White-faced capuchin monkeys show triadic awareness in their choice of allies

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1 ANIMAL BEHAVIOUR, 2004, 67, 165e170 doi: /j.anbehav White-faced capuchin monkeys show triadic awareness in their choice of allies SUSAN PERRY*, H. CLARK BARRETT & JOSEPH H. MANSON* *Max Planck Institute for Evolutionary Anthropology, Leipzig ydepartment of Anthropology, University of California, Los Angeles zcenter for Behavior, Evolution and Culture, University of California, Los Angeles (Received 1 November 2002; initial acceptance 6 January 2003; final acceptance 27 April 2003; MS. number: 7517) The social intelligence hypothesis, which holds that social challenges have selected for increased intelligence and social skills, has been supported by evidence that, in catarrhine primates, individuals know about the characteristics of groupmates social relationships. Evidence for such triadic awareness has not been sought for platyrrhine primates, although two platyrrhine genera, capuchins, Cebus, and squirrel monkeys, Saimiri, are among the most highly encephalized primates. We examined patterns of coalitionary recruitment in wild white-faced capuchins, C. capucinus. Analyses have shown that more dominant individuals are more likely to join aggressive coalitions than low-rankers, and that individuals preferentially support those with whom they have stronger affiliative relationships. Data from 110 fights, analysed using simulation techniques that produced distributions of results expected under null hypotheses, revealed that contestants preferentially solicited prospective coalition partners that (1) were dominant to their opponents, and (2) had better social relationships (higher ratios of affiliative/ cooperative interactions to agonistic interactions) with themselves than with their opponents. Further analyses showed that soliciting dominant partners could be explained by either of two simpler rules, Solicit an ally that outranks yourself or Solicit the highest-ranking available individual. However, soliciting partners with better social relationships appears to indicate triadic awareness, because subjects did not preferentially solicit the nearby individual with whom they shared the highest-quality social relationship. Effects of relative relationship quality on coalition solicitation decisions were independent of effects of dominance rank. Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. According to the social intelligence hypothesis (Jolly 1966; Humphrey 1976; Byrne & Whiten 1988; Cheney & Seyfarth 1990), the challenges of navigating a complex political landscape have been a major selective force in the shaping of the primate mind. Primates living in complex social groups need to understand the nature of the social relationships between other group members, so that they can use such information to their advantage when selecting social partners for particular purposes. Since the social intelligence hypothesis was originally proposed, a database has slowly accumulated supporting the idea that Old World monkeys and apes understand the nature of other individuals social relationships (reviewed in Correspondence: S. Perry, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig, Germany ( perry@eva.mpg.de). H. C. Barrett is at the Department of Anthropology, UCLA, 405 Hilgard Avenue, Los Angeles, CA , U.S.A. 0003e3472/03/$30.00/0 Tomasello & Call 1997). However, New World primates have been largely overlooked in this endeavour. Because capuchin monkeys, Cebus, along with squirrel monkeys, Saimiri, have the largest encephalization quotients of any nonhuman primate (Stephan et al. 1988), they represent a particularly valuable source of data in the quest to understand the selective factors affecting the evolution of intelligence. Experimental studies of Old World monkeys provide the most convincing source of evidence of triadic awareness (i.e. animal A understands some aspect of the quality of relationship between animals B and C) in primates. For example, Dasser (1988a, b) showed that juvenile longtailed macaques, Macaca fascicularis, understand the kinship structure of their groups, successfully matching mothereoffspring and sibling pairs in a picture-sorting task. Cheney & Seyfarth (1990) performed playback experiments on vervet monkeys, Chlorocebus aethiops, in 165 Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

2 166 ANIMAL BEHAVIOUR, 67, 1 which females indicated knowledge of mothereoffspring relationships by looking towards the mother of a juvenile whose scream had just been played to them. Another set of experiments on baboons, Papio cynocephalus ursinus (Cheney et al. 1995), indicated that females understand one another s rank relationships, because they responded with more interest to a playback of a dominant expressing submission to a subordinate than vice versa. Pairs of unrelated female baboons also reacted differently to simulated conflicts as a function of the apparent contestants kin relationship to themselves, in a manner suggesting triadic awareness of kinship (Cheney & Seyfarth 1999). Bachmann & Kummer s (1980) experiments with hamadryas baboons, Papio cynocephalus hamadryas, indicate that adult males assess the quality of the relationships of maleefemale pairs and use that information when deciding whether to challenge the male for possession of the female. In addition to the experimental evidence, there is much evidence from observational studies suggesting that monkeys and apes show triadic awareness (e.g. Cheney & Seyfarth 1990; Tomasello & Call 1997). For example, the patterning of reconciliation and redirected aggression in vervets (Cheney & Seyfarth 1989), stumptailed macaques, M. arctoides (Call et al. 2002), and pigtailed macaques, M. nemestrina (Judge 1991), suggests that these monkeys understand kinship relationships. Observed patterns of coalition formation (e.g. Silk 1992; Perry 2003) also suggest a sophisticated understanding of rank, kinship and affiliative relationships. However, observational studies are usually limited in their capacity to rule out alternative cognitive interpretations. Silk (1999) showed that male bonnet macaques, M. radiata, understand others rank relationships, by demonstrating via simulation techniques that they solicit males ranking higher than their opponents more often than is expected by chance, ruling out the possibility that they use a simpler rule of thumb (e.g. Solicit a male that outranks yourself or Always solicit the most dominant individual ). We extended this general approach to wild white-faced capuchin monkeys, Cebus capucinus, to test whether they understand the rank relationships and relationship quality of other group members and use this knowledge in their solicitation of allies. Research on the coalitionary aggression of white-faced capuchins (Perry 1996, 1997, 1998a, b, 2003) has revealed the following three basic rules regarding their decisions of which opponent to support in an ongoing fight: (1) support females versus males (85% of 95 fights); (2) support the dominant opponent (57% of 202 fights; this rule is in conflict with rule 1, because females are subordinate to males, but in fights between same-sexed opponents, dominant females were supported 98% of the time (N ¼ 40 fights) and dominant males at least 89% of the time; N ¼ 36 fights in which rank was definitely known); (3) support the monkey with whom the decisionmaker has the better relationship, as measured by the proportion of interactions that were affiliative (85% of 170 fights). Given that high-rankers are far more likely than low-rankers to choose to become involved in fights (Perry 1996, 1997), and are probably more effective allies, we predicted that individuals involved in ongoing dyadic disputes would be more likely to solicit support from others that are dominant to their opponent. Given the tendency of white-faced capuchins to support the opponent with whom they have the stronger affiliative relationship, we also predicted that individuals involved in ongoing fights would preferentially solicit support from others that have a stronger affiliative relationship with themselves than with their opponent. Subjects METHODS Data were collected as part of an observational study of capuchin social relationships at Lomas Barbudal Biological Reserve and surrounding private and public lands in Guanacaste, Costa Rica (Perry 1995, 1996, 1997, 1998a, b). The data used in this study are from a single study group, Abby s group, obtained from May 1991 to May The group consisted of 21 individuals: four adult males (one of whom immigrated in November 1992 at the time of a rank reversal involving the alpha male; Perry 1998a), six adult females and 11 immatures. Adults and large juveniles were recognizable by natural differences in features such as scars, colouring and facial shape. Small juveniles were marked with Clairol Born Blonde hair dye, squirted at their backs from 1e2 m with a 100-cc syringe from which we had removed the needle. This procedure never produced noticeable distress in the subjects. The study was approved by the University of Michigan Committee on Use and Care of Animals. Marking was approved by the Servicio de Parques Naciónales de Costa Rica and the regional division (Area de Conservacion Tempisque). Procedure Data were collected in the form of 10-min focal follows, during which continuous data were recorded on all social behaviours (Perry 1995, 1996, 1997, 1998b). The fights used in this study were drawn from a sample of 1405 h of focal data. Every 2.5 min, we conducted a scan sample in which we recorded the identities of all individuals in view of the focal animal as well as their precise proximities to the focal animal. These scan data were used to determine the relevant audience (i.e. pool of potential recruitees) for each fight. Any monkey within view of the focal animal was considered to be a potential recruitee. The precise distance depended upon visibility, but the radius of animals considered to be recruitable was about 10e20 m. Two observers participated in data collection; one watched the focal individual, narrating the action into a microcassette recorder, while the other called out the identities of other individuals who were approaching or directing vocalizations and gestures towards the focal animal or its opponents. Whenever the two observers disagreed on the identities of participants or their activities, these fights were dropped from the sample.

3 PERRY ET AL.: TRIADIC AWARENESS IN CAPUCHINS 167 Data Analysis Two criteria had to be met for the fights to be included in the sample for analysis. First, the fight had to be serious enough to warrant an agonistic response from the target of the initial aggressive act. We used this criterion because white-faced capuchins sometimes form coalitions against distant individuals that are not attending to them (and may even be sleeping), possibly as a form of communication between the coalition partners, and such interactions are not triadic because they do not necessarily depend on the victim s characteristics. Second, the recruitment signals used had to be obviously directed at a particular individual, such as the headflag gesture (head is jerked quickly towards the solicitee and then back towards the opponent), embrace, cheek-to-cheek posture (two monkeys stand side-by-side with their cheeks touching while jointly threatening a common opponent) and overlord posture (monkeys align themselves on top of one another, with heads stacked like a totem pole and hands clasping the partner s chest, and jointly threaten the common opponent). Ranks were determined by examining submissive responses (avoidance and cowering) within dyadic interactions (i.e. situations in which potential allies were not close at hand to bias the results; see also Perry 1996, 1998b). Females formed a clear linear hierarchy, in which all females were subordinate to all males. There were six dyads for which we were unable unequivocally to determine rank: one of these was a pair of subordinate adult males, and the others were pairs of juveniles who had not yet attained their adult ranks. For the purpose of analysis, we assigned tied ranks to the members of these dyads. There was one rank reversal involving a pair of males during the study. For these males, we used the rank that was current for the time of each fight included in the analysis. The index of relationship quality was calculated in the following way. For each of the 210 dyads, we extracted their entire history of interactions. For each 10-min focal follow, any interactions for the dyad were coded as being neutral, affiliative (e.g. grooming, resting in contact) and/ or cooperative (e.g. supporting one another in fights), or agonistic (aggressive or submissive). Then we divided the number of samples including affiliative/cooperative behaviours by the sum of the numbers of samples with affiliative/cooperative interactions and samples with agonistic behaviours. This measure has several advantages over more traditionally used relationship quality measures, such as grooming rates, aggression rates or time spent in proximity, because it incorporates many aspects of the relationship into a single measure. Because the study group s adult males social relationships changed dramatically following a male rank reversal (Perry 1998a), we calculated separate relationship quality indices before and after rank reversal for every dyad in the study group, and used for analyses whichever index was current at the time of the fight. Statistical results were obtained by conducting Monte Carlo simulations (H. C. Barrett, unpublished software program in Visual Basic) that used data on observed audience composition for each fight to determine the distribution of decision outcomes under the null model that our subjects solicited coalition partners at random. In these simulations, the program randomly selected a monkey from the audience (or from some designated subset of the audience) for each fight in the database. Each simulation was run times to produce an expected distribution of proportions of correct decisions according to the criterion in question, that is, decisions in which a particular hypothesized decision rule was followed, if the subjects were soliciting prospective coalition partners at random. To determine statistical significance for each prediction, we then noted where, within each simulationgenerated distribution, the observed proportion of correct decisions fell. RESULTS In describing the results, we use the following codes: D is the decision-maker (the individual deciding whom to recruit), O is the decision-maker s opponent, and S is the potential ally whose support is solicited by the decisionmaker. Characteristics of the Sample One hundred and ten conflicts met the criteria described above for inclusion in the sample (XGSD audience size ¼ 3:42G1:83; mean proportion of audience members that outranked O ¼ 0:52G0:35; mean proportion of audience members that had a higher relationship quality index with D than with O ¼ 0:59G0:38; mean proportion of audience members that both outranked O and had a higher relationship quality index with D than with O ¼ 0:30G0:33). Triadic Awareness of Rank Relationships Decision-makers preferentially solicited support from Ss that outranked O (71.8% of cases). The observed proportion of correct decisions fell above the highest proportion generated by the simulation in runs (P!0:00005; Fig. 1a). However, Ds showed an even stronger preference for soliciting Ss that outranked themselves (78.2% of cases, P!0:00005). This result raised the possibility that subjects were following a cognitively simpler rule ( Solicit a prospective ally that outranks yourself ) rather than a cognitive rule requiring triadic awareness. To resolve this ambiguity, we replicated an analysis carried out by Silk (1999) that compared observed decisions to those predicted by a null model in which D chooses randomly only from a pool of potential allies that are dominant to D. In other words, we generated a null model of outcomes that would be obtained if D followed the simple rule, Solicit a prospective ally that outranks yourself, to see whether this rule alone would have generated our observed distribution of fight outcomes by chance. For each fight in which O outranked D (N ¼ 48), the simulation selected an audience member at random. If this audience member did not outrank D, the simulation

4 168 ANIMAL BEHAVIOUR, 67, 1 Proportion of simulations (a) (b) (c) Relationship quality index (%) Figure 1. Monte Carlo simulations of decision-makers (D) choices of whom to solicit (S) against an opponent (O). In all simulations, an ally was chosen at random from the audience members for each of 110 observed fights, and a correct decision was scored when the chosen ally met the specified criterion. The program repeated this procedure times to generate a distribution of proportions of correct decisions expected if D were choosing S at random from the audience members. Observed percentages of correct decisions are indicated by arrows. (a) A correct decision was scored when S was dominant to O. (b) A correct decision was scored when S had a higher relationship quality index with D than with O. (c) For fights in which the observed S outranked O (N ¼ 79), a correct decision was scored when S had a higher relationship quality index with D than with O. chose another audience member at random. Upon selecting an audience member that did outrank D, the simulation scored a correct decision if this audience member outranked both D and O; otherwise it scored an incorrect decision. The observed percentage of correct decisions (58.3% of the cases in which O outranked D) was not significantly greater than expected by chance (P ¼ 0:19), suggesting that the simple rule Solicit a prospective ally that outranks yourself alone could have generated our observed proportion of cases in which S outranked both D and O. We also considered whether our subjects were simply soliciting support from the highest-ranking audience member, perhaps distinguishing this individual using a cue such as piloerection or posture rather than triadic awareness of dominance relationships. First, we replicated Silk s (1999) analysis in which she examined whether there was a correlation between S s dominance rank and the rank of the higher-ranked of the two contestants D and O. Silk reasoned that if D consistently solicited the highest-ranked audience member, regardless of O s rank, then no correlation between these variables would be expected. On the other hand, if Ds solicited prospective allies based on whether they outranked Os, then Ds faced with lower-ranking Os would have a larger number of potential Ss to choose from compared with Ds faced with higher-ranking Os. Thus, on average, the Ss selected by Ds facing lower-ranking Os would rank lower than the Ss selected by Ds facing higher-ranking Os. Using each fight as a separate data point, we obtained a trend towards a positive correlation between S s dominance rank and that of the higher-ranked of the two contestants D and O (Spearman rank correlation r S : r S ¼ 0:17, N ¼ 110, P ¼ 0:07), but the result vanished when we used, as data points, the mean dominance rank of S across all cases in which the highest ranking of D and O held a particular ordinal rank (Spearman rank correlation: r S ¼ 0:40, N ¼ 14, P ¼ 0:16). Second, we ran a simulation that revealed that our subjects preferentially chose the highest-ranking audience member (65.5% of cases; P!0:00005). Triadic Awareness of Quality of Social Relationships Decision-makers preferentially solicited support from Ss that had higher relationship quality indices with themselves than with O (67.3% of cases; P ¼ 0:02; Fig. 1b). This result could have been produced by a decision rule that does not involve triadic awareness: Solicit the audience member with whom you have the highest relationship quality index. However, our simulation revealed that Ds did not follow this rule at a frequency greater than expected by chance (41.8% of cases; P ¼ 0:61). Effects of Rank and Relationship Quality Our subjects used both dominance rank and relative relationship quality as criteria for choosing whom to solicit. Among those audience members that had higher relationship quality indices with D than with O, Ds preferentially solicited the highest-ranking audience member (26.4% of cases; P ¼ 0:00005). However, dominance rank and relative relationship quality had independent effects on solicitation decisions. Considering only the 79 cases in which S outranked O, Ds preferentially solicited Ss that had higher relationship quality indices with themselves than with O (60.8% of 79 cases; P ¼ 0:035; Fig. 1c). Considering only the 74 cases in which S had a higher relationship quality index with D than with O, Ds preferentially solicited Ss that outranked O (64.9% of 74 cases; P!0:00005). Finally, we tested whether our subjects might have used the following rule, which does not require triadic awareness: from the audience members who rank higher than D, solicit the individual having the highest relationship quality index with D. The monkeys did not solicit

5 PERRY ET AL.: TRIADIC AWARENESS IN CAPUCHINS 169 help from such individuals at a rate higher than expected by chance (27.8% of 79 cases; P ¼ 0:30). DISCUSSION These results suggest that white-faced capuchin monkeys consider both relationship quality and dominance rank when deciding whom to recruit as allies in coalitionary aggression. However, although our subjects appeared to show triadic awareness by using relative criteria of relationship quality, they may use dominance rank only as an absolute criterion, preferring the highest-ranking available prospective ally regardless of their opponent s rank. Furthermore, these results should be interpreted with some caution because they are based on observations of a single social group. Dominance Rank and Solicitation Decisions Our analyses indicate that our subjects preferentially solicited high-ranking coalition partners. However, it is unclear whether they used a decision rule incorporating triadic awareness ( Solicit an ally that outranks your opponent ), a simpler decision rule using only their knowledge of their own dominance relationships ( Solicit an ally that outranks yourself ), or the rule Solicit the highest-ranking available conspecific. Solicited individuals outranked decision-makers opponents, but when opponents outranked decision-makers, solicited individuals were no more likely than expected by chance to outrank both decision-makers and their opponents. These results suggest that white-faced capuchins follow the simpler rule, Solicit an ally that outranks yourself, when choosing coalition partners. The highest-ranking audience member was solicited much more frequently than expected by chance. When we sought to clarify whether our subjects used the Solicit the highest-ranking available conspecific rule by calculating the correlation between the solicited individual s rank and the higher of the two contestants ranks, we obtained equivocal results. In summary, our results do not permit us to conclude whether white-faced capuchins have triadic awareness of dominance relationships. They may use a combination of decision rules concerning dominance rank when choosing coalition partners, and some of these rules may incorporate triadic awareness. It is also possible that using absolute dominance rank as a recruitment criterion is sufficient to generate efficacious recruitment decisions; perhaps the highest-ranking ally is almost always the most willing and effective ally, regardless of the relative ranks of decision-maker and opponent. In this case, testing whether our subjects followed the rule Solicit an ally that outranks your opponent would be an inappropriate assay of triadic awareness in this species. Relationship Quality and Solicitation Decisions Our results regarding the role of relationship quality in our subjects coalitionary solicitation decisions were more straightforward. Using an index of proportion of all interactions that were affiliative or cooperative, we found that white-faced capuchins preferentially solicited allies that had better relationships with themselves than with their opponents. This result was not attributable to Ds soliciting Ss that had the highest relationship quality index with themselves among audience members. Therefore, we infer that Ds compared their own relationship with the prospective ally to their opponent s relationship with that individual, and used this comparison when deciding whom to solicit. Thus, they showed triadic awareness of other group members social relationships. An alternative interpretation is that, rather than showing triadic awareness, the decision-makers were soliciting monkeys who had better relationships with themselves than with their opponents because of cues that are given by the audience members during or just before the fights. Individuals with better relationships with D may be more likely to signal their willingness to aid D than individuals with worse relationships with D. Perhaps decision-makers use these signals, rather than their knowledge of audience members social relationships, to decide whom to solicit. To address this hypothesis, we restricted analysis to cases in which S did not aid D. In these cases, it is unlikely that S signalled its intent to intervene in the conflict in support of D. Nevertheless, we found for this subsample, as in the entire sample of fights, that D was significantly more likely than expected by chance to solicit Ss that had higher relationship quality indices with D than with O (62.9% of 35 cases; P ¼ 0:034). It is important to distinguish between the effects of dominance rank and the effects of relationship quality on coalition solicitation decisions, because they could have been confounded. For example, low-ranking white-faced capuchins might have generally lower-quality social relationships with other group members than highrankers, or rank distance might influence the quality of social relationships. Our subjects followed both decision rules simultaneously (i.e. Solicit the highest-ranking potential ally from those that have a higher relationship quality index with you than with your opponent ) more frequently than expected by chance. However, by analysing subsamples of the observed fights, we found that dominance rank and relationship quality had independent effects on coalition solicitation decisions. When considering only those cases in which subjects solicited individuals that outranked their opponents, we found that they preferentially solicited individuals that had better relationships with themselves than with their opponents (but did not preferentially solicit the individual from that subset having the highest relationship quality index with themselves). Similarly, in the subsample of cases in which subjects preferentially solicited individuals that had better relationships with themselves than with their opponents, they preferentially solicited individuals that outranked their opponents. Conclusions These results, like those of Silk (1999), show that purely observational data, analysed using simulation techniques,

6 170 ANIMAL BEHAVIOUR, 67, 1 can shed light on triadic awareness in nonhuman animals, and that recruitment of coalition partners is a behavioural domain that can reveal the extent of monkeys knowledge about others social relationships. Furthermore, these results represent the first within-species test of any portion of the social intelligence hypothesis in a platyrrhine primate. Although comparative treatments of this hypothesis (Barton and Dunbar 1997) have begun to include New World monkey taxa as data points, the extent to which platyrrhines actually show sophisticated social cognition is still largely unexplored. Acknowledgments We thank J. Gros-Louis and L. Sirot for their invaluable assistance in data collection. S.P. thanks the following funding agencies: L.S.B. Leakey Foundation (two grants), National Science Foundation (graduate fellowship to S.P., and grants to B. Smuts and J. Mitani), National Geographic Society, Sigma Xi, Rackham Graduate School (Research Partnership grant with B. Smuts, predoctoral fellowship and dissertation grant), the Evolution and Human Behavior Program and the University of Michigan Alumnae Society. We thank the Costa Rican Servicio de Parques Naciónales and the ACT for permission to work in Lomas Barbudal Biological Reserve, and the community of San Ramón de Bagaces and Rancho Jojoba for permission to work on private lands near the reserve. L. Sirot, M. Tomaszycki, M. Landys and S. Newman assisted in data transcription and data entry into the computer. G. Frankie and J. Frankie, the Rosales family and M. Cedillos provided logistical assistance in the field. J. Silk, D. Stahl, J. Gros-Louis, R. Seyfarth, R. Kurzban and two anonymous referees provided helpful comments regarding data analysis or comments on the manuscript. 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