Phylogeography, genetic diversity, and intraspecific genetic structure of the black-horned capuchin (Sapajus nigritus).

Recent molecular studies have clarified the overarching taxonomy of capuchin monkeys, but intraspecific genetic diversity remains unexplored for most capuchin species. One example is Sapajus nigritus, the southernmost capuchin monkey, found in Brazil and Argentina; its phenotypic diversity has been recognized as two geographic subspecies, but the intraspecific genetic structure of this taxon is poorly known. Here, we sampled across most of this species' geographic distribution, producing a newly sequenced data set for genetic analyses that included 78 individuals from 14 populations. We investigated the intraspecific diversity, genetic structure, and evolutionary history using three mitochondrial markers. Our results indicated that S. nigritus populations exhibited high levels of genetic structure. We found strong support for two monophyletic clades within this species with a deep phylogenetic split, and clear separation from other related taxa. Vicariance events seem to have played a prevalent role in shaping S. nigritus genetic differentiation. The Paraíba do Sul River may have driven the deep divergence between southern and northern clades, whereas the Tietê River may have had a weaker, more recent effect on the divergence of populations within the southern clade.

Identification of Leishmania infantum and Leishmania braziliensis in captive primates from a zoo in Brazil.

Wild nonhuman primates (NHP) are considered natural hosts of a protozoan parasite from the genus Leishmania, the etiological agent of leishmaniasis. It is important to study the population of this infectious agent in zoo animals to establish surveillance and control mechanisms in Sorocaba through the application of a One Health approach, this is where human-animal-environment health and disease interface and can aid in the protection of endangered species. This study aimed to identify Leishmania infantum and Leishmania braziliensis in NHP living in a city where leishmaniasis is endemic. DNA was extracted from 48 NHP and analyzed using polymerase chain reaction primers that are specific for the species L. infantum and L. braziliensis. The results of our research revealed the first report of L. infantum and L. braziliensis naturally infecting primates at Sorocaba zoo. One primate from the species Plecturocebus vieirai was positive for L. infantum and five primates (four Alouatta caraya and one Ateles chamek) were positive for L. braziliensis. This indicates a possible role of these animals on the maintenance of these parasites.

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.

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.

Males follow females during fissioning of a group of northern muriquis.

Although well documented in matrilocal primate species, group fission is still a poorly known phenomenon among patrilocal primates. In this paper we describe in detail a group fission event in the population of northern muriquis at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala in Caratinga, Minas Gerais, Brazil, using Social Network Analyses (SNA). Data on association patterns were collected during systematic observations from May 2002 to September 2005, and analyzed for dry (from May to October) and rainy seasons (from November to April). The fission process started with subgroup formation in the rainy season 2002-2003, and was completed by the dry season of 2003. By the dry season 2003, the parent group (Jaó) had fissioned to form a second mixed-sex group (Nadir) while a subgroup of males (MU) moved between the parent group and the newly established group. Before the Jaó group fission started (dry season 2002) and during its initial phases (rainy season 2002-2003), females that ultimately composed the daughter group (Nadir) were the most peripheral in the association network. In the rainy season 2002-2003, the median monthly (N=6) operational sex ratio (OSR) of Jaó group was 2.81. However, once Jaó females initiated the fissioning process to establish the Nadir group, the OSR was more favorable to males in the Nadir group than in the Jaó group. Our results suggest that males followed the females to escape an unfavorable OSR in their natal group.

Dispersão e estrutura social de macacos-prego (Sapajus nigritus) do Parque Estadual Carlos Botelho, São Paulo / Dispersal and social structure in black capuchin monkeys (Sapajus nigritus) of Carlos Botelho State Park, São Paulo

Padrões de assimetria sexual na dispersão e relações de parentesco são fatores intimamente relacionados e considerados fundamentais para a compreensão da estrutura social dos primatas. Apesar da relevância desses dois assuntos, pouco se sabe sobre como eles afetam o comportamento individual e a estrutura social nos primatas neotropicais. Assim, essa pesquisa teve como objetivos: determinar o padrão de dispersão de uma população selvagem de macacosprego (Sapajus nigritus) por meio de análises genéticas e examinar o efeito do parentesco sobre a estrutura social dos grupos de S. nigritus. Esta pesquisa foi realizada no Parque Estadual Carlos Botelho, localizado no município de São Miguel Arcanjo/SP. Todo material genético foi obtido através de amostras fecais dos indivíduos adultos e subadultos de três grupos sociais. Após a extração do DNA, parte dele foi amplificada através da técnica da Reação em Cadeia da Polimerase. Para as análises genéticas utilizamos marcadores moleculares do tipo microssatélites. Os métodos de amostragem por varredura instantânea e ad libitum foram utilizados para o registro do comportamento dos indivíduos adultos de dois grupos. Os dados genéticos obtidos nesta tese indicaram que ambos os sexos dispersam, pois: 1) o grau de parentesco intragupo entre machos não diferiu do grau de parentesco entre fêmeas, 2) não houve diferenciação genética ao analisar a distribuição das frêquencias alélicas de machos e de fêmeas, e 3) não houve diferença entre machos e fêmeas quanto à probabilidade de terem nascido dentro dos grupos sociais nos quais foram amostrados. Os resultados de associações espaciais e interações sociais indicaram que as fêmeas adultas não formam fortes relações sociais entre si, sendo pouco afiliativas. Os machos adultos estabelecem fracas relações sociais, que podem ser classificadas como tolerantes e caracterizadas pela ausência de catação e pela baixa frequência de interações agonísticas.(AU)

Sex-biased dispersal patterns and kinship are related factors extremely important to understand the social structure of primates. In spite of their importance, little is known about how these factors affect individual behavior and the social structure of neotropical primates. Therefore, the aims of this research were: to determine the dispersal pattern of a wild population of black capuchin monkeys (Sapajus nigritus) through genetic analyses, and to verify the effect of kinship on the social structure of groups of S. nigritus. This research was conducted at Carlos Botelho State Park, in the municipality of São Miguel Arcanjo/SP. We used DNA from fecal samples of adult and subadult members from three wild social groups. DNA was amplified by Polymerase Chain Reaction and microsatellite molecular markers were used. Behavioral data were collected systematically for two groups, and we used scan sampling and ad libitum methods to record the behavior of adults. Genetic data indicated that both sexes disperse from their natal groups, since: 1) relatedness between males was not statistically different from relatedness between females, 2) there was no difference between males and females in population genetic differentiation, and 3) there was no difference between males and females in the probability of being born in the group from which they were sampled. The results of the spatial association and social interactions analysis indicate that females are little affiliative and do not form strong relationships among themselves. Adult males established weak relationships, being classified as tolerant, and characterized by no grooming interactions and by low frequency of agonism.(AU)

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.

Comportamento social de machos adultos de muriquis-do-norte (Brachyteles hypoxanthus) num grupo misto e numa unidade de machos, na estação biológica de Caratinga, MG / Social behaviour of adult male northern muriquis (Brachyteles hypoxanthus) in heterosexual and all male group, at the Estação Biológica de Caratinga, MG

Muriquis-do-norte (Brachyteles hypoxanthus) são caracterizados pela filopatria entre os machos, a formação de grupos multi-macho/multi-fêmea e um sistema de acasalamento poligâmico, com alto grau de promiscuidade. No entanto, alterações ambientais (ecológicas ou demográficas) podem conduzir a modificações no sistema social (seja na estrutura social, organização social ou sistema de acasalamento) considerado como o típico da espécie. A formação de um grupo composto somente por machos (denominado UM), que se associa constantemente com um grupo misto, ou seja, multi-macho/multi-fêmea (denominado grupo Nadir), e a transferência de machos entre grupos distintos, são padrões comportamentais não descritos para os muriquis-do-norte da Estação Biológica de Caratinga, MG. Assim, esta pesquisa teve como objetivos: 1) analisar as interações sociais entre os machos da UM com os machos adultos do grupo Nadir, 2) comparar o comportamento dos machos UM com o comportamento dos machos adultos do grupo Nadir, e 3) analisar as relações sociais entre os machos adultos do grupo Nadir. Dezessete machos adultos foram alvo desta pesquisa, 8 indivíduos da UM e 9 do grupo Nadir. Os machos adultos do grupo Nadir foram divididos em: imigrantes (machos que se transferiram da UM para o grupo Nadir, 4 indivíduos), e residentes (machos fundaram o grupo Nadir, 5 indivíduos). Interações afiliativas, dinâmica espacial e vizinhos em diferentes categorias de distância espacial foram registrados pelo método animal focal. O método de todas as ocorrências foi empregado para o registro de cópulas e interações agonísticas. Os resultados demonstraram que apesar dos machos UM se associarem com o grupo Nadir, sendo constantemente observados na periferia ou até mesmo dentro do grupo, as interações sociais entre os machos UM e GN não se caracterizaram como relações sociais de indivíduos pertencentes ao mesmo grupo (...)

Comportamento social de machos adultos de muriquis-do-norte (Brachyteles hypoxanthus) num grupo misto e numa unidade de machos, na estação biológica de Caratinga, MG

Muriquis-do-norte (Brachyteles hypoxanthus) são caracterizados pela filopatria entre os machos, a formação de grupos multi-macho/multi-fêmea e um sistema de acasalamento poligâmico, com alto grau de promiscuidade. No entanto, alterações ambientais (ecológicas ou demográficas) podem conduzir a modificações no sistema social (seja na estrutura social, organização social ou sistema de acasalamento) considerado como o típico da espécie. A formação de um grupo composto somente por machos (denominado UM), que se associa constantemente com um grupo misto, ou seja, multi-macho/multi-fêmea (denominado grupo Nadir), e a transferência de machos entre grupos distintos, são padrões comportamentais não descritos para os muriquis-do-norte da Estação Biológica de Caratinga, MG. Assim, esta pesquisa teve como objetivos: 1) analisar as interações sociais entre os machos da UM com os machos adultos do grupo Nadir, 2) comparar o comportamento dos machos UM com o comportamento dos machos adultos do grupo Nadir, e 3) analisar as relações sociais entre os machos adultos do grupo Nadir. (...)

... Dezessete machos adultos foram alvo desta pesquisa, 8 indivíduos da UM e 9 do grupo Nadir. Os machos adultos do grupo Nadir foram divididos em: imigrantes (machos que se transferiram da UM para o grupo Nadir, 4 indivíduos), e residentes (machos fundaram o grupo Nadir, 5 indivíduos). Interações afiliativas, dinâmica espacial e vizinhos em diferentes categorias de distância espacial foram registrados pelo método animal focal. O método de todas as ocorrências foi empregado para o registro de cópulas e interações agonísticas. Os resultados demonstraram que apesar dos machos UM se associarem com o grupo Nadir, sendo constantemente observados na periferia ou até mesmo dentro do grupo, as interações sociais entre os machos UM e GN não se caracterizaram como relações sociais de indivíduos pertencentes ao mesmo grupo. Entretanto, as interações sociais dos machos UM com os machos GN não apresentaram um padrão homogêneo, sendo as interações com os imigrantes diferenciadas das interações com os residentes. Ao comparar o comportamento dos machos UM e GN, houve diferença significativa somente no padrão de associação espacial. A análise dos dados referente às relações sociais dos machos GN revelou uma assimetria, pois os imigrantes formaram associações mais fortes com os residentes do que entre si e foram os responsáveis pela manutenção de proximidade e interações afiliativas com os residentes. A tolerância entre os machos UM e machos GN, principalmente dos imigrantes, foi explicada pela familiaridade entre eles. Em relação às relações sociais entre os machos GN, inferi um status social diferenciado entre imigrantes e residentes, devido à maior atratividade que os residentes exerceram sobre os imigrantes. A capacidade de se adaptar a condições demográficas específicas, variando sua organização e estrutura social, evidencia a flexibilidade

Northern muriquis (Brachyteles hypoxanthus) are characterized by male philopatry, by multi-male/multi-female groups and by a polygamous mating system, with high levels of promiscuity. Nevertheless, environmental changes (ecological or demographic) can lead to changes in the social system (in the social structure, as well as in the social organization, or in the mating system) considered as typical of the species. Behavioural patterns such as the formation of an all male group (called UM), constantly associated with a multi-male/multi-female group (called Nadir group), and the transfer of males between distinct groups, are not described yet for northern muriquis of the Estação Biológica de Caratinga, MG. Therefore, the aims of this research were: 1) to analyse the social interactions between the UM males and the adult males of the Nadir group, 2) to compare the behaviour of UM males and the behaviour of adult males of the Nadir group, and 3) to analyse the social relationships among the adult males of the Nadir group. Seventeen adult males were the subjects of this research, 8 individuals belonged to the UM and 9 belonged to the Nadir group. The adult males of Nadir group were separeted into: immigrant (males that transfer from UM to Nadir group, 4 individuals), and resident (males that founded the Nadir group, 5 individuals). Afilliative interactions, spacial dynamics and neighbours at different categories of spacial distances were registered by focal animal sampling. (...)

... The all occurrences sampling was used to record episodes of copulation and agonistic interactions. The results indicated that the social interactions between UM e GN males did not characterize social relationships between members of the same group, even though the UM males associated with the Nadir group, being often observed at the border or even inside the group. The interactions between males of the two groups did not obey a unique pattern. The interactions with immigrant males were different from those with resident males. The comparison between the UM and GN male behaviour revealed significant differences only in the pattern of spatial association. The analysis of GN males social relationships revealed an asymmetry, because the immigrants had stronger associations with residents than among themselves and were the responsible for approaching and for mantaining afilliative interactions with residents. GN males, particularly immigrants, were tolerant towards UM males, probably due to the familiarity among them. Regarding the social relationships among GN males, it was possible to distinguish the social status between immigrants and residents, since resident males were highly attractive to the immigrant males. The adaptive capacity to adjust to specific demographyc conditions, trough changes in the social organization and structure, highlights the behavioural flexibility of the species