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.

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.

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'.

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.

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.

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.

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.

Acquisition and functional consequences of social knowledge in macaques.

To manoeuvre in complex societies, it is beneficial to acquire knowledge about the social relationships existing among group mates, so as to better predict their behaviour. Although such knowledge has been firmly established in a variety of animal taxa, how animals acquire such knowledge, as well as its functional significance, remains poorly understood. In order to understand how primates acquire and use their social knowledge, we studied kin-biased redirected aggression in Japanese macaques (Macaca fuscata) relying on a large database of over 15 000 aggressive episodes. Confirming previous research, macaques redirected aggression preferentially to the kin of their aggressor. An analysis that controlled for the rate of affiliation between aggressors and targets of redirection showed that macaques identified the relatives of group mates on the basis of the frequency of their ongoing associations. By contrast, having observed group mates interact with their mother as infants did not increase the monkeys' success in correctly identifying kin relationships among third parties. Inter-individual variation in the successful identification of the kin of aggressors and in redirecting aggression accordingly translated into differences in the amount of aggression received, highlighting a selective advantage for those individuals that were better able to acquire and use social knowledge.

Reciprocity in group-living animals: partner control versus partner choice.

Reciprocity is probably the most debated of the evolutionary explanations for cooperation. Part of the confusion surrounding this debate stems from a failure to note that two different processes can result in reciprocity: partner control and partner choice. We suggest that the common observation that group-living animals direct their cooperative behaviours preferentially to those individuals from which they receive most cooperation is to be interpreted as the result of the sum of the two separate processes of partner control and partner choice. We review evidence that partner choice is the prevalent process in primates and propose explanations for this pattern. We make predictions that highlight the need for studies that separate the effects of partner control and partner choice in a broader variety of group-living taxa.

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.

Symmetry-based reciprocity: evolutionary constraints on a proximate mechanism.

Background. While the evolution of reciprocal cooperation has attracted an enormous attention, the proximate mechanisms underlying the ability of animals to cooperate reciprocally are comparatively neglected. Symmetry-based reciprocity is a hypothetical proximate mechanism that has been suggested to be widespread among cognitively unsophisticated animals. Methods. We developed two agent-based models of symmetry-based reciprocity (one relying on an arbitrary tag and the other on interindividual proximity) and tested their ability both to reproduce significant emergent features of cooperation in group living animals and to promote the evolution of cooperation. Results. Populations formed by agents adopting symmetry-based reciprocity showed differentiated "social relationships" and a positive correlation between cooperation given and received: two common aspects of animal cooperation. However, when reproduction and selection across multiple generations were added to the models, agents adopting symmetry-based reciprocity were outcompeted by selfish agents that never cooperated. Discussion. In order to evolve, hypothetical proximate mechanisms must be able to stand competition from alternative strategies. While the results of our simulations require confirmation using analytical methods, we provisionally suggest symmetry-based reciprocity is to be abandoned as a possible proximate mechanism underlying the ability of animals to reciprocate cooperative interactions.

Short-term costs and benefits of grooming in Japanese macaques.

This study investigated the short-term consequences of giving grooming in Japanese macaques (Macaca fuscata) in order to obtain information on its immediate costs and benefits. Giving grooming was associated with increased aggression received from groomees and decreased aggression received from third parties (but only as long as the groomer maintained proximity to the groomee). Grooming was also associated with decreased scratching rates. These results emphasize the unpredictable outcome of individual grooming interactions and the difficulties of social decision-making for monkeys living in despotic societies.

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.

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.

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.

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.