Experimental evidence of parasite-induced behavioural alterations modulated by food availability in wild capuchin monkeys.

In disease dynamics, host behaviour can both determine the quantity of parasites a host is exposed to, and be a consequence of infection. Observational and experimental studies in non-human primates have consistently found that parasitic infections result in less movement and reduced foraging, which was interpreted as an adaptive response of the host to counter infection. Variation in host nutritional condition may add complexity to the infection-behaviour relationship, and its influence may shed light on its significance. To experimentally evaluate how host activity and social relationships are affected by the interaction of parasitism and nutrition, during two years we manipulated food availability by provisioning bananas, and helminth infections by applying antiparasitic drugs, in two groups of wild black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. We collected faecal samples to determine the intensity of helminthic infections, as well as data on behaviour and social proximity. Individuals with unmanipulated helminth burdens foraged less than dewormed individuals only when food provisioning was low. Resting time was increased when capuchins were highly provisioned, but it did not vary according to the antiparasitic treatment. Proximity associations to other group members were not affected by the antiparasitic treatment. This is the first experimental evidence of a modulating effect of food availability on the influence of helminth infection on activity in wild primates. The findings are more consistent with an impact on host behaviour due to the debilitating effect caused by parasites than with an adaptive response to help fight infections.

Grooming site preferences in black capuchin monkeys: Hygienic vs. social functions revisited.

When primates groom each other, they tend to concentrate on those parts of the body they cannot efficiently self-groom (i.e., not visually accessible), and prefer to intensify grooming in areas with high hair density, thus suggesting a hygienic function. However, preferences for some body sites over others during social grooming may also result from different degrees of social bonding and relative dominance. To assess the relative importance of physical (hygienic) and social factors, we examined grooming interactions in two groups of wild black capuchin monkeys (Sapajus nigritus) during 15 nonconsecutive months. We evaluated the distribution of social grooming across body sites according to their accessibility by self-grooming and hair density. At the same time, we assessed whether the degree of dyadic social bonding affects the relative body orientation between groomer and groomee and the access to vulnerable body sites (e.g., face, throat, groin) during grooming. As expected, capuchins preferentially groomed inaccessible body sites (e.g., back and head), with a disproportionate effort directed to the tufts of their partners. We found that dyadic social bond strength, together with rank distance, significantly affected the proportion of grooming in ventro-ventral body relative orientation only in dominant-subordinate groomer-groomee dyads. This may indicate that, when two individuals differ in rank but are strongly bonded, the level of uncertainty related to the social context is already resolved and thus grooming per se is no longer perceived by the subordinate as an uncertain/risky situation. We found no effect of social bonding on grooming vulnerable body sites for any type of dyad. Our findings suggest that grooming site preferences in black capuchin monkeys simultaneously reflect hygienic and social functions.

The impact of food provisioning on parasite infection in wild black capuchin monkeys: a network approach.

Nonhuman primates host a variety of gastrointestinal parasites that infect individuals through different transmission routes. Social contact among group members (e.g., body contact, grooming) brings the risk of parasite infection, especially when the pathogen infection is directly transmitted. Along with this, accidental provisioning (i.e., food provisioning occurring during close tourist-wildlife interactions) is also considered to increase the risk of infection, as aggregation during feeding can cause higher exposure to parasite infective stages. However, while some attention has been paid to the relationship between social behavior and parasites, the link between accidental food provisioning and characteristics of parasite infection in primates has thus far received less attention. This study examines the potential effect of accidental provisioning on patterns of inter-individual spatial association, and in turn on parasite infection risk in a wild group of black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. To do so, we simulated events of accidental provisioning via researcher-managed provisioning experiments and tested whether experimental provisioning affects the inter-individual spatial distribution within groups. In addition, we determined whether patterns of parasite infection were better predicted by naturally occurring spatial networks (i.e., spatial association during natural observations) or by provisioning spatial networks (i.e., spatial interactions during experimental provisioning). We found a significant increase in network centrality that was potentially associated with an overall increase in individual connections with other group members during experimental trials. However, when assessing the effects of natural and provisioning network metrics on parasite characteristics, we did not observe a significant effect of centrality measures (i.e., closeness and betweenness) on parasite richness and single infection by Filariopsis sp. Taken together, our findings suggest that alterations of within-group spatial networks due to accidental provisioning may have a limited influence in determining the characteristics of parasite infections in black capuchin monkeys.