Testing for anticipation of partners' reciprocity and other social parameters: An experimental approach in wild vervet monkeys (Chlorocebus pygerythrus).

It has been suggested that social challenges in group-living species in which individuals maintain long-term relationships select for advanced cognitive processes. A key challenge for testing this hypothesis is to design experiments that allow the assessment of animals' knowledge of conspecifics and how they use that information to their own advantage. Here, we present data on wild vervets using an experimental paradigm that induced a competitive context. After training females to obtain food from a personal box, we placed their box in proximity to another monkey's personal box to create potential conflict. We have previously shown that high-ranking female vervets exchange tolerance, though to a lesser extent when the audience contains an individual that outranks the subordinate partner, and coalitionary support for grooming. Our questions here were (a) whether subordinates adjust the likelihood of approaching their box when their recent dominant grooming partners are already present and (b) if dominants are more likely to threaten the box partner in the presence of their recent high-ranking grooming partner. Although we found some effects of age and group on the subjects' behavior, no evidence emerged that subordinates incorporate the effects of recent grooming history. Dominants were more likely to threaten the box partner in the presence of a high-ranking individual within the audience, independent of their own grooming history. We suggest that our paradigm can be used to discern the degree to which individuals of different species take into account recent social history with others that affect these others' behavior toward themselves. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Female vervet monkeys fine-tune decisions on tolerance versus conflict in a communication network.

Group living promotes opportunities for both cooperation and competition. Selection on the ability to cope with such opposing social opportunities has been proposed as a driving force in the evolution of large brains in primates and other social species. However, we still know little about the degree of complexity involved in such social strategies. Here, we report advanced social strategies in wild vervet monkeys. Building on recent experimental evidence that subordinate females trade grooming for tolerance from higher-ranking individuals during foraging activities, we show that the audience composition strongly affects this trade. First, tolerance was lower if the audience contained individuals that outranked the subordinate partner, independently of audience size and kinship relationships. Second, we found a significant interaction between previous grooming and relative rank of bystanders: dominant subjects valued recent grooming by subordinates while intermediate ranked subjects valued the option to aggress subordinate partners in the presence of a dominant audience. Aggressors were also more likely to emit coalition recruitment calls if the audience contained individuals that outranked the subordinate partner. In conclusion, vervet monkeys include both recent grooming and knowledge about third-party relationships to make complex decisions when trading grooming for tolerance, leading to a finely balanced trade-off between reciprocation and opportunities to reinforce rank relationships.

Intergroup Variation of Social Relationships in Wild Vervet Monkeys: A Dynamic Network Approach.

Social network analysis is a powerful tool that enables us to describe and quantify relationships between individuals. So far most of the studies rely on the analyses of various network snapshots, but do not capture changes over time. Here we use a stochastic actor-oriented model (SAOM) to test both the structure and the dynamics of relationships of three groups of wild vervet monkeys. We found that triadic closure (i.e., the friend of a friend is a friend) was significant in all three groups while degree popularity (i.e., the willingness to associate with individuals with high degree of connections) was significant in only two groups (AK, BD). The structure and dynamics of relationships according to the attributes of sex, matrilineand age differed significantly among groups. With respect to the structure, when analyzing the likelihood of bonds according to the different attributes, we found that individuals associate themselves preferably to individuals of the same sex only in two groups (AK, NH), while significant results for attachment to individuals of the same matriline were found also in two groups (BD, NH). With respect to the dynamics, i.e., how quickly relationships are modified, we found in two groups (AK, BD) that females' relationships were more prone to variation than males.' In the BD group, relationships within high-ranking matrilines were less stable than low-ranking ones while in the NH group, juveniles' relationships were also less stable than adults' ones. The intergroup variation indicates that establishing species-specific or even population specific characteristics of social networks for later between-species comparisons will be challenging. Although, such variation could also indicate some methodological issue, we are quite confident that data was collected similarly within the different groups. Our study therefore provides a potential new method to quantify social complexity according to natural demographic variation.

Wild Vervet Monkeys Trade Tolerance and Specific Coalitionary Support for Grooming in Experimentally Induced Conflicts.

Grooming is a key social behavior in many primate species. Research has focused on three important aspects: the short- and long-term trading patterns of grooming for itself and/or for other commodities like tolerance or coalitionary support, the issue of whether exchanges are a convincing example for reciprocity, and what decision rules underlie trading. These issues remain largely unresolved due to the correlative nature of observational studies and the rarity of experimental studies. Here, we present a new experimental paradigm to address these questions in wild vervet monkeys (Chlorocebus pygerythrus). Adult females were first trained to approach a personal box, identifiable by unique color patterns, to access high-quality food. During the experiments, two boxes were placed next to each other to induce conflict through forced proximity. We found that while dominants were generally more tolerant toward bonded individuals, recent grooming increased tolerance independently of relationship quality. The latter result shows that vervet monkeys traded grooming for short-term tolerance, where dominants used a direct-reciprocity decision rule. In contrast, females invariably supported the higher-ranking opponent in a conflict, independently of who was the recent grooming partner. Nevertheless, recent grooming increased the probability that a female supported the partner during conflicts with a low-ranking third party. Thus, females' decisions about coalitionary support seem to integrate information about the current social hierarchy with recent grooming events. In conclusion, decision rules underlying trading of grooming for other commodities involve a variety of timescales and factors.

Social networks in primates: smart and tolerant species have more efficient networks.

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species). We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities.

Potent social learning and conformity shape a wild primate's foraging decisions.

Conformity to local behavioral norms reflects the pervading role of culture in human life. Laboratory experiments have begun to suggest a role for conformity in animal social learning, but evidence from the wild remains circumstantial. Here, we show experimentally that wild vervet monkeys will abandon personal foraging preferences in favor of group norms new to them. Groups first learned to avoid the bitter-tasting alternative of two foods. Presentations of these options untreated months later revealed that all new infants naïve to the foods adopted maternal preferences. Males who migrated between groups where the alternative food was eaten switched to the new local norm. Such powerful effects of social learning represent a more potent force than hitherto recognized in shaping group differences among wild animals.

Third-party ranks knowledge in wild vervet monkeys (Chlorocebus aethiops pygerythrus).

The Machiavellian/Social Intelligence Hypothesis proposes that a complex social environment selected for advanced cognitive abilities in vertebrates. In primates it has been proposed that sophisticated social strategies like obtaining suitable coalition partners are an important component of social intelligence. Knowing the rank relationships between group members is a basic requirement for the efficient use of coalitions and the anticipation of counter-coalitions. Experimental evidence for such knowledge currently exists in only few species. Here, we conducted rank reversal playback experiments on adult females belonging to three different groups of free-ranging vervet monkeys (Chlorocebus aethiops pygerythrus) to test their knowledge of the female hierarchy. Playbacks simulating rank reversals (subordinate aggressing a dominant) induced longer looking times than playbacks simulating a dominant aggressing a subordinate. Vervet monkey females therefore seem to compute the rank relationships between other females. Our results suggest that detailed social knowledge about rank relationships may be widespread in primates and potentially also in other species living in stable groups.