The role of anointing in robust capuchin monkey, Sapajus apella, social dynamics. Emily J.E. Messer et al. Animal Behaviour, Volume 190, August 2022, Pages 103-114. https://doi.org/10.1016/j.anbehav.2022.04.017
Highlights
•Social network analysis revealed association changes in group organization.
•Anointing is an antiparasitic behaviour analogous to social grooming.
•Social anointing has evolved within the context of complex social behaviour.
•We conceptualize anointing in capuchins as ‘social medication’.
Abstract: Anointing is a behaviour in which animals apply pungent-smelling materials over their bodies. It can be done individually or socially in contact with others. Social anointing can provide coverage of body parts inaccessible to the individual, consistent with hypotheses that propose medicinal benefits. However, in highly social capuchin monkeys, Sapajus and Cebus spp., anointing has been suggested to also benefit group members through ‘social bonding’. To test this, we used social network analysis to measure changes in proximity patterns during and shortly after anointing compared to a baseline condition. We presented two capuchin groups with varying quantities of onion, which reliably induces anointing, to create ‘rare resource’ and ‘abundant resource’ conditions. We examined the immediate and overall effects of anointing behaviour on the monkeys' social networks, using patterns of proximity as a measure of social bonds. For one group, proximity increased significantly after anointing over baseline values for both rare and abundant resource conditions, but for the other group proximity only increased following the rare resource condition, suggesting a role in mediating social relationships. Social interactions were affected differently in the two groups, reflecting the complex nature of capuchin social organization. Although peripheral males anointed in proximity to other group members, the weak centrality only changed in one group following anointing bouts, indicating variable social responses to anointing. We suggest in part that anointing in capuchins is analogous to social grooming: both behaviours have an antiparasitic function and can be done individually or socially requiring contact between two or more individuals. We propose that they have evolved a social function within complex repertoires of social behaviours. Our alternative perspective avoids treating medicinal and social explanations as alternative hypotheses and, along with increasing support for the medical explanations for anointing, allows us to conceptualize social anointing in capuchins as ‘social medication’.
Keywords: anointingcapuchin monkeyfur rubbingsocial bondingsocial network analysis
Discussion
We observed that capuchin monkeys enthusiastically anointed whether resource density was high or low. However, the effect of anointing on their social dynamics varied by group and the density of resources available. While we found increased levels of association after anointing for the West group regardless of resource density, the East group monkeys increased their associations after anointing only when the resource was rare.
When resources were sufficiently plentiful for every monkey to have a piece of onion, strength values in the West group were significantly higher (either having stronger or more associations with others) after anointing in both resource conditions compared to the baseline. This suggests that anointing can mediate social relationships, since monkeys did not need to increase proximity to anoint in the abundant resource condition. Moreover, their associations were highest after anointing in the abundant resource condition compared to the rare resource condition, showing that the monkeys chose to continue to associate together after anointing. Conversely in the East group, we found that the monkeys' associations were highest after anointing in the rare resource condition, indicating that the monkeys remained closer together than in the baseline condition after anointing only when they would have had to come close together to gain access to limited materials. Thus, associations with group members were higher after anointing regardless of the density of available resources for the West monkeys. By contrast in the East group, we saw changes in social structure emerge after anointing when resource density was lower, an increase in proximity patterns that could in part be due to the limited resources available.
During anointing, the West group's associations increased above the baseline in the two anointing conditions, but the effect was greater in the abundant resource condition. Thus, when resource density was higher, which could facilitate individual anointing and decrease associations, monkeys in the West group were opting to increase their associations. Conversely, in the East group, we found no differences in the monkeys' associations during anointing in either of the two resource conditions compared to the baseline. Therefore, although the East group engaged in anointing, the effect on their social structure was only evident after anointing, perhaps after the monkeys had to come together to access the limited resource. These group differences are likely to be a reflection of the complex nature of capuchin social organization.
Differing social dynamics within the East and West groups could be contributing to these differing results. The West group was formed of one main matriline plus two unrelated adult males, whereas the East group had two main matrilines and two unrelated adult males. Thus, from the outset, the West group individuals had a higher level of overall relatedness between individuals than the East group. Indeed, Welker, Hoehmann and Schaefer-Witt (1990) have argued that the matrilines in their captive Cebus apella formed the foundation of the group's social structure (Fragaszy et al., 2004). As such, the West group's main single matriline versus the East group's two matrilines could be contributing to the changes in social dynamics we report. Future work examining the function of social bonding in other capuchin monkeys' anointing behaviour should seek to include measures of relatedness between individuals.
In capuchins, the matrilines underlie rank structures that affect access to resources and social organization. In our two groups of capuchins, the more dominant group members could monopolize resources from subordinates which tended to wait. All the monkeys with the lowest baseline measures of strength (four males: Kato, Toka, Carlos and Manuel; two females: Junon and Pedra) were subordinates. Junon was the only adult female to have a baseline strength score less than one, likely because she was from a different matriline, and subordinate to the two other adult females. While we may expect the four subordinate males to have had lower baseline strength, perhaps indicating they were the most likely to be peripheral males, Pedra's (our only subadult female) low strength was less expected and may change as she reaches sexual maturity.
Our social network analysis provides some support for the social-bonding hypothesis (see also Leca et al., 2007; Paukner & Suomi, 2008; Valderrama et al., 2000), particularly in the West group, where there was an increase in group cohesion in the short term after anointing. Analysis of longer-term changes in social dynamics over time following differing access to anointing materials would provide further insight into any longer-term changes to group social structure.
Only the West group peripheral males' overall integration (connectedness) into their group differed across the five conditions, as peripheral males increased associations during anointing. Although all the peripheral males were engaging in social anointing (E. Messer & M. Bowler, personal observation), and potentially gaining from the functional benefits of reaching inaccessible and nonvisible areas of their body (as we have previously shown with the same group of capuchin monkeys, Bowler et al., 2015), changes in their social integration were not detectable in the East group. This difference might be due to individual differences between the males' positions in the dominance hierarchy of their respective groups. Although both groups had subordinate males with low baseline associations (e.g. Kato and Carlos in the East group and Toka in the West group), both groups also contained subordinate males that had higher centrality scores (e.g. Manuel in the East group, and Diego and Figo in the West group). Moreover, in the West group, Diego, a beta male, became the alpha male after the study. Future work excluding beta males in peripheral male subgroupings (e.g. Izawa, 1980) and including more data collected on the social network position of other peripheral males to increase the sample size would be useful to examine any subtler changes, for example in competitive friction. When we compared the rest of the group centrality measures without the peripheral males', we found no significant effect of anointing, indicating that the remaining monkeys did not become more integrated into the groups after anointing. Thus, although anointing impacted the monkeys’ strength scores, these associations may be short lived. We surmise that anointing with onions in robust capuchin monkeys appears to impact individual connectedness rather than group integration.
Because we focused on monkey proximity patterns and collected scan data every 4 min, we could not accurately assess who joined whom and how monkeys reacted to these aggregations during anointing. To provide further insights into the impact of such social influences and the effect of resource density on individuals’ proximal choices, future work could explore the spread of social and individual anointing over time in groups of monkeys, and any contagious effects of the behaviour.
In capuchins, anointing has an apparent role in self-medication (Alfaro et al., 2011). Previous studies of anointing have shown that social anointing may be an entirely functional extension of this, helping to provide medicinal coverage for group members (e.g. Bowler et al., 2015), which may be relatives or potential hosts for infectious parasites. As such, these phenomena may also provide some insight into the basis of human healthcare networks where individuals care for the sick (Kessler, 2020). Future work examining any changes in group structure during social anointing could provide further insights into anointing as social medicine.
Here we have shown that anointing in robust capuchin monkeys affected social behaviour through increased and/or stronger associations. There is perhaps a strong partial analogy here with grooming, shown in capuchin monkeys to serve various hygiene and social functions (Fragaszy et al., 2004). Autogrooming appears to fill an obvious role of removing ectoparasites and other debris while social grooming (allogrooming) extends this benefit by reaching parts of the body that an individual cannot reach itself by a groomer actively grooming another individual (Barton, 1985). Adding to this, groomers could also benefit if they consume parasites they remove. However, there is also plentiful evidence that social grooming serves additional social functions (di Bitetti, 1997; Dunbar, 1991; Sánchez-Villagra et al., 1998; Nunn, Altizer, & Altizer, 2006), with individuals prioritizing grooming with those ranked slightly higher than themselves (Seyfarth, 1977; but see Parr et al., 1997 which indicates that robust capuchins are more likely to groom other closely ranked individuals). Although grooming likely changes with the social organization and varies with ecological conditions (e.g. see Lazaro-Perea, de Fátima Arruda, & Snowdon, 2004), it has also been shown to be a resource to be traded with others such as for food sharing (de Waal, 1997; but this can be affected by rank differences, e.g. see Jaeggi et al., 2013), or support in aggressive disputes (Hemelrijk, 1994; Seyfarth, 1977; Seyfarth & Cheney, 1984).
Conclusion
Social and medicinal hypotheses for anointing are not mutually exclusive, and while the widespread nature of anointing within the primates and other taxa suggests that there is an underlying nonsocial benefit to the behaviour, like grooming, anointing in capuchin monkeys has evolved within the context of a highly complex repertoire of social behaviours and may have taken on an additional social function. The complexity of social behaviour in these monkeys may make separating the cause and effect of anointing on social structure challenging. Our alternative perspective departs from treating medicinal and social explanations as alternative hypotheses, and along with increasing support for the medical explanations for anointing, justifies describing anointing in capuchin monkeys as ‘social medication’.