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.

Experimental evidence for heterospecific alarm signal recognition via associative learning in wild capuchin monkeys.

Many vertebrate taxa respond to heterospecific alarm calls with anti-predator behaviours. While it is unclear how apparent recognition is achieved, learned associations between the occurrence of the call and the presence of a predator are considered the most likely explanation. Conclusive evidence that this behaviour is indeed underpinned by learning, however, is scarce. This study tested whether wild black capuchin monkeys (Sapajus nigritus) learn to associate novel sounds with predators through a two-phase field experiment. During an initial training phase, three study groups were each presented with a playback of one of the three novel sounds together with a simulated felid predator on four occasions over an 8- to 12-week period. This was followed by a test phase, wherein each of the three sounds was played back to individuals in all three groups, allowing each sound to serve as both a test stimulus for individuals trained with that sound, and a control stimulus for individuals trained with another sound. Antipredator responses were significantly stronger in response to test sounds than to controls. Limited observations suggest that antipredator responses persisted for at least 2 years without reinforcement of the predator-sound link. Additionally, responses to noisier sounds were typically stronger than were those to more tonal sounds, although the effect of sound type cannot be disentangled from potential effects of group. This study provides the strongest evidence to date that learning affects the responses of primates to sounds such as heterospecific alarm calls, and supports the contention that signals provide receivers with information.

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.

Do sexual calls in female black capuchin monkeys (Sapajus nigritus) vary with fertility? An acoustic analysis.

Females across a range of animal taxa produce vocalizations and signals uniquely associated with periods of mating. While such signals may ultimately function to increase female attractivity to males, conflicting findings challenge the extent to which these signals co-vary in accordance with the probability of conception. Female black capuchin monkeys (Sapajus nigritus) display an elaborate repertoire of both vocal and visual components as part of their socio-sexual behavior, and previous analyses have shown that the rates of production of visual, but not vocal, components provide graded information on female ovulation. It remains possible, however, that the acoustic parameters of these sexual calls, rather than their rate of productions, co-vary with female fertility. To test this, we analyzed structural and temporal call parameters from estrous calls and post-copulatory calls recorded over five consecutive mating seasons in 12 sexually mature females at Iguazú National Park, Argentina. Calls given during the fertile phase of the female ovarian cycle were compared with those given during the non-fertile phase, as determined by profiles of female reproductive hormones. Similarly, within the fertile phase, we tested whether temporal or spectral acoustic parameters of calls gradually change with the approach of ovulation. We did not find any significant relationship between call parameters and the two measures of female fertility in either female estrous calls or post-copulatory calls. However, some differences between pre- and post-copulatory calls were apparent. Overall, our results indicate that sexual calls in black capuchin females do not provide precise information about the timing of ovulation, but may allow listeners to make probabilistic inferences about whether copulations have taken place. This, combined with previous findings, suggests that females in our study may use signals in different modalities to convey information about their fertility and sexual behavior with varying degrees of precision.

Male resource defense mating system in primates? An experimental test in wild capuchin monkeys.

Ecological models of mating systems provide a theoretical framework to predict the effect of the defendability of both breeding resources and mating partners on mating patterns. In resource-based mating systems, male control over breeding resources is tightly linked to female mating preference. To date, few field studies have experimentally investigated the relationship between male resource control and female mating preference in mammals due to difficulties in manipulating ecological factors (e.g., food contestability). We tested the within-group male resource defense hypothesis experimentally in a wild population of black capuchin monkeys (Sapajus nigritus) in Iguazú National Park, Argentina. Sapajus spp. represent an ideal study model as, in contrast to most primates, they have been previously argued to be characterized by female mate choice and a resource-based mating system in which within-group resource monopolization by high-ranking males drives female mating preference for those males. Here, we examined whether females (N = 12) showed a weaker preference for alpha males during mating seasons in which food distribution was experimentally manipulated to be less defendable relative to those in which it was highly defendable. Results did not support the within-group male resource defense hypothesis, as female sexual preferences for alpha males did not vary based on food defendability. We discuss possible reasons for our results, including the possibility of other direct and indirect benefits females receive in exercising mate choice, the potential lack of tolerance over food directed towards females by alpha males, and phylogenetic constraints.

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.

Female behavioral proceptivity functions as a probabilistic signal of fertility, not female quality, in a New World primate.

The interests of males and females in mating contexts often conflict, and identifying the information conveyed by sexual signals is central to understanding how signalers manage such conflicts. Research into the information provided by female primate sexual signals has focused on exaggerated anogenital swellings as either reliable-indicators of reproductive quality (reliable-indicator hypothesis) or probabilistic signals of fertility (graded-signal hypothesis). While these morphological signals are mostly confined to catarrhine primates, these hypotheses are potentially widely applicable across primates, but have not been tested in taxa that lack such morphological signals. Here, we tested these hypotheses in wild black capuchins (Sapajus nigritus), a species in which females lack morphological sexual signals but produce conspicuous behavioral estrous displays. Specifically, we examined the proportion of time different females spent producing these signals with respect to measures of female quality (dominance rank, parity, age-related fecundity and cycle type) and in relation to the timing of fertility, as determined by analysis of fecal progesterone. Time spent displaying did not vary across females based on measures of female quality, but increased with the approach of ovulation. Further, male mating effort varied according to the timing of female fertility. Proceptive behaviors in this species thus meet predictions of the graded-signal hypothesis, providing the first support for this hypothesis based solely on behavioral signals.

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.

Methodological Considerations in the Analysis of Fecal Glucocorticoid Metabolites in Tufted Capuchins (Cebus apella).

Analysis of fecal glucocorticoid (GC) metabolites has recently become the standard method to monitor adrenocortical activity in primates noninvasively. However, given variation in the production, metabolism, and excretion of GCs across species and even between sexes, there are no standard methods that are universally applicable. In particular, it is important to validate assays intended to measure GC production, test extraction and storage procedures, and consider the time course of GC metabolite excretion relative to the production and circulation of the native hormones. This study examines these four methodological aspects of fecal GC metabolite analysis in tufted capuchins (Cebus apella). Specifically, we conducted an adrenocorticotrophic hormone (ACTH) challenge on one male and one female capuchin to test the validity of four GC enzyme immunoassays (EIAs) and document the time course characterizing GC metabolite excretion in this species. In addition, we compare a common field-friendly technique for extracting fecal GC metabolites to an established laboratory extraction methodology and test for effects of storing "field extracts" for up to 1 yr. Results suggest that a corticosterone EIA is most sensitive to changes in GC production, provides reliable measures when extracted according to the field method, and measures GC metabolites which remain highly stable after even 12 mo of storage. Further, the time course of GC metabolite excretion is shorter than that described yet for any primate taxa. These results provide guidelines for studies of GCs in tufted capuchins, and underscore the importance of validating methods for fecal hormone analysis for each species of interest.

Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate.

Seyfarth's model assumes that female primates derive rank-related benefits from higher-ranking females in exchange for grooming. As a consequence, the model predicts females prefer high-ranking females as grooming partners and compete for the opportunity to groom them. Therefore, allogrooming is expected to be directed up the dominance hierarchy and to occur more often between females with adjacent ranks. Although data from Old World primates generally support the model, studies on the relation between grooming and dominance rank in the New World genus Cebus have found conflicting results, showing considerable variability across groups and species. In this study, we investigated the pattern of grooming in wild tufted capuchin females (Cebus apella nigritus) in Iguazú National Park, Argentina by testing both the assumption (i.e., that females gain rank-related return benefits from grooming) and predictions (i.e., that females direct grooming up the dominance hierarchy and the majority of grooming occurs between females with adjacent ranks) of Seyfarth's model. Study subjects were 9 adult females belonging to a single group. Results showed that grooming was given in return for tolerance during naturally occurring feeding, a benefit that higher-ranking females can more easily grant. Female grooming was directed up the hierarchy and was given more often to partners with similar rank. These findings provide supporting evidence for both the assumption and predictions of Seyfarth's model and represent, more generally, the first evidence of reciprocal behavioural interchanges driven by rank-related benefits in New World female primates.

Social relationships between adult females and the alpha male in wild tufted capuchin monkeys.

Primates are notable for the widespread presence of long-term female-male associations which go beyond the mating context. However, little attention has been given to the factors that affect within-species variation in female-male relationships, especially among New World primates. Although detailed accounts of heterosexual relationships in Cebus species are scarce, a few studies have suggested the occurrence of strong associations between adult females and high-ranking males. This study explores affiliative relationships between females and the alpha male during the nonbreeding season in wild tufted capuchin monkeys (Cebus apella nigritus). Affiliative relationships were explored through female-male patterns of spatial proximity and grooming. By adopting a social network approach, we analyzed: (1) whether the alpha male is the preferred male partner for females and, (2) whether variation (if any) in female-alpha male affiliation can be explained through both female individual characteristics and social network metrics. Our results showed that alpha males were the favorite male partner for adult females in the proximity networks, but this did not hold true in the grooming networks. In addition, female-alpha male interaction patterns showed considerable variation, with only some females being strongly associated with the alpha male. Our results suggest that such a variation can be explained by female dominance rank, level of centrality (the quantity and intensity of spatial connection with other females) and prestige (the quantity of grooming received by other females) in female-female social networks. Taken together, these findings highlight two aspects of female-alpha male relationships in tufted capuchin monkeys: the alpha male represents the most socially integrated male in the group, and females with high dominance ranks and high centrality in both proximity and grooming networks show stronger relationships with the alpha male.

Grooming and coalitions in Japanese macaques (Macaca fuscata): partner choice and the time frame reciprocation.

Evidence of a reciprocal exchange of grooming and agonistic support in primates is mixed. In this study, the authors analyzed a large database of grooming and coalitions in captive female Japanese macaques (Macaca fuscata) to investigate their within-group distribution and temporal relations. Macaques groomed preferentially those individuals that groomed them most and supported preferentially those individuals that supported them most. They also supported preferentially those individuals that groomed them most and groomed preferentially those individuals that supported them most. These results were not explained by covariation of grooming and support with third variables such as kinship, rank, or time spent in proximity. However, receiving grooming did not increase the short-term probability of supporting a partner, and being supported did not increase the short-term probability of grooming a partner. The proximate mechanisms underlying the exchange of services were discussed in relation to the time frame of the behavioral choices made by the monkeys.