Social tension after grooming in wild Japanese macaques (Macaca fuscata yakui) is sex specific and sensitive to social relationships.

Changes in the rate of self-directed behavior-a proxy for social tension-offer valuable insights into individuals' experiences of social interactions. Many studies have tested the tension-reduction hypothesis, whereby grooming is expected to reduce social tension in the grooming partners. However, it is still unclear whether responses to grooming are affected by social factors such as an individual's role or social relationship with their partner, and whether responses are similar for females and males. Focussing on same-sex grooming in Yakushima Japanese macaques (Macaca fuscata yakui), we analyzed the effects of two social factors on the change in the rate of self-scratching after receiving grooming: sitting in contact with their partner outside of grooming contexts (as a measure of relationship strength) and rank distance. We collected 10-min postgrooming and matched-control focal samples on recipients of grooming. After controlling for postinhibitory rebound effects, grooming reduced scratching in females (suggesting that grooming was relaxing for the receiver), but not in males. In females, this reduction was associated with increased sitting in contact and increased rank distance: being groomed was more tension-reducing if the grooming partners spent time together outside of grooming contexts, or if their difference in rank was greater and therefore more conspicuous. The reduction effect was mediated by sitting in contact only when females had a higher-ranking-that is, more dominant and potentially aggressive-groomer. Our findings suggest that not all grooming interactions are perceived as equal, which has implications for its use as an index of relationship quality. To our knowledge, this represents the first study of postgrooming social tension in male Japanese macaques and our results highlight the need for caution when generalizing findings from only one sex to the species level.

Emotional states following grooming in female mandrills.

Grooming is a common cooperative behavior whose exact costs and benefits are still to be fully elucidated. In this study, we evaluated the emotional consequences of giving and receiving grooming in mandrills (Mandrillus sphinx), and how these may change along time after the termination of grooming. We used scratching as a behavioral indicator of anxiety-like emotions. Groomees showed increased scratching immediately after the termination of grooming, while in the subsequent minutes scratching decreased below baseline. The initial increase was larger after longer grooming events, suggesting it represented a case of postinhibitory rebound. The subsequent decline in scratching rates was larger after grooming received by a kin, suggesting interactions with kin are particularly relaxing. Scratching rates shown by groomers were unaffected by grooming interactions. These results highlight that the emotional states following grooming can have a complex time course, and may contribute to explain the inconsistencies found in the previous literature.

Anxiety in Geoffroy's spider monkeys (Ateles geoffroyi): Can scratching be used as an indicator?

Self-directed behavior, such as self-scratching (hereafter, scratching), occurs in several taxa across the animal kingdom, including nonhuman primates. There is substantial evidence that scratching is an indicator of anxiety-like emotions in a variety of nonhuman primate species. Despite its importance as a window into emotional states, few studies have investigated scratching in Platyrrhines. We investigated scratching patterns of 24 Geoffroy's spider monkeys (Ateles geoffroyi) belonging to a group living in the Otoch Ma'ax Yetel Kooh protected area in the Yucatàn peninsula (Mexico). We assessed whether scratching could be used as an indicator of anxiety levels in this species by testing predictions based on contexts and behaviors associated with risk and uncertainty. We found no effect of the subject's sex and age, subgroup size, male presence, and the occurrence of fusions between subgroups on scratching rates. Similarly, we found no effect of infant proximity on their mother's scratching rates. Supporting our prediction, we found evidence that isolation from conspecifics affected scratching rates as individuals scratched more frequently the more time they spent isolated. Being in proximity with a partner with a relationship characterized by uncertainty affected scratching rates as individuals scratched more frequently when in proximity with a partner with whom they engaged in embraces (an indicator of uncertainty) than when in proximity with a partner with whom they did not exchange embraces. Our study provides insight into the factors affecting scratching in Geoffroy's spider monkeys, suggesting that scratching may indicate anxiety in this species at least in some contexts and thus opening a window into the emotional experience of another Platyrrhine monkey species.

Monitoring of group mates in relation to their behavior in mandrills.

Primates are known to have considerable knowledge about the social relationships that link their group mates and are likely to derive this information from observing the social interactions that occur in their social group. They may, therefore, be hypothesized to pay particular attention to the social interactions involving group mates. In this study, we evaluated how the attention captive mandrills (Mandrillus sphinx) devote to their group mates was modulated by the behavior of the latter. Mandrills looked most frequently at foraging individuals and least frequently at sleeping individuals. Mandrills also looked at grooming individuals more than at individuals that were simply sitting in contact. Grooming dyads were looked at regardless of the social rank and kinship of the individuals involved. These results contribute to our understanding of how primates obtain their social knowledge.

Mandrills represent their own dominance hierarchy on a cardinal, not ordinal, scale.

Attempts to measure dominance relationships using cardinal, rather than ordinal ranks have a long history. Nevertheless, it is still unclear if cardinal dominance ranks have an impact on the life of animals. In particular, no information is available on how individual group living animals represent their own dominance hierarchy. This can be investigated testing whether cardinal rank differences affect how animals interact with different group mates. In this study, we evaluated how mandrills (Mandrillus sphinx) interacted with group mates in relation to differences in cardinal ranks while controlling for differences in ordinal ranks. Mandrills were more likely both to avoid an approaching group mate and to direct their grooming to a group mate when differences in cardinal ranks were larger (controlling for differences in ordinal ranks). These results suggest mandrills represent their own dominance hierarchy as based on a cardinal, not an ordinal, scale.

Age-related changes in the social behavior of tufted capuchin monkeys.

The effects of aging on the social behavior of nonhuman primates is little understood, especially in New World monkeys. We studied the members of a colony of tufted capuchin monkeys (Sapajus sp.) in order to evaluate age related changes in their social behavior. We conducted observations on 25 subjects aged 4-36 years, living in captive social groups. We found that affiliative interactions (grooming and proximity) decreased with age, and that grooming was increasingly directed to a single preferred partner. Manipulation of objects in the environment also decreased with age, while locomotion and aggression showed no change. Overall, these results concur with previous findings on both human and nonhuman primates, and cast doubts on interpretations of age associated changes in human social behavior that rely of uniquely human advanced cognitive capacities.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34-38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Factors affecting cashew processing by wild bearded capuchin monkeys (Sapajus libidinosus, Kerr 1792).

Cashew nuts are very nutritious but so well defended by caustic chemicals that very few species eat them. We investigated how wild bearded capuchin monkeys (Sapajus libidinosus) living at Fazenda Boa Vista (FBV; Piauí, Brazil) process cashew nuts (Anacardium spp.) to avoid the caustic chemicals contained in the seed mesocarp. We recorded the behavior of 23 individuals toward fresh (N = 1282) and dry (N = 477) cashew nuts. Adult capuchins used different sets of behaviors to process nuts: rubbing for fresh nuts and tool use for dry nuts. Moreover, adults succeed to open dry nuts both by using teeth and tools. Age and body mass significantly affected success. Signs of discomfort (e.g., chemical burns, drooling) were rare. Young capuchins do not frequently closely observe adults processing cashew nuts, nor eat bits of nut processed by others. Thus, observing the behavior of skillful group members does not seem important for learning how to process cashew nuts, although being together with group members eating cashews is likely to facilitate interest toward nuts and their inclusion into the diet. These findings differ from those obtained when capuchins crack palm nuts, where observations of others cracking nuts and encounters with the artifacts of cracking produced by others are common and support young individuals' persistent practice at cracking. Cashew nut processing by capuchins in FBV appears to differ from that observed in a conspecific population living 320 km apart, where capuchins use tools to open both fresh and dry nuts. Moreover, in the latter population, chemical burns due to cashew caustic compounds appear to be common. The sources of these differences across populations deserve investigation, especially given that social influences on young monkeys learning to open cashew nuts at FBV seem to be nonspecific. Am. J. Primatol. 78:799-815, 2016. © 2016 Wiley Periodicals, Inc.

Exchanging grooming, but not tolerance and aggression in common marmosets (Callithrix jacchus).

In this study, we investigated the reciprocal exchanges of grooming, tolerance and reduced aggression in common marmosets (Callithrix jacchus), a cooperatively breeding primate whose groups are typically characterized by uniformly high genetic relatedness and high interdependency between group members. Both partner control and partner choice processes played a role in the reciprocal exchanges of grooming. In contrast, we did not find any evidence of reciprocity between grooming and tolerance over a preferred food source or between grooming and reduced aggression. Thus, reciprocity seems to play a variable role in the exchange of cooperative behaviors in marmosets.

Partner choice promotes cooperation: the two faces of testing with agent-based models.

Reciprocity is one of the most debated among the mechanisms that have been proposed to explain the evolution of cooperation. While a distinction can be made between two general processes that can underlie reciprocation (within-pair temporal relations between cooperative events, and partner choice based on benefits received), theoretical modelling has concentrated on the former, while the latter has been often neglected. We developed a set of agent-based models in which agents adopted a strategy of obligate cooperation and partner choice based on benefits received. Our models tested the ability of partner choice both to reproduce significant emergent features of cooperation in group living animals and to promote the evolution of cooperation. Populations formed by agents adopting a strategy of obligate cooperation and partner choice based on benefits received showed differentiated "social relationships" and a positive correlation between cooperation given and received, two common phenomena in animal cooperation. When selection across multiple generations was added to the model, agents adopting a strategy of partner choice based on benefits received outperformed selfish agents that did not cooperate. Our results suggest partner choice is a significant aspect of cooperation and provides a possible mechanism for its evolution.

Do displacement activities help preschool children to inhibit a forbidden action?

Displacement activities are commonly recognized as behavioral patterns, mostly including self-directed actions (e.g., scratching, self-touching), that often occur in situations involving conflicting motivational tendencies. In ethology, several researchers have suggested that displacement activities could facilitate individuals in dealing with the stress experienced in a frustrating context. In child developmental research, some authors have assessed whether distraction strategies could help children to inhibit a dominant response during delay of gratification tasks. However, little is known about the displacement activities that young children may produce in such situations. This study was aimed at investigating whether displacement activities had an effect on preschool children's ability to postpone an immediate gratification (i.e., interacting with an attractive toy, a musical box), thereby functioning as regulators of their emotional state. To this end, we administered 143 2- to 4-year-olds with a delay maintenance task and related their performance with displacement activities they produced during the task and with actions with an external object. Children's latency to touch the musical box was positively related to their rate of displacement activities. However, the rate of displacement activities increased progressively as long as the children were able to inhibit the interaction with the musical box. In addition, the rate of displacement activities during the first 1 min of test did not predict the ability of children to inhibit the interaction with the box. These results suggest that displacement activities represented a functionless by-product of motivational conflict rather than a strategy that children used to inhibit their response to an attractive stimulus.

Relationship between dominance hierarchy steepness and rank-relatedness of benefits in primates.

In animal social groups, the extent to which individuals consistently win agonistic interactions and their ability to monopolize resources represent 2 core aspects of their competitive regime. However, whether these two aspects are closely correlated within groups has rarely been studied. Here, we tested the hypothesis that hierarchy steepness, which is generally used to represent power differentials between group members, predicts the variation in the distribution of fitness-related benefits (i.e. fecundity, infant survival, mating success, and feeding success) in relation to individual dominance ranks. We tested this hypothesis in primate groups using comparative phylogenetic meta-analytical techniques. Specifically, we reviewed published and unpublished studies to extract data on individual dominance ranks, their access to fitness-related benefits, and hierarchy steepness. We collected and included in our analysis a total of 153 data points, representing 27 species (including 2 chimpanzee sub-species). From these, we used 4 common methods to measure individual dominance ranks and hierarchy steepness, i.e. D ij -based normalized David's scores, randomized Elo-ratings, and David's scores and Elo-ratings estimated in Bayesian frameworks. We found that hierarchy steepness had no effect on the strength of the relationship between dominance rank and access to fitness-related benefits. Our results suggest that hierarchy steepness does not reflect between-group variation in the extent to which individual dominance affects the acquisition of fitness-related benefits in primates. Although the ability to win agonistic encounters is essential, we speculate that other behavioral strategies adopted by individuals may play crucial roles in resource acquisition in animal competitive regimes.

Precursors and aftermath of severe targeted aggression in captive cotton-top tamarins.

We observed a zoo-housed group of cotton-top tamarins (Saguinus oedipus) before and after a bout of severe targeted aggression directed towards two of its members. The aggression was so severe and repeated that the zoo personnel was forced to remove the two victims and the main aggressor. In the tense period that preceded removal, the tamarins showed increased aggression, a steeper and linear dominance hierarchy, and reduced post-conflict reconciliation compared to the period following removal. In contrast, affiliative interactions such as grooming and peaceful food transfers did not differ in the two periods of observations. Patterns of reciprocity also remained stable. These results highlight the flexibility of tamarin social relationships and provide useful information for managing captive colonies and improving animal welfare.

Food transfers in capuchin monkeys: an experiment on partner choice.

Although most primates live in groups, experiments on reciprocity usually test individuals in dyads. This could hide the processes emerging in richer social settings, reducing the ecological validity of the results. We run an experiment on reciprocal food transfers testing capuchin monkeys (Cebus apella) in triads, so that subjects could choose to allow access to their food to either of their two partners. We tested the hypothesis that partner choice was related to a comparison of long-term social bonds with the two partners, more than to a comparison of recent food transfer events from the two partners. The results confirmed this hypothesis, thus supporting the notion that reciprocal partner preferences are based on long-term accounts of benefits that have been exchanged.

Hierarchical steepness, counter-aggression, and macaque social style scale.

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four-grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style-two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter-aggression)-to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter-aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter-aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species' phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness.

Variation in communicative complexity in relation to social structure and organization in non-human primates.

Communicative complexity relates to social complexity, as individuals in more complex social systems either use more signals or more complex signals than individuals living in less complex ones. Taking the individual group member's perspective, here we examine communicative complexity in relation to social complexity, which arises from two components of social systems: social structure and social organization. We review the concepts of social relationships and social complexity and evaluate their implications for communicative and cognitive complexity using examples from primate species. We focus on spider monkeys (Ateles geoffroyi), as their social organization is characterized by flexibility in grouping dynamics and they use a variety of communicative signals. We conclude that no simple relationship exists among social complexity, communicative complexity and cognitive complexity, with social complexity not necessarily implying cognitive complexity, and communicative and cognitive complexity being independently linked to social complexity. To better understand the commonly implied link between social complexity and cognitive complexity it is crucial to recognize the complementary role of communicative complexity. A more elaborated communicative toolkit provides the needed flexibility to deal with dynamic and multifaceted social relationships and high variation in fission-fusion dynamics. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Social relationships between adult females and the alpha male in wild tufted capuchin monkeys.

Primates are notable for the widespread presence of long-term female-male associations which go beyond the mating context. However, little attention has been given to the factors that affect within-species variation in female-male relationships, especially among New World primates. Although detailed accounts of heterosexual relationships in Cebus species are scarce, a few studies have suggested the occurrence of strong associations between adult females and high-ranking males. This study explores affiliative relationships between females and the alpha male during the nonbreeding season in wild tufted capuchin monkeys (Cebus apella nigritus). Affiliative relationships were explored through female-male patterns of spatial proximity and grooming. By adopting a social network approach, we analyzed: (1) whether the alpha male is the preferred male partner for females and, (2) whether variation (if any) in female-alpha male affiliation can be explained through both female individual characteristics and social network metrics. Our results showed that alpha males were the favorite male partner for adult females in the proximity networks, but this did not hold true in the grooming networks. In addition, female-alpha male interaction patterns showed considerable variation, with only some females being strongly associated with the alpha male. Our results suggest that such a variation can be explained by female dominance rank, level of centrality (the quantity and intensity of spatial connection with other females) and prestige (the quantity of grooming received by other females) in female-female social networks. Taken together, these findings highlight two aspects of female-alpha male relationships in tufted capuchin monkeys: the alpha male represents the most socially integrated male in the group, and females with high dominance ranks and high centrality in both proximity and grooming networks show stronger relationships with the alpha male.

Testing the two sides of indirect reciprocity in tufted capuchin monkeys.

We addressed two different aspects of indirect reciprocity in tufted capuchin monkeys (Sapajus spp.) studying two common cooperative behaviours, grooming and food sharing. In an observational study, we tested whether capuchin monkeys were more likely to groom an individual that had just groomed a group mate than an individual that had not groomed anybody. In an experimental study, we tested whether capuchin monkeys were more likely to share their food with a partner when in the presence of a bystander (or of an image of the eyes of a conspecific) than when alone with their partner. In the observational study, we found an increase in the likelihood of receiving grooming after giving grooming, but this effect seemed to depend on social facilitation rather than on indirect reciprocity, as we found a similar effect after receiving (rather than giving) grooming. In the experimental study, the presence of a bystander or of an image of eyes did not affect the amount of food transferred to a group mate. Overall, these results suggest capuchin monkeys do not engage in indirect reciprocity.

The relative roles of kinship and reciprocity in explaining primate altruism.

Several hypotheses have been proposed to explain the evolution of altruistic behaviours. Their relative roles in explaining actual cases of animal altruism are, however, unclear. In particular, while kin selection is widely believed to have a pervasive influence on animal behaviour, reciprocity is generally thought to be rare. Despite this general agreement, there has been no direct test comparing the relative roles of kinship and reciprocity in explaining animal altruism. In this paper, we report on the results of such a test based on a meta-analysis of allogrooming in primates, grooming being probably the most common altruistic behaviour among mammals. In direct contrast to the prevailing view, reciprocity played a much larger role than kinship in explaining primate allogrooming. These results point to a more significant role of reciprocity in the evolution of animal altruism than is generally acknowledged.

Conflict over grooming topography between mandrill groomers and groomees.

Grooming directed to different body areas is likely to imply different costs and benefits for groomers and groomees. In this study, we investigated social influences on grooming topography in captive female mandrills (Mandrillus sphinx). Subordinate groomers preferred to direct grooming to "safe" areas (the back and rump) compared to dominant groomers, while subordinate groomees did not solicit preferentially grooming to safe areas. Groomers tended to initiate grooming episodes from safe areas, while groomees solicited the switch to unsafe areas. Our results highlight a previously unrecognized source of conflict between the partners of grooming, one of the most common cooperative interactions in animals.