The Vocal Repertoire of the Bearded Capuchin (Cebidae: Sapajus libidinosus): Implications for Understanding the Complexity of Neotropical Primate Communication.

Vocal communication is an essential aspect of primate social behaviour. The bearded capuchin Sapajus libidinosus is endemic to Brazil, and some studies have described specific vocalisation types for this species; however, there is still no complete description of its vocal repertoire. Thus, this study aimed to describe the vocal repertoire of a group of S. libidinosus living in theParque Nacional de Brasília, a protected area in the Cerrado area of Central Brazil. We carried out focal samplings and recording of vocalisations of members of an S. libidinosus troop in different behavioural contexts. The call analyses revealed 25 different types of vocalisations, and each call presented significant structural variation. We grouped these vocalisations according to the context of the emission or acoustic structure into the following categories: contact calls (contact note, infant babbling, trill, teeth- and lip-smacking, and sirena); foraging calls (chihui, grgr, and patinado); whistle series (food-associated, long-distance, and intergroup encounter); aggressive calls (aggressive contact note, ascending rapid staccato, cough cough, and pip); calls in response to aggression (scream, squeal, and pulsed scream), sexual display calls (chuck and raspy oestrous call), and stress-related calls (alarm call/bark, hiccup, hip, double hip, and wah wah). S. libidinosus presented a very rich vocal repertoire, revealing a pattern consistent with the repertoire of other capuchin monkey species. This is the first comprehensive description of the S. libidinosus vocal repertoire and highlights the complexity of neotropical primate communication.

Non-human primate token use shows possibilities but also limitations for establishing a form of currency.

Non-human primates evaluate choices based on quantitative information and subjective valuation of options. Non-human primates can learn to value tokens as placeholders for primary rewards (such as food). With those tokens established as a potential form of 'currency', it is then possible to examine how they respond to opportunities to earn and use tokens in ways such as accumulating tokens or exchanging tokens with each other or with human experimenters to gain primary rewards. Sometimes, individuals make efficient and beneficial choices to obtain tokens and then exchange them at the right moments to gain optimal reward. Sometimes, they even accumulate such rewards through extended delay of gratification, or through other exchange-based interactions. Thus, non-human primates are capable of associating value to arbitrary tokens that may function as currency-like stimuli, but there also are strong limitations on how non-human primates can integrate such tokens into choice situations or use such tokens to fully 'symbolize' economic decision-making. These limitations are important to acknowledge when considering the evolutionary emergence of currency use in our species. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Optional tool use: The case of wild bearded capuchins (Sapajus libidinosus) cracking cashew nuts by biting or by using percussors.

Tool use in humans can be optional, that is, the same person can use different tools or no tool to achieve a given goal. Strategies to reach the same goal may differ across individuals and cultures and at the intra-individual level. This is the first experimental study at the intra-individual level on the optional use of a tool in wild nonhuman primates. We investigated optional tool use by wild bearded capuchins (Sapajus libidinosus) of Fazenda Boa Vista (FBV; Piauí, Brazil). These monkeys habitually succeed in cracking open the mesocarp of dry cashew nuts (Anacardium spp.) by pounding them with stones and/or by biting. We assessed whether availability of a stone and resistance of the nut affected capuchins' choice to pound or to bite the nuts and their rates of success. Sixteen capuchins (1-16 years) received small and large dry cashew nuts by an anvil together with a stone (Stone condition) or without a stone (No-Stone condition). In the Stone conditions, subjects used it to crack the nut in 89.1% (large nuts) and 90.1% (small nut) of the trials. Nut size significantly affected the number of strikes used to open it. Availability of the stone significantly increased the average percent of success. In the No-Stone conditions, monkeys searched for and used other percussors to crack the nuts in 54% of trials. In all conditions, age affects percentage of success and number of strikes to reach success. We argue that exclusive use of stones in other sites may be due to the higher abundance of stones at these sites compared with FBV. Since capuchins opened cashews with a tool 1-2 years earlier than they succeed at cracking more resistant palm nuts, we suggest that success at opening cashew nuts with percussors may support the monkeys' persistent efforts to crack palm nuts.

Against all odds: Numerical assessment by tufted capuchin monkeys.

When competitors are able to assess the asymmetry in the resource holding potential before interacting, individuals or groups should avoid interacting with stronger opponents, thereby avoiding the energy costs and risk of injury associated with aggressive intergroup encounters. Thus, escalated aggression is expected only between closely matched competitors. Among Argentine tufted capuchin monkeys (Sapajus nigritus), intergroup dominance is decided by the asymmetry in male group size. Using playback experiments, I simulated intergroup encounters with neighboring groups, manipulating both the apparent numerical asymmetry and the resource context. During experimental trials, I recorded the approach behavior of the focal individual, as well as changes in neighbor density and individual travel speed following the presentation of the playback stimulus, to assess whether individual willingness to participate in resource defense was affected by the probability of winning the encounter. In spite of the competitive disadvantage, neither males nor females showed a decreased probability of approach when the numerical odds strongly favored the opposing group. Instead decisions regarding whether to participate appear to be driven primarily by the resource context. Nevertheless, changes in individual behavior during approaches suggest that tufted capuchin monkeys are sensitive to the relative odds. Individuals accelerated less when approaching a larger group, although no changes in neighbor density were apparent. The absence of an effect of the numerical asymmetry on willingness to approach the playback speaker suggests that subordinate groups benefit from engaging in intergroup aggression with larger neighbors, despite the high probability of losing. These encounters may serve to assess the current subjective resource valuation of the neighboring group or limit territorial expansion by large groups by decreasing the marginal value of home range exclusivity. Because these encounters are riskier, however, individuals appear to alter their approaches, becoming more tentative as the numerical odds increasingly favor the opposing group.

Face-to-face interactions between mothers and female infants in wild bearded capuchin monkeys (Sapajus libidinosus).

Once considered uniquely human, mother-infant face-to-face interactions (FF) were observed in a few captive primates. In these studies, FF were correlated to physical contact suggesting a mechanism mediating proximity between mother and infant, as is the case for humans. We investigated this hypothesis in wild capuchin monkeys (Sapajus libidinosus) during the first year of life of eight female infants. Data were weekly focal-day videos of infants from which we recorded FF with mothers. We expected FF would increase with infants' age (as time in contact with mothers decreased) and would more likely occur in the absence of physical contact between the dyad. There was no effect of age in the proportion of interaction time spent in FF, nor in types of FF. A quarter of FF episodes occurred in the absence of physical contact between the dyad, and in most of them physical contact was resumed following the FF. Contrary to predictions, the stability in the first year, mainly when mothers-female infants were in contact, indicates that FF act primarily promoting opportunities for affective communication and intuitive care. However, we found some supportive evidence for the hypothesis that FF regulate proximity between mother and infant, mainly in resume physical contact.

Small but wise: Common marmosets (Callithrix jacchus) use acoustic signals as cues to avoid interactions with blonde capuchin monkeys (Sapajus flavius).

Vocalizations are often used by animals to communicate and mediate social interactions. Animals may benefit from eavesdropping on calls from other species to avoid predation and thus increase their chances of survival. Here we use both observational and experimental evidence to investigate eavesdropping and how acoustic signals may mediate interactions between two sympatric and endemic primate species (common marmosets and blonde capuchin monkeys) in a fragment of Atlantic Rainforest in Northeastern Brazil. We observed 22 natural vocal encounters between the study species, but no evident visual or physical contact over the study period. These two species seem to use the same area throughout the day, but at different times. We broadcasted alarm and long distance calls to and from both species as well as two control stimuli (i.e., forest background noise and a loud call from an Amazonian primate) in our playback experiments. Common marmosets showed anti-predator behavior (i.e., vigilance and flight) when exposed to blonde capuchin calls both naturally and experimentally. However, blonde capuchin monkeys showed no anti-predator behavior in response to common marmoset calls. Blonde capuchins uttered long distance calls and looked in the direction of the speaker following exposure to their own long distance call, whereas they fled when exposed to their own alarm calls. Both blonde capuchin monkeys and common marmosets showed fear behaviors in response to the loud call from a primate species unknown to them, and showed no apparent response to the forest background noise. Common marmoset responses to blonde capuchin calls suggests that the latter is a potential predator. Furthermore, common marmosets appear to be eavesdropping on calls from blonde capuchin monkeys to avoid potentially costly encounters with them.

Age-related changes in the social behavior of tufted capuchin monkeys.

The effects of aging on the social behavior of nonhuman primates is little understood, especially in New World monkeys. We studied the members of a colony of tufted capuchin monkeys (Sapajus sp.) in order to evaluate age related changes in their social behavior. We conducted observations on 25 subjects aged 4-36 years, living in captive social groups. We found that affiliative interactions (grooming and proximity) decreased with age, and that grooming was increasingly directed to a single preferred partner. Manipulation of objects in the environment also decreased with age, while locomotion and aggression showed no change. Overall, these results concur with previous findings on both human and nonhuman primates, and cast doubts on interpretations of age associated changes in human social behavior that rely of uniquely human advanced cognitive capacities.