Testing the anxiety reduction function of grooming interactions in wild Barbary macaques (Macaca sylvanus)

Together with its hygienic and social function, grooming is thought to reduce anxiety. However, empirical evidence on the anxiety-reduction function of grooming is scarce. We collected 10-minute focal data on the donor and recipient of grooming using the post-grooming / matchedcontrol (PG-MC) method. In these PGs and MCs sessions, we recorded the occurrence of selfdirected behaviours (i.e. scratching and self-grooming), which are behavioural indicators of anxiety. We found mixed evidence of the relationship between anxiety and grooming interactions. The link between grooming and anxiety may be more complex than originally thought

Grooming interactions and cooperation in wild Barbary macaques (Macaca sylvanus)

The study of cooperation has been crucial to research on the evolution of social living in human and animal societies. Grooming interactions have been used as model to investigate the exchange of services in animals. Using both established and novel methodologies, this thesis examines grooming interactions and cooperation in two populations of wild Barbary macaques living in the Middle Atlas Mountains of Morocco. It is important to have a comprehensive idea of the costs and benefits of grooming interactions, and of the effect of grooming interactions on the anxiety of the grooming partners. This thesis showed that, contrary to previous studies, anxiety increased after grooming interactions in both the donor and recipient. This highlights the need to further investigate the link between grooming and emotions. Individuals may also affect the grooming interactions of other group members. This thesis showed that individuals benefit from disrupting grooming interactions of group members by gaining grooming opportunities for themselves and by stopping the group members from grooming each other, although grooming disruptions may be risky. Monkeys may affect others’ grooming interactions to favour their own social and dominance positions. A key aspect of this thesis was also to assess whether grooming is reciprocated in the short-term and which type of reciprocity (i.e. direct, indirect and generalised) play a role in the exchanges of grooming. This study showed that direct but not indirect and generalised reciprocity play a role in the exchange of grooming. While there is a wide range of evidence that direct reciprocity plays a role in the exchange of services in animals, there is little evidence of indirect and generalised reciprocity. Additionally to exchanging grooming for grooming, animals also exchange grooming for other services such as tolerance around food resource and support during agonistic interactions. In this thesis, no evidence of short-term contingency between the exchange of grooming and food tolerance was found. The exchanges of services may be little affected by recent single events, and mechanisms involving an emotional mediation based on long-term social bonds between partners may play a more important role. The capacity to make effective choices among potential social partners is an important social skill, as choosing the best available partner improves the chances to establish successful cooperative interactions. This thesis highlighted, to some extents, the importance of factors such as tolerance and relationship quality between partners, in the performances of individuals and their choice of partners to solve a cooperative task. Tolerant relationships may have been a prerequisite for the evolution of cognitively complex cooperation. Testing a comprehensive framework of predictions, this thesis brings novel contributions to the understanding of grooming interactions and cooperation in wild Barbary macaque

Cooperation in wild Barbary macaques: factors affecting free partner choice

A key aspect of cooperation is partner choice: choosing the best available partner improves the chances of a successful cooperative interaction and decreases the likelihood of being exploited. However, in studies on cooperation subjects are rarely allowed to freely choose their partners. Group-living animals live in a complex social environment where they can choose among several social partners differing in, for example, sex, age, temperament, or dominance status. Our study investigated whether wild Barbary macaques succeed to cooperate using an experimental apparatus, and whether individual and social factors affect their choice of partners and the degree of cooperation. We used the string pulling task that requires two monkeys to manipulate simultaneously a rope in order to receive a food reward. The monkeys were free to interact with the apparatus or not and to choose their partner. The results showed that Barbary macaques are able to pair up with a partner to cooperate using the apparatus. High level of tolerance between monkeys was necessary for the initiation of successful cooperation, while strong social bond positively affected the maintenance of cooperative interactions. Dominance status, sex, age, and temperament of the subjects also affected their choice and performance. These factors thus need to be taken into account in cooperative experiment on animals. Tolerance between social partners is likely to be a prerequisite for the evolution of cooperation

Testing the role of direct, indirect and generalised reciprocity in grooming exchanges of wild Barbary macaques

In non-human primates, grooming is thought to be a costly activity for the donor and beneficial for the recipient. Reciprocity assumes that individuals act as the donor and recipient of grooming and switch roles over time to balance the benefits and costs. Three main patterns of reciprocity may follow a grooming given by A to B: (1) direct reciprocity, where B return the grooming to A; (2) indirect reciprocity, where individual C, not involved in the former grooming between A and B, grooms A; and (3) generalized reciprocity, where B grooms any individual including A. We tested the role of direct, indirect, and generalized reciprocity in explaining grooming exchanges of wild Barbary macaques. We collected the occurrence and latency of the three types of grooming reciprocity during one hour focal session run simultaneously on two partners who just stopped grooming (post-grooming session) or who were in proximity (i.e. within 1.5 meters) without grooming (control session). We ran the analyses on 284 post-grooming sessions and 63 control sessions. Directly reciprocated grooming from B to A was more likely to occur, and occurred earlier when A had previously groomed B than in control sessions. We found no evidence for indirect or generalised reciprocity. Our results indicate that grooming distribution in Barbary macaques is partnerspecific and occurs according to direct reciprocity. Such partner specificity can explain the lack of evidence for generalised reciprocity, whereas indirect reciprocity may be too cognitively demanding to occur in macaques

Grooming increases self-directed behaviour in wild Barbary macaques, Macaca sylvanus

Allogrooming has hygienic and social functions. Moreover, anxiety is thought to be reduced in the first few minutes after a grooming interaction is terminated. Few data exist on postgrooming reduction in anxiety, and mostly concern the recipient of grooming and captive animals. We analysed whether anxiety is reduced after grooming and whether this reduction differs between the donor and recipient of grooming. We collected 10 min postgrooming and matched-control (PGeMC) focal data on the donor and recipient of the same grooming interaction in wild Barbary macaques. We recorded all the occurrences of self-directed behaviours (i.e. self-scratching and self-grooming) as these are reliable indicators of anxiety. The occurrence of self-directed behaviour was greater in PGs than in MCs for both the donor and recipient. This increase in postgrooming anxiety was more evident for the recipient than for the donor. The postgrooming increase in anxiety was not due to a higher risk of receiving aggression after grooming. Unlike previous studies, our results indicate that anxiety may increase after grooming in Barbary macaques. If so, the social and hygienic benefits of grooming may outweigh its short-term anxiety cost. Self-directed behaviour may increase because of the emotional response to the change in activity (e.g. from grooming to travelling) and/or frustration at the termination of grooming. Our findings highlight the need to investigate further the link between emotions and grooming

Introducing a cooperative task to a wild group of Barbary macaques

A key aspect of cooperation is the choice of partners with whom to cooperate, as this determines if an individual can establish a successful cooperative interaction and reduce the chances to be exploited. In most of the experiments on cooperation conducted so far, subjects had no opportunity to choose their cooperative partner, or the choice was reduced between two individuals. Non-human primates, however, live in complex social groups and can choose their social partner among several individuals. We presented a cooperative apparatus to a wild provisioned group of Barbary macaques, leaving them the choice to interact or not with the apparatus, and with any of their group companions. We used the same experiment used in captive studies on cooperation (Crawford, 1937), requiring two monkeys to pull a rope simultaneously in order to both get rewards. We found mixed evidence of cooperation in our study group and we discuss here the methodological and theoretical difficulties of running experiments with free-ranging animals

Divide and rule: costs and benefits of grooming disruption in wild Barbary macaques

In non-human primates, allo-grooming has a hygienic function and is the main behaviour used to establish and maintain friendly relationships (Dunbar, 1991). Allo-grooming is also used as a ‘currency’ that can be exchanged for grooming or other social services such as agonistic support and tolerance over food (Noé & Hammerstein, 1994; Schino, 2007; Carne et al, 2011; Berghänel et al, 2011). The biological market approach predicts that the availability of a commodity and the resource-holding-potential of each animal both affect the payoffs that each animal gain from the exchange of commodities (Noë et al, 2001). For example, when food is scarce only high-ranking individuals have direct access to high-quality food sources whereas low-ranking individuals may exchange a service given (e.g. grooming) against tolerance over food. Allo-grooming can give various benefits (e.g. hygienic or agonistic support) and its distribution is affected by the dominance position of each animal in a group. Therefore, dominant animals can coerce allo-grooming from subordinates or prevent other group members from accessing the social benefits associated with grooming exchanges. Here we analysed whether grooming disruption is a tactic animals use to coerce grooming or to take control over the social relationships other group members build or maintain. Subjects of this study were 13 adult monkeys from a wild non-provisioned group of Barbary macaques living in the Middle Atlas Mountains of Morocco. Data were collected from April to December 2011, using a post-disruption (PD) – matched-control (MC) focal sessions method. As soon as a monkey approached two grooming partners at a minimum distance of 1.5m and stopped the grooming interaction for at least 10 seconds, we ran a 10-minutes PD focal session on the disrupting monkey (i.e. the disrupter). During the PDs, we recorded the first grooming interaction and aggression (e.g. charge or chase) involving the disrupter, as well as ID of the partners. At the same time, data were collected on whether the former grooming partners resumed grooming within 10 minutes from the disruption. Ten minutes MC focal sessions were run on the disrupter and using the same data collection method used in the PD sessions. As potential benefits of the disruption for the disrupter, we considered 1) any grooming between the disrupter and the targets of the disruption (i.e. any of the two former grooming partners), and 2) whether the disruption was successful (i.e. no grooming was observed between the former grooming partners in the PD session) or not. As potential costs of the disruption for the disrupter, we considered aggression received by the disrupter from one or both the former grooming partners. All the disrupters were dominant over one or both former grooming partners. We found no significant difference for the grooming rate exchanged between the disrupter and the former grooming partners between PDs and MCs. However, the disrupters were significantly successful at disrupting grooming in the PDs. Finally, we found that the disrupters were at greater risk of receiving aggression from the former grooming partners in PDs than MCs, but not significantly so. Our results indicate that grooming disruption is costly for the disrupter (i.e. increased aggression risk) but does not give grooming benefits for the disrupter. However, the disrupters were successful at stopping the grooming between two grooming partners. We suggest that monkeys disrupt grooming as a strategy to maintain their dominant position. By stopping grooming, dominants prevent lower-ranking individuals to maintain or build social relationships that these individuals could use to form alliances against dominant animals. This spiteful behaviour may allow individuals to influence the social relationships of other group members at their own advantage. The advantage of keeping a dominant position may outweight the direct cost of the disruption. Such a strategy would be similar to the ‘Divide et impera’ maxim that has been successfully employed in political, military and economic contexts in human history

Gesture production in monkeys, apes and prelinguistic children: The interplay between development and evolution.

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Gestural communication in olive baboons (Papio anubis): repertoire and intentionality

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Gestural Communication in Olive Baboons (Papio anubis): Repertoire and Properties.

International audienceGiven their close phylogenetic proximity with humans, non-human primates are used as model to investigate the evolution of advanced communicative systems. In this regard, studies concerning gestural communication know a renewed interest. In apes, it has been shown that the production of gestures is intentional (e.g. the gestures are adjusted to the attentional state of the recipient), flexible (e.g. the same gesture can be used in several contexts), and variable across individuals and populations. However, compared to apes the gestural communication of monkeys has been understudied. It is thus important to establish which signals are used by monkeys and to investigate whether their gestural system possess the same properties as the gestural system found in apes. In this study we investigated the gestural communication of 47 captive olive baboons of all ages living in three social groups. We used a focal sampling approach to observe each subject for a total of 5 h spread over one year. For each signal produced by the focal subject toward a recipient we recorded its physical description, the orientation of the signaller, the attentional state of the recipient, the situational context and the response of the recipient. We collected a total of 2 820 focal sessions, corresponding to 60 sessions of 5 min for each subject, which allowed to establish a preliminary list of 65 signals produced by the baboons. Preliminary results indicate that 91% of the signals were produced when the signaller was looking at the recipient, and 85% when the recipient was attending. The data will be further analysed to investigate in details the properties of the signals, notably in terms of intentionality, flexibility and variability. This study represents the first systematic investigation of the gestural communicative system of olive baboons and the results will be compared to the gestural system described in apes