from more dominant individuals (Barrett and Henzi, 2001; Chapais, 2006; Henzi et al., 2003; Kapsalis and Berman, 1996; Muroyama, 1994; Silk, 1992; Stammbach, 1988). We have shown, more recently, that female relationships, in both the De Hoop and Drakensberg baboon populations, differ qualitatively in different seasons (Henzi et al., in preparation). The application of new and powerful network analysis techniques (Lusseau and Newman, 2004) revealed that, in both populations, when food was plentiful, female associations, at both sites, were either only ‘‘brief’’ (measured in hours) or ‘‘casual’’ (measured in days). In contrast, when food was scarce, females formed ‘‘constant companionships’’ (the lagged association rate was constant over time). It is difficult to explain these results with reference to quantitative variation in factors like nearest neighbor distance or feeding competition since the study sites differ ecologically and the females’ ecological responses to food availability therefore differ across sites accordingly. Moreover, and more pertinently, females did not generally resume relationships with the same individuals following the period of seasonal dissolution, while the downgrading of relationships did not lead to group fission or fragmentation. This suggests that models of social life predicated on the presumption that grooming acts as a ‘‘social glue’’ may also need rethinking (Dunbar, 1992). If relationships can dissolve at certain times of year with no adverse effects on group integrity, and female dissolve and form bonds with different individuals across time, it becomes harder to see why ecologically and demographically induced reductions in grooming time lead eventually and inevitably to permanent fission. Interestingly, in his original derivation, Dunbar (1992) found no relationship between group size and social time for the Papio baboons and concluded that the relationship was masked by other factors (note that, for the purposes of these and related analyses, Dunbar treated social time as equivalent to grooming time, on the basis that grooming accounts for over 95% of social time in this genus). It now seems that his alternative suggestion, that group size is genuinely irrelevant in the case of baboons, may have been the correct one. Or rather, group size may be irrelevant in the sense that Dunbar (1992) originally assumed: a group represents a network of bonds whose functional value requires high temporal integrity. As we suggest below, however, the argument may retain its value if it is reconfigured. Female bond strength and duration have also been investigated in Amboseli yellow baboons, using an index of sociality calculated from grooming and proximity scores (Silk et al., 2006a,b). This revealed that many dyads had very weak bonds, while very few had quite strong bonds and that, on average, a female formed only 1.5 ‘‘very strong’’ bonds per year

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(Silk et al., 2006a). These are similar to results obtained from Moremi, Botswana, on chacma baboons, where females groomed, on average, only 8 of the 18 available females and fully half of the female cohort devoted the majority of their grooming to just 1 other female (Silk et al., 1999). Moreover, out of a total of 1430 coresident dyads at Amboseli (coresident referring to dyads residing in the same troop at the same time), only 14 maintained a close bond for at least 5 years, which is not too surprising since the mean duration of coresidence was only 3.47 years (Silk et al., 2006b). In addition, bond duration may have been overestimated since Silk et al. (2006b) did not require high sociality index scores to be maintained across consecutive years, allowing for a 1‐year gap between ‘‘consecutive’’ years. If Female B, for example, was among Female A’s top three partners in 1992, 1993, 1995, and 1996, but not in 1994, the duration of the close social bond was still scored as 5 years (Silk et al., 2006b). In addition to overestimating bond duration slightly, this also presents a picture of social bonds as having significantly more temporal consistency than is experienced by the animals themselves. Such short coresidence times (given that females who reach adulthood can normally expect to live for another 10 years: Altmann, 1980; Altmann and Alberts, 2003), together with the low numbers of ‘‘very strong bonds’’ formed each year and the small number of dyads sustaining bond durations of 5 years or more, suggest that Amboseli females may well also display cyclicity in bond quality and that dynamic contingency in the availability of individuals then characterizes the lives of all female baboons. This perspective makes sense because the ever‐present vagaries of predation, disease, and other sources of mortality can lead to the sudden and irreparable loss of a particular social partner. Fission events can also lead to the loss of partners: the short average coresidence times at Amboseli are very much a consequence of groups splitting over time. Interestingly, these fission events often result in matrilines splitting, where a mother will leave her daughter(s), despite the existence of a strong bond between them (Silk et al. 2006a,b). This is something that has also been found in chacma baboons, where it was suggested that females distribute themselves in ways that result in an improvement in their dominance ranks (Ron et al., 1994). Given the frequency of such events over a female’s life, as the Amboseli data and our own indicate, one might expect selection on females either to sustain several partnerships at any time (which may explain the ‘‘many weak bonds’’ at Amboseli) or to recover from the loss of a partner by rapidly seeking a replacement. In this context, it is worth considering, as one example, the work of Engh et al. (2005), who showed that the loss of a close kin partner to predation raised cortisol levels in chacma baboon females. They interpreted this to be

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a stress response to the loss of a close social partner, a consequent increase in social isolation and, as such, a form of bereavement. Cortisol’s effects are, however, many and varied and an acute rise in cortisol is also associated with increased alertness and readiness to act (Korte et al., 2005). While the interpretation by Engh et al. is plausible, it is not the only one consistent with their findings. The observed stress response could actually reflect a reaction to the predation event itself, and the need for increased vigilance and alertness in order to avoid suffering the same fate. The ‘‘bereavement’’ interpretation, which connects to the idea of long‐term bonds, is based on the fact that only females who lost a close relative showed this acute response. However, no control was made for the fact that close kin tend to cluster spatially (Rendall et al., 1996), and it is therefore reasonable to suggest that proximity at the time of predation induced greater stress in the survivor. The argument that the transience of the rise in glucocorticoid levels was due to an increase in grooming and partner diversity, driven by a need to reduce social isolation following the loss of a close social partner, is similarly plausible but explicable without recourse to any sense of the need to establish new, enduring bonds with other females. It is possible that females increased their grooming in response to an increase in oxytocin, as the authors suggest, but merely to increase social contact in general and not as a means of establishing new social bonds with particular individuals. Again, this could be a response to the predation event itself and an attempt to occupy more central, safer, positions in the troop where, by definition, more individuals will be encountered. The real point to be made is that interpretation in terms of social isolation rests on an anthropocentrically derived, folk‐theoretical assumption that enduring social bonds exist and are recognized by females, so that it is specifically the disruption of a social bond that causes this physiological response (here Engh et al., 2005, draw explicit parallels between the baboons’ response and that of bereaved or lonely humans). The suggestion that females are responding to their social isolation and that they attempted to cope with their loss by extending their social network, plus the juxtaposition of the baboons’ response with human psychological responses, implicitly promotes the view that relationships are ‘‘real’’ and are valued by the baboons in and of themselves. The assumption itself remains untested. The alternative view is that there is no need to interject an anthropocentric concept of social relationships in order to derive an adaptively plausible explanation. The findings can be equally well addressed by the proposition that females have been selected to respond adaptively to short‐term dynamic changes in their environment, using short‐term social tactics to reduce their own risk of predation. Given that such stressful events are

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likely to be common, as Engh et al. (2005; see also Beehner et al., 2005) also point out, selection might be expected to produce females that remained relatively phlegmatic in the face of social loss, and whose ties were consequently likely to be flexible and contingent. Indeed, it is likely that this kind of social response, acting over the short term in response to specific events, leads to the correlation between sociability and offspring survival. Rather than long‐term social bonds sustained with particular individuals increasing fitness, it could be the ability to seek out appropriate short‐term social interactions with many individuals in response to stressful, reproductive, and other kinds of events that underpin offspring survival. Short‐term contingent responses of this kind, if appropriate, must then naturally translate into long‐term adaptive responses. Given the present lack of evidence to demonstrate that female monkeys possess the kinds of analogical reasoning abilities (Thompson, 1995; Thompson and Oden, 2000), prospective reasoning (Roberts, 2002), or episodic memory capacity (Hampton et al., 2005) needed to prospectively manage enduring, long‐term social relationships, combined with the short durations over which females coreside in troops, it may be that recasting both the social brain hypothesis and socioecological theories of female coexistence to account for contingency will yield real dividends. At the least, this approach proffers a competing hypothesis of greater validity than the statistical null models that are currently relied on (Barrett et al., 2007). For those who are concerned only with the evolutionary function of relationships, this will seem like something of a nonargument, since what may or may not go on in the animals’ heads is clearly irrelevant. However, the point is worth making because functional behaviors require proximate mechanisms and we need to ask what prompts and produces behavior, as well as how it contributes to fitness (Tinbergen, 1963). The separation of mechanism and function is essential because, with primates especially, it is all too easy to elide the two and slide between evolutionary and proximate explanations: an animal that acts as if it knows that its relationships are valuable and worth protecting may well be doing so in an evolutionary sense, but not necessarily at a more proximate level. Natural selection can and has produced rules of thumb that lead animals to behave in their own interests, without any cognitive assessment of what they are doing, or at least without the kinds of cognitive assessment we attribute to them. Our own folk‐ psychological understanding of female primates, and its success with respect to functional explanations of social behavior, cannot be taken to indicate that we understand anything about the ‘‘folk psychology’’ that female primates might use to understand each other. This is a point worth emphasizing because this elision between proximate and ultimate explanations then acts to circumscribe the range of possible functional hypotheses that are actually

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put to the test, so that only those that address an intentional conception of primate action are considered. Owren and Rendall (2001), for example, discuss this issue in some detail with respect to primate vocal signaling studies. The argument, then, is for a specific application of Occam’s razor to theories of female coexistence: the assumption that females have an overt cognitive recognition and prospective understanding of their relationships is not needed to explain the patterns we see in the data. Note that this is not an argument for evolutionary parsimony: evolution need not be parsimonious and parsimony itself is not an inherent virtue of evolutionary explanation (Barrett et al., 2007). Rather, our argument is that this extra hypothetical construct is superfluous when attempting to account for female social engagement in a satisfactory manner. In effect, this means removing the temporal component from relationships as perceived by the females themselves. We, as humans, can, of course, continue to abstract over interactions to come up with ‘‘relationships’’ (sensu Hinde, 1981) that may be informative with respect to many evolutionary questions, but we need to recognize that such relationships do not correspond to any real‐world entity or overtly represented as such in the animals’ heads; that is, we cannot assume that the temporal component introduced by abstraction over arbitrary, human‐relative time periods has any necessary relevance to the animals under study or provides the proximate motivation for the behaviors they display.

V. A SPATIAL APPROACH TO SOCIAL INTERACTIONS Even without a human‐like representation of time, social animals are still obliged to contemplate space. The recognition of this necessity drove formulations of the functional significance of gregariousness from early on, where both the positive and negative consequences of particular spatial arrangements were assumed to underpin individual social strategies in relation to both predation and foraging (Hamilton, 1971; van Schaik, 1983). If females use social contact and proximity to jockey for position and influence within spatial confines, and monitor others to facilitate this, we can explain variability in social engagement, its contingent and instrumental nature, and its ultimate value without any assumptions about the conceptual, representational knowledge underpinning action, or any projection of this through time. In addition, if we think in terms of spatial integrity alone, Dunbar’s ‘‘social glue’’ argument retains its value, since it is the cohesion of the group in space that becomes important, not the cohesiveness of particular subgroups over

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time. The inevitable spatial fragmentation of large groups, and the consequent inability to keep in contact with other group members, may be all we need to explain why large groups tend to fission. The variability in patterns of fission among baboon females seems to fit with this view: females may leave a group with the putative father of their offspring to avoid infanticide (Henzi and Barrett, 2003), they may fission in such a way that matrilines stay together (Nash, 1976), or in a way that enables each female to improve her rank (Ron et al., 1994). We can also reconfigure coalitions along these lines if we consider them to be the presentation of a spatially integrated ‘‘united front’’ by two or more females in response to current need. Such ‘‘coalitions’’ could act to reduce social stress on individuals by reducing the immediate likelihood of displacement or aggression, thus fulfilling their hypothesized socioecological function. Maintenance of spatial proximity may therefore serve as a ‘‘passive’’ form of coalitionary support, something Seyfarth (1980) originally hinted at, and reflect an immediate, dynamic response to shifts in partner location. In addition, the spacing of individuals can impede or enhance the likelihood of more active forms of coalitionary support. For example, juvenile and high‐ ranking female capuchins tend to be found in the center of the group, with the result that these females regularly support their juvenile kin in conflicts. Low‐ranking, spatially peripheral females rarely support their juvenile kin because, quite literally, they are not in a position to do so (O’Brien and Robinson, 1993). The advantage of immediate, spatially driven responses is that this kind of active coalition formation is then, as we have argued, simply an additional component in a suite of social tactics. Its rarity in the wild and the lack of evidence that participation is secured by prospective, reciprocal investment cease to be problematic because coalitions no longer need to bear the explanatory weight that past formulations placed on them. As Silk et al. (2004) have demonstrated, coalitions are best seen as mutualistic interactions that females adopt for their immediate individual benefit rather than as the foundation on which female relationships are built. Indeed, it is interesting to note that the link between coalitions, grooming, and relationships appears to have arisen initially because of an assumption that reciprocal altruism and the iterated prisoner’s dilemma (Axelrod, 1984; Axelrod and Hamilton, 1981; Trivers, 1971) were the best theoretical models to explain this behavior (Cheney and Seyfarth, 1984) rather than mutualisms. The short‐term costs that females bear when aiding their coalition partners, and the inherent problems of cheating that occur within the prisoner’s dilemma thus generated, are only avoided by the iteration and reciprocation of such acts over time (which, in effect, transforms the payoff matrix into a mutualism game). Females need to form

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long‐term, temporally consistent relationships (i.e., iterated interactions with the same partner over time) because this is the only way to offset their short‐term costs. If coalitions are, in fact, mutually beneficial at the time, and there are no short‐term costs to offset, then long‐term relationships become unnecessary to explain female social functioning in the context of coalition formation. In addition to coalitions, the apparent tendency of many FB species to groom up the dominance hierarchy may involve a similar tendency to seek tolerance around higher‐ranked animals both for the benefits this may offer directly, and to reduce the likelihood of interference by third parties while in a dominant’s zone of tolerance. This spatial model also brings out the importance of kin as affiliative partners, both evolutionarily and ontogenetically. To the extent that inclusive fitness acts as a counterweight to a delay in—or absence of—reciprocity, association with kin allows females to breathe a little easier. The costs of maintaining proximity to kin in terms of feeding competition can be traded off against the evolutionary advantages accruing from kin selection, while spatial coalitions of matrilines arise naturally across development as mothers maintain close proximity to their offspring. Offspring learn the advantages of social support provided by their mothers, both passive and active, initially against their older siblings, but later against other individuals too. Close kin will, as empirical data suggest, be likely to show high rates of affiliation with respect to this kind of passive coalitionary behavior, but need not display any such fidelity with respect to other, more active, forms of engagement, where the value and competence of their partner may take precedence (Chapais, 2006). Learning the value of associating with particular individuals through time can, of course, be seen as a form of long‐term relationship. To reiterate, though, this remains a purely metaphorical usage, such a relationship is not something of which the animal itself needs to be aware nor which it is motivated to conserve. In essence, then, we are arguing for a more dynamic, contingent, action‐centered notion of primate social engagement that does not reify concepts that, as far as we know, have only human significance. Finally, this spatially oriented approach also fits with Silk’s et al. hypothesis (Silk et al., 1996) that reconciliation acts as a short‐term signal of benign intent. In all cases, such maneuvering is performed in the ‘‘here and now’’ without the need to posit any advanced form of future planning. Kin and non‐kin will reconcile, regardless of relationship status, because it is not long‐term relationship ‘‘value’’ or ‘‘security’’ that is at stake, but the need to remain within the ambit of protective others for the immediate advantages that proximity brings. Equally, the high number of nonreconciled conflicts may occur under conditions when individuals have been actively attempting to increase their distance from others (i.e., prior aggression is explicitly

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aimed at decreasing proximity) and reconciliation would defeat the object of the exercise. Rejection of the notion that females have an overt cognitive concept of a relationship does not, therefore, mean rejecting entirely the notion that social engagement is complex, only that such complexity may be dynamic and emerge from ongoing spatial engagement in real‐time rather than reflecting complex cognitive cost‐benefit decisions arising from the integration of information across many social events and many social actors (Barrett et al., 2007). One very great advantage of thinking in this way is that it includes New World monkeys as a matter of course, whereas they have often been excluded under the standard ‘‘bonds serviced by grooming’’ model (Dunbar, 1995) because they tend not to display such intense grooming as Old World monkeys, and instead make use of short, discrete affiliative events such as ‘‘embracing’’ (Schaffner and Aureli, 2005). To summarize, our view is that the only true long‐term stable bonds shown by FB primates are with the group as a whole, which, after all, is what we would expect from female philopatry. Within a group, the unpredictable nature of survival and fission; the variability in births over time; and the stochastic nature of male immigration, infanticide, and other demographic events preclude the formation of life‐long enduring bonds for most females and promote a short‐term, more instrumental approach to social interactions with others. In this respect, it is interesting that Silk (2002; Silk et al., 2006a,b) argues so strongly for the existence of ‘‘relationships’’ as real entities in the life of female primates, rather than as human analytical abstractions, given her views on the short‐term value of reconciliation. This may be because she views them in purely evolutionary terms although, even then, her own argument about reconciliation would apply: the selection pressures acting on the proximate mechanisms by which females engage with each other may be very different from the evolutionary forces that have shaped fitness‐enhancing sociality in general. We argue that female ‘‘relationships,’’ as seen by females themselves, need not, and probably do not, take the long‐term, temporally consistent form that has been attributed to them, and that our argument for ‘‘expedient, quotidian cognition’’ (Barrett and Henzi, 2005), with short‐term contingent response to current need, may provide a more satisfactory evolutionary account of female coexistence and cognitive capacity.

VI. CONCLUSIONS Among the measures of success of any decent heuristic schema is that it is self‐limiting. That is, it will, sooner or later, generate information that cannot readily be shoehorned into the existing framework. Any successful

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accommodation of discrepant data requires a transformation or reconfiguration of the very account that generated the data in the first place and paves the way for a new enterprise (Kuhn, 1962). Our proposition is that this is happening to the program that set out to understand local resource competition in FB groups as a social problem that is mediated by conjoint action. The linkage of observable social acts—grooming, reconciliation, and coalitions—to one another through relationships has structured our view of social life and made possible the serious consideration of natural cognition. At the same time, though, it is a formulation that is consistently situated, inadvertently or not, in the structuralist framework that has been so congenial to primatologists from the beginning. So, certain ecologies or resource bases (‘‘clumped’’/‘‘dispersed’’) beget particular social forms (‘‘uni‐male’’/ ‘‘multi‐ male’’; ‘‘nepotistic’’/‘‘egalitarian’’) that make specific demands on participants. The problem is that in a world sufficiently consistent to favor consistent response, selection for the individual propensities on which this must be built is not likely to favor intelligence, and hence larger brain size, because evolved rules of thumb will be more cost efficient (Plotkin, 1994). The reality, of course, is that a monkey’s world is full of surprises and it is this, along with a resource base that can underpin the evolution of large brains (Fish and Lockwood, 2003), that makes cognitive flexibility profitable. In the first place, surprises are ecological since resource structure and gross availability vary both temporally (Barrett et al., 2003; Koenig, 2000) and spatially (Henzi et al., 1992) within the home range. Second, surprises are social. If the value of a particular behavior depends, in large part, on what others are doing (Sutherland, 1996), then a monkey can expect to be confronted by less predictable, contingent responses. As we have argued (Barrett and Henzi, 2005), this all points to the expectation that ambitious monkeys will not or cannot rely on a suite of consistent responses but must tailor their behavior to immediate, local circumstances and affordances. It is therefore not surprising that coalitions are infrequent and that reconciliation does not always occur. For this reason, it seems to us that good research dividends can now be had by viewing female social behavior more globally, so that the deployment of all alternative responses is empirically contextualized. It may help to think of this as accentuating the negative, since the point is that the absence of reconciliation, for example, does not necessarily signal the absence of an appropriate or optimal response to local circumstances. As a final coda, this does not mean necessarily that response repertoires are constraint‐free. It is likely that founder‐effects and evolved differences among demes will tune social reaction norms (Kappeler and van Schaik, 2002) and produce inter‐ and intraspecific differences in both response range (Henzi and Barrett, 2005) and the

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general tenor or style of engagement (Thierry, 1985). A more flexible account of how female monkeys manage their lives together that can incorporate these differences is the ambitious task that now presents itself. VII. SUMMARY In mammals, social groups based on female philopatry (FB societies) are common only among New and Old World monkeys. They have, for this reason, featured prominently in attempts to understand the mechanisms by which individual group members manage local resource competition without threatening group cohesion. It has been argued that this balancing act is achieved through the use of grooming to develop, sustain, and repair long‐term relationships that might prove to be valuable in the future as the basis of coalitions. This proposition, in turn, has been used to explain the evolution of large primate brains because of the cognitive demands that would be necessary to track the affiliation patterns of other group members in relation to one’s own and to plan for uncertain futures. We argue, on the one hand, that there is little evidence for either the cognitive skills or the ‘‘relationships’’ that this account requires and, on the other, that there is too little evidence to link grooming, reconciliation, and coalition formation in this way. The evidence suggests to us that patterns of grooming and reconciliation reflect responses to immediate problems and have short‐term benefits, while the general rarity of coalition formation, which may be due to a corresponding rarity of circumstances in which short‐term benefits could accrue to all participants, undercuts any role it might have as an organizing principle for evolutionary theories of female action. We conclude that there is a good deal of empirical hay to be made by incorporating observed patterns of grooming, reconciliation, and coalition formation into a larger account of the negotiation of coexistence by female monkeys. In such an account, the absence of an apparently strategic behavior will carry an analytical weight at least equal to its presence, and the central objective will be to understand how actors generate appropriate, contingent responses to immediate social problems.

Acknowledgments We would like to thank Professor Tim Roper for this opportunity to develop our ideas and Dr. Drew Rendall for his constructive and very valuable criticisms of the chapter. The NRF of South Africa has funded our long‐term empirical research.

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Coexistence in FemaleBonded Primate Groups

1994), interest in the social dynamics of femalebonded (FB) primates. 43 ... tive of most primate societies, FB groups are certainly much more common within the OldWorld .... females supported each other on only 10% of occasions (dropping to ...... represents a network of bonds whose functional value requires high tempo-.

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