Mapping nut-cracking in a new population of wild capuchin monkeys (Sapajus libidinosus) at Ubajara National Park, Brazil.

Populations of bearded capuchin monkeys (Sapajus libidinosus) vary in their tool use behaviors, with some of this divergence regarded as culturally determined. The use of stone tools, primarily to crack open encased foods, is widespread among bearded capuchins living in dry habitats (Caatinga and Cerrado). Significant diversity in targets, processed foods, material, and size of tools is observed across populations. However, so far, only a few sites have been systematically studied, and we are still distant from a representative picture of the range of variation in capuchins' culture. In this study, we did a systematic assessment of stone tool use sites in the Ubajara National Park (UNP), in the Caatinga region of Ceará, Brazil, recording and measuring stone tools, processed foods, and available lithic resources as part of an extensive comparative research, the CapCult project. We found indirect and direct evidence that capuchin monkeys at UNP customarily use hammerstones and anvils to process at least two species of palm nuts, macauba (Acrocomia aculeata) and the harder babaçu (Attalea speciosa). Most of the anvils were rock surfaces and had leftovers of only one palm nut species. The hammerstones used to process both palm nuts were not significantly different in weight, although the ones used for Ac. aculeata were longer. We found a higher frequency of nut-cracking sites in the drier lowland area of the park, reflecting differences in the density of the most common palm species, Ac. aculeata, and availability of raw stone material. The stone tool use observed in UNP is within the scope of previously reported in savannah capuchin populations. Our study widens the knowledge of stone tool-use diversity in wild capuchin monkeys, which could contribute to shaping conservation policy, including cultural traits.

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.

Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus.

Socioecological models assume that primates adapt their social behavior to ecological conditions, and predict that food availability and distribution, predation risk and risk of infanticide by males affect patterns of social organization, social structure and mating system of primates. However, adaptability and variation of social behavior may be constrained by conservative adaptations and by phylogenetic inertia. The comparative study of closely related species can help to identify the relative contribution of ecological and of genetic determinants to primate social systems. We compared ecological features and social behavior of two species of the genus Sapajus, S. nigritus in Carlos Botelho State Park, an area of Atlantic Forest in São Paulo state, and S. libidinosus in Fazenda Boa Vista, a semi-arid habitat in Piauí state, Brazil. S. libidinosus perceived higher predation risk and fed on clumped, high quality, and usurpable resources (fruits) all year round, whereas S. nigritus perceived lower predation risk and relied on evenly distributed, low-quality food sources (leaves) during periods of fruit shortage. As predicted by socioecology models, S. libidinosus females were philopatric and established linear and stable dominance hierarchies, coalitions, and grooming relationships. S. nigritus females competed less often, and could transfer between groups, which might explain the lack of coalitions and grooming bonds among them. Both populations presented similar group size and composition and the same polygynous mating system. The species differed from each other in accordance with differences in the characteristics of their main food sources, as predicted by socioecological models, suggesting that phylogenetic inertia does not constrain social relationships established among female Sapajus. The similarity in mating systems indicates that this element of the social system is not affected by ecological variables and thus, is a more conservative behavioral feature of the genus Sapajus.

Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus.

The frequency of anointing bouts and the materials used for self- and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self-medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli.

Stone tools differences across three capuchin monkey populations: food's physical properties, ecology, and culture.

Robust capuchin monkeys (Sapajus) are known for processing mechanically challenging foods, having morphological adaptations to do so. However, several populations go beyond body limitations by using stone tools to expand their food range. Those populations use stones in a variety of ways, goals, and with different frequencies. Stone tool size correlates with the food's resistance within some populations. However, we have no detailed comparisons to identify if this correlation is the same across populations. This study described and compared stone raw material availability, food's physical properties (hardness and elasticity), and stone tool weight in three populations of bearded capuchin monkeys (Sapajus libidinosus), including a newly described site (Chapada dos Veadeiros National Park, CVNP). The differences we observed regarding stone tool weight selection among sites were not correlated to the food's physical properties we analyzed. Lithic resource availability could partly explain some differences in the stone tools used. However, the tool weight differences are larger than the raw material variance across sites, meaning some distinctions are possible behavioral traditions, such as the same fruit (Hymenaea) being processed with bigger than needed tools in CVNP than in the other two sites. Capuchin monkey behavioral variability in stone tool use can be caused by several interacting factors, from ecological to cultural.

Female emancipation in a male dominant, sexually dimorphic primate under natural conditions.

In most group-living animals, a dominance hierarchy reduces the costs of competition for limited resources. Dominance ranks may reflect prior attributes, such as body size, related to fighting ability or reflect the history of self-reinforcing effects of winning and losing a conflict (the winner-loser effect), or both. As to prior attributes, in sexually dimorphic species, where males are larger than females, males are assumed to be dominant over females. As to the winner-loser effect, the computational model DomWorld has shown that despite the female's lower initial fighting ability, females achieve some degree of dominance of females over males. In the model, this degree of female dominance increases with the proportion of males in a group. This increase was supposed to emerge from the higher fraction of fights of males among themselves. These correlations were confirmed in despotic macaques, vervet monkeys, and in humans. Here, we first investigate this hypothesis in DomWorld and next in long-term data of 9,300 observation hours on six wild groups of robust capuchin monkeys (Sapajus libidinosus; S. nigritus, and S. xanthosternos) in three Brazilian sites. We test whether both the proportion of males and degree of female dominance over males are indeed associated with a higher relative frequency of aggression among males and a higher relative frequency of aggression of females to males. We confirm these correlations in DomWorld. Next, we confirm in empirical data of capuchin monkeys that with the proportion of males in the group there is indeed an increase in female dominance over males, and in the relative frequency of both male-male aggression and aggression of females to males and that the female dominance index is significantly positively associated with male male aggression. Our results reveal that adult sex ratio influences the power relation between the sexes beyond predictions from socioecological models.

Wild robust capuchin monkey interactions with sympatric primates.

Examining interactions among sympatric primate species can provide interesting information about competition, cooperation, and avoidance between those species. Those interactions can be neutral, positive, or negative for the species involved. Capuchin monkeys are medium-sized primates that can encounter both larger and smaller primates in their varied habitats. Gracile capuchins (Cebus) are reported to present different types of interactions with other primates. Interactions with howler monkeys frequently include physical aggression, while interactions with spider monkeys are mostly threats and chases. Moreover, interaction types are not consistent across populations. Among robust capuchins (Sapajus spp.), however, no reports have been published. Here we describe and classify encounters of Sapajus libidinosus and S. nigritus with Alouatta caraya, A. guariba, Brachyteles arachnoides, and Callithrix jacchus in three sites in the environments of Cerrado, Caatinga (savannah-like), and Atlantic forest, and compare the interaction patterns among sites and different group sizes. The latter is a factor that can influence the outcome, and we expected capuchins in larger groups to be more aggressive toward other primates. Our results of 8421 h of total contact with the capuchin groups show that, indeed, capuchins in sites with larger groups presented aggressive interactions with higher frequency. However, the other species' body size also seems important as smaller primates apparently avoided capuchins, and interactions with the larger muriquis were mostly neutral for the capuchin. Capuchins showed neutral or aggressive behaviors toward howler monkeys, with differences between the rainforest and savannah groups. We found that robust capuchins can present aggressive interactions even to primates larger than themselves and that aggressive behavior was the most common response in populations living in larger groups and drier environments.

Fallback foraging as a way of life: using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation.

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly "specialized" taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods.

Food or threat? Wild capuchin monkeys (Sapajus libidinosus) as both predators and prey of snakes.

Snakes present a hazard to primates, both as active predators and by defensive envenomation. This risk might have been a selective pressure on the evolution of primate visual and cognitive systems, leading to several behavioral traits present in human and non-human primates, such as the ability to quickly learn to fear snakes. Primates seldom prey on snakes, and humans are one of the few primate species that do. We report here another case, the wild capuchin monkey (Sapajus libidinosus), which preys on snakes. We hypothesized that capuchin monkeys, due to their behavioral plasticity, and cognitive and visual skills, would be capable of discriminating dangerous and non-dangerous snakes and behave accordingly. We recorded the behavioral patterns exhibited toward snakes in two populations of S. libidinosus living 320 km apart in Piauí, Brazil. As expected, capuchins have a fear reaction to dangerous snakes (usually venomous or constricting snakes), presenting mobbing behavior toward them. In contrast, they hunt and consume non-dangerous snakes without presenting the fear response. Our findings support the tested hypothesis that S. libidinosus are capable of differentiating snakes by level of danger: on the one hand they protect themselves from dangerous snakes, on the other hand they take opportunities to prey on non-dangerous snakes. Since capuchins and humans are both predators and prey of snakes, further studies of this complex relationship may shed light on the evolution of these traits in the human lineage.

Repellent efficacy of formic acid and the abdominal secretion of carpenter ants (Hymenoptera: Formicidae) against Amblyomma ticks (Acari: Ixodidae).

Formic acid is a substance produced by some ants for defense, trail marking, and recruitment. Some animals are known to rub ants or other arthropods on parts of their plumage or fur to anoint themselves with released substances. A recent study with a semifree-ranging group of capuchin monkeys, Cebus apella L., in the Tietê Ecological Park, Sao Paulo, Brazil, an area of occurrence of the tick species Amblyomma cajennense (F.), revealed that "anting" with carpenter ants, Camponotus rufipes F. (Hymenoptera: Formicidae), occurs frequently, especially during the A. cajennense subadult season. Based on these observations, we tested the repellent effect of the formic acid and the ants themselves against A. cajennense and Amblyomma incisum Neumann nymphs, and Amblyomma parcum Aragdo adult ticks in the laboratory. The results revealed a significant repellent effect of formic acid and ant secretion, and a significant duration of the repellent effect. The results suggest that the anting behavior of capuchin monkeys, and other vertebrates, may be related with repellence of ticks and other ectoparasites.

Predatory threat of harpy eagles for yellow-breasted capuchin monkeys in the Atlantic Forest.

We describe seven encounters between different harpy eagle individuals (Harpia harpyja) and a group of yellow-breasted capuchin monkeys (Sapajus xanthosternos) in Una Biological Reserve. These interactions lasted 58 min on average. In each of those encounters, the capuchin monkeys used particular behavioral strategies against the harpy eagle that were not employed in reaction to other aerial predators. We did not observe any successful predation events, but after one of those encounters an infant disappeared from the capuchin group. As a whole, these observations indicate that the presence of harpy eagles in the group's home range increases predation risk for capuchin monkeys. The present report also suggests a reoccupation by H. harpyja of this area, as no previous recent records identify harpy eagle occurrence in Una Biological Reserve.

Emotional and sexual jealousy as a function of sex and sexual orientation in a Brazilian sample.

The goal of the present study was to compare the relative distress of homosexual and heterosexual Brazilian men and women on scenarios in which they imagined their partners sexually or emotionally involved with another person, using a forced-choice paradigm and continuous measures. Participants were 68 heterosexual men, 72 heterosexual women, 42 homosexual men, and 35 homosexual women. On the forced-choice questions heterosexual men (39 on one question and 37 on the other) were more upset than their female counterparts (21 on one question and 15 on the other) by scenarios of sexual infidelity than those of emotional infidelity. On questions using continuous measures no significant difference was found between pleasurable sex and attachment scenarios for heterosexual women or heterosexual men. On the highly upsetting scenarios heterosexual men discriminated between flirting and both pleasurable sex and attachment scenarios, being less disturbed by the former. In contrast, heterosexual women were equally distressed by the three scenarios. Scores for the homosexual men and homosexual women fell in between those of the heterosexual men and heterosexual women and did not show a clear cut preference for the sexual infidelity or the emotional alternative on the forced-choice paradigm. However, on the continuous measures of jealousy homosexuals resembled heterosexuals of the opposite sex. There was no evidence that jealousy would be less intense among homosexuals although reproductive outcomes were not at risk.

Estilos de cuidado materno em primatas: considerações a partir de uma espécie do Novo Mundo / Styles de soins maternels dans les primates: considerations d'une espèce du Nouveau Monde / Estilos de cuidado materno en primates: consideraciones a partir de una especie del Nuevo Mundo / Maternal care styles in primates: considering a New World species

Resumo Quando buscamos entender o comportamento humano, comparações com primatas não humanos são especialmente relevantes para identificar homoplasias (características semelhantes que evoluem independentemente em diferentes espécies). Neste artigo, apresentamos um estudo longitudinal de dois anos sobre o comportamento materno de macacos-prego (Sapajus spp.) em condições naturalísticas. Nossos resultados permitiram identificar estilos de cuidado distintos dentro de um contínuo de permissividade a proteção. O desenvolvimento observado do vínculo entre mães e filhotes sugere que o período de dependência de filhotes de macaco-prego envolve, além de processos de maturação física, o estabelecimento e desenvolvimento de processos psicológicos associados ao sistema de apego. É possível que a variabilidade de estilos maternos resultante da combinação de características de mães, filhotes e contextos socioecológicos, aliada ao prolongamento do vínculo de apego, pavimente caminhos para diferentes trajetórias de desenvolvimento. Como em humanos, esse pode ser um dos mecanismos pelos quais surgem e se consolidam as diferenças interindividuais nas populações adultas.

Résumé Lorsque nous cherchons à comprendre le comportement humain, les comparaisons avec les primates non humains sont particulièrement pertinentes pour identifier les homoplasies (caractéristiques similaires qui évoluent indépendamment dans différentes espèces). Dans cet article, nous présentons les résultats d'une étude longitudinale de deux ans sur le comportement maternel du Sapajou capucin (Sapajus spp.) dans des conditions naturelles. Nos résultats nous ont permis d'identifier différents styles de soins maternels dans un continuum de permissivité à la protection. Nous avons observé que le modèle de lien d'attachement entre la mère et la progéniture suggère que la période de dépendance des bébés singes implique, en plus des processus de maturation physique, l'établissement et le développement de processus psychologiques associés au système d'attachement. Il est possible que la variabilité des styles maternels résultant de la combinaison des caractéristiques de la mère, de la progéniture et du contexte socioécologique, ainsi que l'extension du lien d'attachement, ouvrent la voie à différentes trajectoires de développement. Comme les humains, il peut être un des mécanismes par lequel les différences interindividuelles apparaissent et se consolident au sein des populations adultes.

Resumen Cuando buscamos entender el comportamiento humano, comparaciones con primates no humanos son especialmente relevantes para identificar homoplasias (características similares que evolucionan independientemente en diferentes especies). En este artículo, presentamos los resultados de un estudio longitudinal de dos años sobre el comportamiento materno de monos capuchinos (Sapajus spp.) en condiciones naturales. Los resultados permitieron identificar estilos de cuidado materno distintos dentro de un continuo de permisividad a la protección. Se observó que el patrón de desarrollo del vínculo de apego entre madre y cría sugiere que el período de dependencia de la cría de monos capuchinos involucra, además de procesos de maduración física, el establecimiento y desarrollo de procesos psicológicos asociados al sistema de apego. Es posible que la variabilidad de estilos maternos resultante de la combinación de características de madres, crías y contextos socioecológicos, aliada a la prolongación del vínculo de apego, establezca caminos para diferentes trayectorias de desarrollo. Tal como en humanos, este puede ser uno de los mecanismos por los que surgen y se consolidan las diferencias interindividuales en las poblaciones adultas.

Abstract When aiming understand the human behavior, comparisons with nonhuman primates are especially relevant to identify homoplasies (similar characteristics that evolve independently in different species). In this paper, we present a two-year longitudinal study on the maternal behavior of capuchin monkeys (Sapajus spp.) under naturalistic conditions. Our results revel distinct maternal care styles within a continuum ranging from permissiveness (laissez-faire) to protectiveness. The observed development of mothers and infants bond suggests that the dependence period of capuchin monkeys infants involves, in addition to physical maturation processes, the establishment and development of psychological processes associated with the attachment system. It is possible that the variability of maternal styles - resulting from the combination of mothers' and infants' characteristics, as well as socioecological contexts, along with the extension of the attachment bond - are responsible for paving the way for different developmental trajectories. This may be one of the mechanisms underlying interindividual differences arise in adult populations, as seen in humans.

Cross-genus adoption of a marmoset (Callithrix jacchus) by wild capuchin monkeys (Cebus libidinosus): case report.

We report a case of interspecies adoption of an infant marmoset (Callithrix jacchus) by wild capuchin monkeys (Cebus libidinosus). The marmoset was an infant when it was first observed in the capuchin group on 3 March 2004. Since it first appeared it has been observed informally and frequently. In January 2005 systematic observations were made of the marmoset and a capuchin of similar age. Throughout its period of adoption the marmoset appeared to be socially integrated into the group, benefiting from nurturant behaviors exhibited by two successive adoptive "mothers" and pronounced tolerance from all members of the group. This case highlights the flexibility of both Callithrix and Cebus in accommodating variable social behaviors and other characteristics (including size) of social partners.