Complex patterns of grooming and sexual activity in Barbary macaques (Macaca sylvanus)

Grooming in primates is often considered a “currency” that can be exchanged for other “services” or “commodities” such as reciprocal grooming, coalitionary support, infant handling, tolerance around food sources, active food sharing, or mating opportunities. Previous studies on primate grooming‐for‐sex exchange viewed the males as the demanding class, with the females as suppliers of mating opportunities. In this study, we examine the broader context of grooming‐for‐mating exchange in Barbary macaques in Gibraltar. Our data show that Barbary macaque males groom females with whom they are mating more frequently and for longer periods than other females, and the relationship between grooming and mating remains significant in both sexual and nonsexual contexts. In addition, females groomed males with whom they were mating more frequently and for longer periods than other males. In both sexes, grooming was observed to be far more frequent and to occur for longer durations in sexual compared to nonsexual contexts. We did not find any difference in grooming behavior between presexual and postsexual contexts. Our data suggest that there is no simple model to describe Barbary macaque grooming patterns in sexual contexts. Although our results are partly consistent with male use of grooming as payment for mating, broadly assessed grooming‐mating patterns cannot be solely explained by a male‐driven grooming‐for‐mating exchange.     

No Short‐Term Contingency Between Grooming and Food Tolerance in Barbary Macaques (Macaca sylvanus)

The exchange of services such as allo‐grooming, allo‐preening, food tolerance and agonistic support has been observed in a range of species. Two proximate mechanisms have been proposed to explain the exchanges of services in animals. First, an animal can give a service to a partner depending on how the partner behaved towards it in the recent past. This mechanism is usually tested by examining the within‐dyad temporal relation between events given and received over short time periods. Second, the partner choice mechanism assumes that animals give favours towards specific partners but not others, by comparing how each partner behaved towards them over longer time frames. As such, the partner choice mechanism does not make specific predictions on a temporal contingency between services received and given over short time frames. While there is evidence for a long‐term positive correlation between services exchanged in animals, results for short‐term contingencies between services given and received are mixed. Our study investigated the exchange of grooming for food tolerance in a partially provisioned group of Barbary macaques, by analysing the short‐term contingency between these events. Tolerance over food was compared immediately after grooming and in control condition, using food of different shareability. We found no evidence that grooming increases food tolerance or decrease aggression around food in the short term. Food tolerance was affected by the shareability of the food and the sex of the partners. The exchanges of grooming and food tolerance in non‐human primates may be little affected by recent single events. We suggest that long‐term exchanges between services given and received and social partner choice may play a more important role in explaining social interactions than short‐term contingent events.     

Differences in Activity Budgets and Diet Between Semiprovisioned and Wild‐Feeding Groups of the Endangered Barbary Macaque (Macaca sylvanus) in the Central High Atlas Mountains,Morocco

The Barbary macaque, Macaca sylvanus is a very adaptable primate species occupying a wide range of habitats in Morocco and Algeria. Several groups of this endangered macaque can be found in tourist sites, where they are affected by the presence of visitors providing food to them. We compare the activity budgets and the diet of semiprovisioned and wild‐feeding groups of Barbary macaques in the central High Atlas Mountains of Morocco from February to August 2008. We used instantaneous scan sampling at 15‐min intervals. The behaviors included in the activity budget were feeding, moving, foraging, resting, and aggressive display. Food items were grouped into seven categories. We found no differences between the two groups in the daily percentages of records attributed to feeding. The semiprovisioned group spent significantly more time engaged in resting and aggressive behavior, and foraged and moved significantly less than the wild‐feeding group. There was no significant difference between the two groups in time spent eating leaves, fruits, or roots and bark. The semiprovisioned group, however, spent significantly less time per day feeding on herbs, seeds, and acorns than the wild‐feeding group. Human food accounted for 26% of the daily feeding records for the semiprovisioned group and 1% for the wild‐feeding group. Our findings agree with previous studies and indicate that in the tourist site, where food is highly clumped, macaques decreased foraging time yet showed higher levels of contest competition. Our results support the common claim that the diet of the Barbary macaque is highly flexible, differing among its varied habitats. Conservation efforts for the Barbary macaques should take into account the changes in behavior that human‐modified environments may cause.     

Dominance style of female white‐faced capuchins

Dominance style, the level of tolerance displayed by dominant individuals toward subordinate ones, is exhibited along a continuum from despotic to relaxed. It is a useful concept to describe the nature of dominance relationships in macaque species and it bridges among multiple features of dominance hierarchies, aggression, kinship and conflict resolution. Capuchins share many behavioral similarities with Old World monkeys and like macaques, may exhibit a suite of covarying characteristics related to dominance. Here, we provide an assessment of dominance style by examining measures of aggression and kin bias in 22 adult female white‐faced capuchin monkeys (Cebus capucinus) in three social groups at Santa Rosa Sector, Costa Rica. We found that bidirectionality of aggression was low (mean = 6.9% ± SE 1.6). However, there were few significant correlations between kin relatedness and social behavior (approaching, grooming, proximity, and co‐feeding), even though the intensity of kin bias in grooming was moderate and higher in the larger group. We conclude that patterns of aggression and kin‐biased behavior in our study animals are dissimilar to the patterns of covariation observed in macaque species. While unidirectional aggression suggests a despotic dominance style, the moderate expression of kin bias suggests an intermediate to relaxed classification when compared with results from an analysis of 19 macaque species. Additional studies of capuchin species and behaviors associated with dominance style (i.e., conciliatory tendencies) would help to create a comparative framework for the genus Cebus, and allow for more detailed cross‐species comparison of dominance relationships across all primates. Am J Phys Anthropol 150:591–601, 2013. © 2013 Wiley Periodicals, Inc.     

Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support

Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.     

Alpha male chimpanzee grooming patterns: implications for dominance “style”

In social primates, individuals use various tactics to compete for dominance rank. Grooming, displays and contact aggression are common components of a male chimpanzee's dominance repertoire. The optimal combination of these behaviors is likely to differ among males with individuals exhibiting a dominance “style” that reflects their tendency to use cooperative and/or agonistic dominance tactics. Here, we examine the grooming behavior of three alpha male chimpanzees at Gombe National Park, Tanzania. We found that (1) these males differed significantly in their tendency to groom with other males; (2) each male's grooming patterns remained consistent before, during and after his tenure as alpha, and (3) the three males tended to groom with high‐ middle‐ and low‐ranking partners equally. We suggest that body mass may be one possible determinant of differences in grooming behavior. The largest male exhibited the lowest overall grooming rates, whereas the smallest male spent the most time grooming others. This is probably because large males are more effective at physically intimidating subordinates. To achieve alpha status, a small male may need to compensate for reduced size by investing more time and energy in grooming, thereby ensuring coalitionary support from others. Rates of contact aggression and charging displays conformed to this prediction, suggesting that each male exhibited a different dominance “style.” Am. J. Primatol. 71:136–144, 2009. © 2008 Wiley‐Liss, Inc.     

Trade‐offs in primate grooming reciprocation: testing behavioural flexibility and correlated evolution

Primates may trade altruistic behaviours, such as grooming, either for itself or for different rank‐related benefits, such as tolerance or agonistic support. Ecological conditions are expected to affect competition and thus the steepness of dominance hierarchies. This, in turn, may influence the value of the different currencies that primates exchange. Thus, it can be hypothesized that, as the dominance hierarchy becomes steeper, more grooming is directed up the hierarchy (in exchange for tolerance or agonistic support) and less grooming is exchanged for other grooming. We assembled a large database of within‐group grooming distribution in primates (38 social groups belonging to 16 species and eight genera) and tested these hypotheses both within species (i.e. comparing different groups of the same species) and between species (using comparative methods that control for phylogenetic relatedness). We found within‐species evidence that steeper dominance hierarchies were associated with more grooming being directed up the hierarchy, and that a trade‐off occurred between the tendency to groom up the hierarchy and the degree of grooming reciprocation (although, in some analyses, only a nonsignificant trend was observed). By contrast, phylogenetically controlled comparisons between species did not reveal evidence of correlated evolution between the steepness of the dominance hierarchy, the tendency to direct grooming up the hierarchy, and the degree of grooming reciprocation. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 439–446.     

Whom to Groom and for What? Patterns of Grooming in Female Barbary Macaques (Macaca sylvanus)

Grooming is one of the most conspicuous social interactions among nonhuman primates. The selection of grooming partners can provide important clues about factors relevant for the distribution of grooming within a social group. We analyzed grooming behavior among 17 semi-free ranging female Barbary macaques (Macaca sylvanus). We tested whether grooming is related to kinship, rank and friendship. Furthermore, we tested whether grooming is reciprocated or exchanged for rank related benefits (i.e. lower aggression and increased tolerance whilst feeding). We found that in general grooming was reciprocally exchanged, directed up the hierarchy and at the same time affected by friendship and kinship. Grooming was more frequent among individuals with higher friendship values as well as amongst related individuals. We also divided our data set on the basis of rank difference and tested if different power asymmetries between individuals affected the tendency to exchange grooming for rank related benefits and grooming reciprocation. In support of our initial hypothesis our results show that the reciprocation of grooming was a significant predictor of grooming interactions between individuals of similar rank, but not between those individuals more distantly separated in the social hierarchy. However, we did not find any evidence for grooming being exchanged for rank related benefits in either data set. Our results, together with previously published studies, illustrate the behavioral flexibility of macaques. It is clear that multiple studies of the same species are necessary to gather the data required for the solid comparative studies needed to shed light on patterns of grooming behavior in primates.     

Using biological markets principles to examine patterns of grooming exchange in Macaca thibetana

Biological markets principles offer testable hypotheses to explain variation in grooming exchange patterns among nonhuman primates. They predict that when within-group contest competition (WGC) is high and dominance hierarchies steep, grooming interchange with other "commodity" behaviors (such as agonistic support) should prevail. In contrast, when WGC is low and gradients shallow, market theory predicts that grooming reciprocity should prevail. We tested these predictions in a wild, provisioned Tibetan macaque (Macaca thibetana) group across six time periods during which the group had been subjected to varying degrees of range restriction. Data on female-female aggression, grooming, and support were collected using all-occurrences and focal animal sampling techniques, and analyzed using ANCOVA methods and correlation analyses. We found that hierarchical steepness varied significantly across periods, but did not correlate with two indirect indicators of WGC (group size and range restriction) in predicted directions. Contrary to expectations, we found a negative correlation between steepness and group size, perhaps because the responses of group members to external risks (i.e. prolonged and unavoidable exposure to humans) may have overshadowed the effects of WGC. As predicted, grooming reciprocity was significant in each period and negatively correlated with steepness, even after we controlled group size, kinship, rank differences, and proximity. In contrast, there was no evidence for grooming interchange with agonistic support or for a positive relationship between interchange and steepness. We hypothesize that stressful conditions and/or the presence of stable hierarchies during each period may have led to a greater market demand for grooming than support. We suggest that future studies testing these predictions consider more direct measures of WGC and commodities in addition to support, such as feeding tolerance and access to infants.     

Grooming,rank, and agonistic support in tufted capuchin monkeys

Studies investigating the relation between allogrooming and social rank in capuchin monkeys (genus Cebus) have yielded inconsistent results. In this study, we investigated the relation between grooming, agonistic support, aggression and social rank in a captive group of tufted capuchin monkeys (C. apella). Differently from most previous studies, we based our analyses on a relatively large database and studied a group with known genealogical relationships. Tufted capuchin females did not exchange grooming for rank‐related benefits such as agonistic support or reduced aggression. Coherently with this picture, they did not groom up the hierarchy and did not compete for accessing high‐ranking grooming partners. It is suggested that a small group size, coupled with a strong kin bias, may make the exchange of grooming for rank‐related benefits impossible or unprofitable, thus eliminating the advantages of grooming up the hierarchy. We provide several possible explanations for the heterogeneity of results across capuchin studies that have addressed similar questions. Am. J. Primatol. 71:101–105, 2009. © 2008 Wiley‐Liss, Inc.     

Post‐conflict third‐party affiliation in chimpanzees: what's in it for the third party?

Affiliative behavior after conflicts between conflict participants and other group members is common in many primate species. The proposed functions for such triadic interactions are numerous, mostly concerning the benefit for the former conflict opponents. We investigated post‐conflict third‐party affiliation (TPA) in captive chimpanzees (Pan troglodytes) with the aim of assessing what the affiliating third parties may gain from affiliation. Specifically, we tested whether third‐party‐initiated affiliation protects the third parties from further aggression by conflict opponents. We found support for this “self‐protection hypothesis,” in that third parties selectively directed affiliation to those opponents who more often gave further aggression to them, and affiliation effectively decreased their chance of receiving aggression from these opponents. However, a subset of affiliation, provided to conflict victims by their own kin, appeared to not be self‐protective and the function of it remained open. We conclude that chimpanzee third‐party‐initiated affiliation is a more heterogeneous behavior than thus far assumed. Am. J. Primatol. 71:409–418, 2009. © 2009 Wiley‐Liss, Inc.     

Inter-individual relationships in proboscis monkeys: a preliminary comparison with other non-human primates

This is the first report on inter-individual relationships within a one-male group of proboscis monkeys (Nasalis larvatus) based on detailed identification of individuals. From May 2005 to 2006, focal and ad libitum data of agonistic and grooming behaviour were collected in a forest along the Menanggul River, Sabah, Malaysia. During the study period, we collected over 1,968 h of focal data on the adult male and 1,539 h of focal data on the six females. Their social interactions, including agonistic and grooming behaviour, appeared to follow typical patterns reported for other colobines: the incidence of social interaction within groups is low. Of 39 agonistic events, 26 were displacement from sleeping places along the river, 6 were the α male threatening other monkeys to mediate quarrels between females and between females and juveniles, and 7 were displacement from feeding places. Although the agonistic behaviour matrix based on the 33 intra-group agonistic events (excluding events between adults and juveniles and between adults and infants) was indicative of non-significant linearity, there were some specific dominated individuals within the group of proboscis monkeys. Nonetheless, grooming behaviour among adult females within a group were not affected by the dominance hierarchy. This study also conducted initial comparisons of grooming patterns among proboscis monkeys and other primate species. On the basis of comparison of their grooming networks, similar grooming patterns among both-sex-disperse and male-philopatric/female-disperse species were detected. Because adult females in these species migrate to groups repeatedly, it may be difficult to establish the firm grooming exchange relationship for particular individuals within groups, unlike in female-philopatric/male-disperse species. However, grooming distribution patterns within groups among primate species were difficult to explain solely on the basis of their dispersal patterns. Newly immigrated females in some species including proboscis monkeys are eager to have social interactions with senior group members to improve their social position.     

Grooming and agonistic support: a meta-analysis of primate reciprocal altruism

Grooming and agonistic support are 2 common primate behaviorsthat have been hypothesized to constitute examples of reciprocalaltruism. In particular, because primates often direct theirgrooming up the dominance hierarchy, it has been suggested thatthey may exchange grooming for agonistic support. Empiricaltests of this hypothesis have resulted in highly inconsistentfindings. I synthesized the published literature on the relationbetween grooming and agonistic support in primates using modernmeta-analytical techniques. A meta-analysis of 36 studies carriedout on 14 different species showed that a significant positiverelation exists between grooming and agonistic support (weightedaverage r = 0.154, corrected for publication bias). These findingssuggest that grooming and agonistic support may have evolvedas part of a system of low-cost reciprocal altruism. They alsohighlight the potential of meta-analysis in tackling the studyof behavioral phenomena characterized by low overall frequencyand small effect sizes.     

A dynamic interaction between aggression and grooming reciprocity among female chacma baboons

We used data from a natural experiment on adult female chacma baboons, Papio cynocephalus ursinus, to test the hypothesis that variation in aggression through time influences patterns of grooming reciprocity within a social group. Owing to a change in the baboons' competitive regime, we were able to compare data from periods when aggression was high (period 1) and low (period 2). During period 2, the slope of the relationship between aggression and rank was significantly shallower than during period 1 and less aggression was directed at the lowest-ranking females suggesting there had been a reduction in the dominance gradient. We attributed this to reduced effectiveness of dominance as a means of excluding other females from feeding resources. The reduction in aggression during period 2 was accompanied by an increase in grooming reciprocity between dyads suggesting that high-ranking females no longer attracted grooming by subordinates in exchange for tolerance, and that grooming in period 2 was exchanged for its intrinsic benefits. The loss of rank-related effects on grooming reciprocity in period 2 compared with period 1 further confirmed this. These findings show that female baboons are able to respond flexibly and swiftly to changes in their social circumstances and that a dynamic approach to primate social interactions is worth pursuing. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Interchange of Grooming and Agonistic Support in Chimpanzees

We investigated the temporal relationship between grooming given and agonistic support received in a group of chimpanzees at Chester Zoo, U.K. We compared grooming levels the day before a conflict-with-support to those the day before a conflict-without-support and to baseline to investigate whether individuals groom potential supporters in anticipation of the need for support. We also compared grooming and aggression levels the day after conflicts-with-support to levels the day after conflicts-without-support and to baseline levels to determine whether chimpanzees reward individuals that support them or punish those that do not. Finally, we compared grooming and aggression levels the day after conflicts-with-unsuccessful-solicitations-for-support to those the day after conflicts-with-support and to baseline to examine the behavioral consequences of not providing support when an individual had solicited but did not receive it. Future recipients of support groomed future supporters more the day before receiving support, compared to the day before conflicts-without-support, indicating that grooming increased the likelihood of support. The relationship between prior grooming and support held true only for aggressor and not victim support and is consistent with behavior expected if chimpanzees anticipated the need for agonistic support and groomed their supporter the day before to increase the likelihood of support. We found evidence of a system of reward and punishment. Individuals experienced significantly lower rates of aggression after conflicts in which they provided support than at baseline and after conflicts in which they did not provide support. The finding was true only for aggressor support. We found no evidence that chimpanzees punished individuals whom or that they unsuccessfully solicited with aggression or a reduction in grooming. However, solicitors groomed individuals that they solicited for support significantly more after unsuccessful solicitations than after individuals provided support (but with no difference from baseline), indicating that individuals may attempt to recement their relationship after an unsuccessful solicitation. The findings are consistent with a mechanism of calculated interchange in chimpanzees.     

Human–wildlife conflict: Proximate predictors of aggression between humans and rhesus macaques in India

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co‐inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3‐month study of four free‐ranging populations of rhesus macaques in Dehradun, India from October–December 2012, using event sampling to record all instances of human‐macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one another's behavior. Mitigation of human‐primate conflict, and indeed other types of human‐wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other. Am J Phys Anthropol 156:286–294, 2015. © 2014 Wiley Periodicals, Inc.     

Evaluating Dominance Styles in Assamese and Rhesus Macaques

Researchers have suggested that several types of agonistic and affiliative behavior covary as a set of species-specific traits, and have used the term dominance style to describe the covariation. We compared measures of dominance style between a group of Assamese macaques (Macaca assamensis) and a group of rhesus macaques (M. mulatta), though kinship information was unknown. Assamese and rhesus female-female dyads each showed a low proportion of counter aggression and a low conciliatory tendency, suggesting that they have despotic social relationships. They also showed a despotic pattern on several other types of agonistic and affiliative behavior, such as approach outcomes and grooming distributions, which is consistent with the covariation of dominance style traits. Assamese male-male dyads showed relatively high levels of reconciliation and counter aggression versus other macaque males portrayed in the literature, suggesting that Assamese males have a tolerant dominance style. Insofar as macaque dominance style depends on the behavior of females, we suggest that Assamese macaques, like rhesus macaques, have despotic social relationships, which contrasts with evidence of a strong correlation between phylogeny and dominance style in macaques. Further, our results indicate that strong male bonding and tolerant dominance relationships among males are independent of female dominance style. Lastly, some measures of agonistic behavior, such as rate of aggression or proportion of bites, are likely altered in competitive environments and thus are not useful indicators of dominance style.     

Grooming and aggression in captive Japanese macaques

This study investigated the relations between allogrooming and aggression in a captive group of Japanese macaques (Macaca fuscata). Our aim was to test whether evidence of an interchange between allogrooming and a reduction in aggression could be identified at a group level. Female Japanese macaques did not direct less aggression to those group mates that groomed them most. Although generally they did not direct more grooming to those group mates that attacked them most, they did show increased grooming towards those nonkin group mates that showed the most aggression. These results are interpreted in light of the conflicting processes that are likely to underlie macaque social choices.     

Immediate and Delayed Benefits of Play Behaviour: New Evidence from Chimpanzees (Pan troglodytes)

Evidence for the anticipation of competition at feeding time has been previously documented in both Pan species. Chimpanzees seem to cope with competitive tendency through behavioural mechanisms of tension reduction, and grooming is certainly one of these. Social play and grooming are often matched because they bring animals into close physical contact for long periods, and they have an important role in social cohesion. Our goal was to investigate the occurrence of play behaviour during the pre‐feeding period, before a basic maintenance activity is about to take place, in the chimpanzee colony housed in the ZooParc de Beauval (St Aignan sur Cher, France). The group was composed of 10 adults and nine immature individuals. By scan animal sampling (344 h of observation), we recorded play and grooming interactions in all age‐class combinations during four different periods (pre‐feeding, feeding, post‐feeding, control). We found peak levels of grooming interactions among adults during the pre‐feeding time. A peak frequency at the pre‐feeding time was also found in social play between adults and unrelated immature subjects. This finding suggests that during high tension periods, grooming and play might share similar functions in conflict management. Like grooming, play might have an important role to limit aggression and increase tolerance around food (immediate benefits). Immature animals showed a higher frequency of play in the pre‐feeding than in any other condition (feeding, post‐feeding, and control). During high excitement periods social play probably represents a safe mechanism for immature subjects to test their personal abilities (self‐assessment), the strength/weakness of playmates, and the degree of cooperation/competition with them (social‐assessment). In the light of this new evidence, we can assert that play behaviour is far from being a purposeless activity, at least in the chimpanzee colony under study.