Sapajus Libidinosus Research Articles

Inter-group conflicts involving adult female and male bearded capuchins, Sapajus libidinosus (Primates: Cebidae), in the context of provisioned resources: resource defense or sexual selection?

Intergroup conflicts are energetically more costly than intra-group disputes, and thus typically occur in contexts in which the energetic returns are relatively high. In anthropogenic environments, provisioned resources tend to be rich in energy and highly agglomerated. While females are expected to defend provisioned resources, the adult males, in turn, are expected to defend the females. Based on this premise, the present study focused on an urban forest in the city of Goiânia (Goiás, Brazil), which is inhabited by two groups of bearded capuchins. Behavioral data were collected using instantaneous scan sampling and all-events records to document intergroup conflicts and define their context. We used a backward logistic regression and stepwise linear regression to analyze the participation of the individuals in the conflicts. Conflicts were more frequent in the context of provisioning, although the number of neither females nor males involved in the conflict varied significantly between contexts. The females did avoid participating in conflicts involving adult males, however, to minimize the risk of being attacked by them. The adult males participated more in the presence of other adult males, which is partly consistent with the hypothesis of the defense of reproductive partners. The conflicts were not more intense in the context of provisioned resources, which contrasted with expectations. The hierarchical relationship between the two study groups, and the fact that the groups were derived from the same social unit, may have contributed to a reduction in the intensity of the conflicts.

The emergence of collective knowledge and cumulative culture in animals, humans and machines.

The emergence of collective knowledge and cumulative culture in animals, humans and machines.

Minimal age-related variation in bipedal behavior in Sapajus

Our understanding of how bipedalism evolved in hominins has been refined through studies of bipedal behavior in non-human primates, both in the wild and in the laboratory. Bipedal behavior in non-human primates makes up a relatively small portion of their behavioral repertoire. Understanding when bipedal behaviors occur and how bipedal behaviors emerge can provide further insight into the context in which bipedal behaviors may have evolved. Here, we examine age-related variation in bipedal behavior in wild bearded capuchins (Sapajus libidinosus). 2,209 records of bipedal posture and locomotion, activity state, and substrate used during bipedal behavior (17.2% of all records of positional behavior) were examined for individuals ranging from 3 months to 15 years or older in two groups (32 individuals in total). Apart from very young individuals that were carried by older conspecifics, individuals of all ages showed similar rates and patterns of bipedal behaviors. Bipedal postures were used predominantly during feeding and foraging, most often in arboreal settings, and most often with their prehensile tail grasping, or in contact with, the substrate. Bipedal locomotion occurred most often on terrestrial substrates and comprised only 3% of all records of bipedal behavior.

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.

Breeding ecology of Rufous Casiornis Casiornis rufus in south-east Brazil

We present new reproductive information for the Rufous Casiornis Casiornis rufus, based on studies undertaken during 1991–99 and in 2018, in the municipality of Arcos, Minas Gerais, south-east Brazil. We found eight nests, all sited in cavities of dead trees or wooden fence posts, on average 62.8 cm above ground. Clutch size was usually three eggs, pale beige overlain with complex markings throughout, similar to those of the genus Myiarchus. Eggs measured on average 22.8 × 16.96 mm, mass c.3 g. Incubation lasted c.15 days, and nestlings remained in the nest 15–17 days, being fed by both adults, mainly with orthopterans. Three of the eight nests produced young that fledged. One nest was predated by both a Black-striped Capuchin Sapajus libidinosus and a Crane Hawk Geranospiza caerulescens, and another by a Black-tufted Marmoset Callithrix cf. penicillata. Nests were constructed in August, and the last nestlings fledged in late October. Most aspects of the breeding ecology of Casiornis are identical to those of other members of the Myiarchini.

Trypanosoma rangeli Genetic, Mammalian Hosts, and Geographical Diversity from Five Brazilian Biomes.

Trypanosoma rangeli is a generalist hemoflagellate that infects mammals and is transmitted by triatomines around Latin America. Due to its high genetic diversity, it can be classified into two to five lineages. In Brazil, its distribution outside the Amazon region is virtually unknown, and knowledge on the ecology of its lineages and on host species diversity requires further investigation. Here, we analyzed 57 T. rangeli samples obtained from hemocultures and blood clots of 1392 mammals captured in different Brazilian biomes. The samples were subjected to small subunit (SSU) rDNA amplification and sequencing to confirm T. rangeli infection. Phylogenetic inferences and haplotype networks were reconstructed to classify T. rangeli lineages and to infer the genetic diversity of the samples. The results obtained in our study highlighted both the mammalian host range and distribution of T. rangeli in Brazil: infection was observed in five new species (Procyon cancrivorous, Priodontes maximum, Alouatta belzebul, Sapajus libidinosus, and Trinomys dimidiatus), and transmission was observed in the Caatinga biome. The coati (Nasua nasua) and capuchin monkey (S. libidinosus) are the key hosts of T. rangeli. We identified all four T. rangeli lineages previously reported in Brazil (A, B, D, and E) and possibly two new genotypes.

Uses of nonhuman primates by humans in northeastern Brazil.

Humans have used non-human primates (hereafter referred to as primates) as food source, medicine, parts of rituals, pets, and models for various studies worldwide. Here we investigated the extent of the use of primates by humans in three areas in northeastern Brazil, the country's most impoverished region. We carried out our study in three biomes (Caatinga, Cerrado, and Atlantic Forest). The results showed that humans exploited all five primate species occurring in the study sites:Callithrix jacchus,Sapajus flavius,Sapajus libidinosus,Alouatta belzebul, andAlouatta ululata. They used the primates as a food source, as pets and medicines, and for leisure. Despite socioeconomic differences in the study areas, we found similarities in the use of primates. Larger primates were targeted for meat, whereas the small common marmosets were targeted as pets. We found conflicting interactions between humans and bearded capuchins due to crop raiding, but no such conflict was found between humans and blonde capuchins, reflecting the differences in crop type, pattern, and tradition in the sites.A.ululata was used as medicine. We suggest that environmental education actions in the study areas should focus on (i) raising awareness among local people of the ecological importance of primates, (ii) providing alternative activities to hunting whenever possible, and (iii) minimising conflicts.

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.

Bearded capuchin (Sapajus libidinosus) predation on a rock cavy (Kerodon rupestris) followed by prey sharing.

We describe predation on an adult rodent rock cavy and sharing of the carcass by a group of male bearded capuchins. Despite many studies, such an interaction has never been observed in bearded capuchins. Rock cavies are large rodents weighing around 25% of the weight of an adult male bearded capuchin. The capuchins chased, caught, and shared the adult rock cavy. We observed no strong evidence of communication or division of roles in the successful capture, suggesting that the social hunting episode was not necessarily coordinated or collaborative. Instead, the individuals apparently tried to achieve the same goal of capturing the prey simultaneously (i.e., individuals synchronously performed similar actions to achieve the task), with the strongest individual emerging victorious and tolerating prey sharing afterwards. Our observations add to the understanding of cooperative behaviours such as social hunting and food sharing in bearded capuchins.

Male-Directed Object Use by Proceptive Female Bearded Capuchin Monkeys (Sapajus libidinosus) in Captivity

Some nonhuman primates use tools to modify the behavior of other animals in social contexts. For example, during their proceptive periods, female bearded capuchins (Sapajus libidinosus) in two wild groups throw stones and push branches toward males, which may function to draw male attention to the females. To further clarify the social and communicative relevance of this behavior, we recorded all occurrences of object use in a captive group (one adult male and four females) at Brasilia Zoo, during 963 h of observation. Additionally, we recorded the occurrence of typical proceptive behaviors and quantified behavioral changes of the male associated with throwing behavior. All females threw objects, such as stones and sticks, at the male (N = 205 events). One of the females also pounded objects near the male (N = 72). The two forms of object use were associated with female proceptivity. Male-directed throws increased the chances of the male changing his behavior, particularly by shifting his attention to the thrower, supporting the hypothesis that throwing at the male function as a communicative act. However, females also used aimed throwing in affiliative contexts (N = 2) and interactions with humans (N = 102) and other animals (N = 61). Thus, our results show that aimed throwing is a flexible behavior, elicited in multiple social contexts and for different purposes. Moreover, our study demonstrates that considering the effects of object use on the behavior of potential targets can help us to understand how primates use objects to mediate communication.

Microsatellite Markers for Bearded Capuchins (Sapajus libidinosus): Transferability and Characterization.

Natural Sapajus libidinosus populations are in continuous decline due to fragmentation, habitat loss, and the illegal pet trade. They live in Caatinga scrub forests, which already lost over 50% of their original cover. The lack of studies on S. libidinosus population genetics means that we do not know how they are being affected by this striking habitat loss and other anthropogenic disturbances. Polymorphic markers are not available for the study of S. libidinosus diversity and population genetics. Thus, here we aimed to test the transferability of 14 microsatellite markers to S. libidinosus. These microsatellites were previously isolated from Cebus capucinus (white-faced capuchin), species belonging to the same subfamily (Cebinae) as the study species. We found that six of the tested microsatellite markers (tetra-nucleotide) were cross-amplified in our target species. All loci were polymorphic. The number of alleles varied from 4 to 7, and the expected heterozygosity ranged from 0.588 to 0.869. The microsatellite markers transferred to S. libidinosus and characterised in our study will be valuable tools to evaluate the genetic variability of both wild and captive populations. They will considerably reduce the costs of microsatellite isolations, helping to prioritise currently limited research and conservation budgets in Brazil.

Revisiting the fourth dimension of tool use: how objects become tools for capuchin monkeys.

Culture allows humans to adapt to a diversity of contexts. Participatory experience in technical activities and activity with artefacts provide the basis for learning traditional technical skills. Some populations of non-human animals use tools. The ways in which artefacts influence the development of a traditional skill in non-human species can provide insight into essential supports for technical traditions in humans and shared learning processes across species. In wild bearded capuchins, nut cracking leaves edible pieces of nuts, nut shells and stones used as hammers at anvil sites. We addressed how mastery of cracking nuts by young monkeys is associated with interactions with these objects. We studied monkeys' reuse of nuts, hammers and anvils and the outcome of attempts to crack nuts, and from these data derived their behavioural variability and proficiency in nut cracking. Behavioural variability was the most robust predictor of whether a monkey collects pieces of nuts cracked by others or reuses stones and nuts, and was a stronger predictor of proficiency than age. Young monkeys were increasingly likely to reuse the stone used by another after the other monkey had left the anvil as they increasingly focused their behaviour on actions relevant to cracking nuts.

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.

Ingestive behaviors in bearded capuchins (Sapajus libidinosus)

The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form–function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.

Assessment of the technique of the anesthetic block of the Brachial Plexus by Supraclavicular approach in Sapajus libidinosus (SPIX, 1823).

The aim of study was to evaluate the efficacy of the supraclavicular brachial plexus block technique in Sapajus libidinosus. Were used eight animals, which were sedated, anesthetized, kept under hypnosis, and submitted to plexus block using a neurolocalizer. The physiological parameters, the nociception and response threshold (mA), were evaluated before and after the block. The response to electrical stimulation and cutaneous sensitivity were evaluated. The groups were compared by the Tukey or Friedman test at 5%. The technique promoted blockage of the plexus, and movement of the thoracic limb in response to electrical stimulation decreased after 10minutes. The applied milliampere increased after 5minutes. The cutaneous sensitivity reflex decreased. The average time of return of spontaneous limb movement exceeded 50minutes. The use of 5mg/kg of lidocaine 2% promoted loss of cutaneous sensitivity and limb muscle relaxation during the evaluation period.

Morfologia do tubo digestório de Alouatta belzebul

O Alouatta belzebul é uma espécie classificada como “Vulnerável” e isso se justifica principalmente pela caça, fragmentação e perda do hábitat nas florestas tropicais. A anatomia deste gênero apresenta características peculiares em todas as espécies estudadas, assim este trabalho objetivou descrever a morfologia do tubo digestório de Alouatta belzebul a fim de fornecer subsídios para avaliação de dietas, realização de procedimentos clínicos e cirúrgicos nestes animais. Foram utilizados 10 espécimes de Alouatta belzebul, adultos, machos, de diferentes idade. O trabalho foi realizado na Universidade Federal de Goiás e aprovado no comitê de ética N.083∕17. Os animais previamente criopreservados, foram descongelados e fixados por meio da infusão intramuscular e intracavitária de solução aquosa de folmol a 10%. Existem diversas variações na anatomia macroscópica do tubo digestório entre os primatas e estas variações ocorrem de acordo com os hábitos alimentares. Em Alouatta belzebul, que são folívoros-frugívoros, o tubo digestório abrange a maior parte da cavidade abdominal. Estes animais possuem números variáveis de rugas palatinas, de 10 a 17 pares de rugas, independente do sexo e idade, valores estes diferentes dos relatados para Sapajus libidinosus, de 18 a 21 pares de rugas. O estômago pseudo-compartimentalizado com uma região glandular e duas aglandulares, assemelhando com os achados de Nasalis larvatus. O intestino grosso apresenta o ceco aumentado em formato de L, corroborando com os achados em Callithrix penicillata. Os resultados demonstram que as variações estruturais do tubo digestório ocorrem de acordo com o hábito alimentar das diferentes espécies.

Habitat suitability for primate conservation in north-east Brazil

AbstractBrazil has a high diversity of primates, but increasing anthropogenic pressures and climate change could influence forest cover in the country and cause future changes in the distribution of primate populations. Here we aim to assess the long-term suitability of habitats for the conservation of three threatened Brazilian primates (Alouatta belzebul, Sapajus flavius and Sapajus libidinosus) through (1) estimating their current and future distributions using species distribution models, (2) evaluating how much of the areas projected to be suitable is represented within protected areas and priority areas for biodiversity conservation, and (3) assessing the extent of remaining forest cover in areas predicted to be suitable for these species. We found that 88% of the suitable areas are outside protected areas and only 24% are located in areas with forest cover. Although not within protected areas, 27% of the climatically suitable areas are considered priority areas for conservation. Future projections, considering a severe climate change scenario, indicate that A. belzebul, S. flavius and S. libidinosus may lose up to 94, 98 and 54% of their suitable range, respectively. The establishment of primate populations and their long-term survival in these areas are at risk. Mitigation actions such as the implementation of new protected areas, forest restoration and reduction of greenhouse gas emissions will be essential for the conservation of Brazilian primates.

Personality traits modulate stress responses after enclosure change of captive capuchin monkeys (Sapajus libidinosus)

Husbandry procedures may cause behavioral and physiological changes to animals living in captivity. However, an individual’s reaction is not uniform and may be related to different coping strategies. In this study, we analyzed whether and how 12 adult captive capuchin monkeys (Sapajus libidinosus) varying in four personality axes (‘Feeding’, ‘Sociability’, ‘Exploration’, and ‘Activity’) differed in their stress responses to an enclosure change. Behavioral data and fecal samples of the individuals were collected for two months before (97 h and 246 fecal samples) and 14 days after the enclosure change (52 h and 666 fecal samples). We used Akaike Information Criteria to select the best linear regression models having personality axes and the period after enclosure change as predictive factors and behaviors potentially indicative of stress (BPIS) and levels of fecal glucocorticoid metabolites (FGM) as the response variables. Best models indicate that specific personality axes acted as a buffer and improved individual stress coping, mainly at the physiological level. More sociable and more active individuals did not show the peak of FGM levels as that exhibited by their less sociable and less active counterparts on the first day of the enclosure change. The link between exploration and resilience to acute stress was less clear: more exploratory individuals showed an increase in FGM levels during the first week of enclosure change, while the less exploratory ones showed a later increase, during the second-week post-enclosure change, suggesting a lesser capacity to recover from stressful stimuli in these individuals. The results presented in this study build on growing literature showing that animals differ in their behavioral profiles and that these differences relate to resilience to environmental disturbances, which may impact individual survival and reproduction, resulting in less genetic diversity of captive colonies and increased issues related to research replicability. We argue that these interindividual differences must be considered in husbandry decisions and during research data collection for the sake of animal welfare and reliable science.

Zoonotic potential of oral microbiota of capuchins monkeys (sapajus libidinosus)

Sapajus libidinosus is a species of primates, popularly known as capuchin monkey. The oral cavity of the monkeys may have pathogenic microbiota for human. Therefore, the study of the microbiota of these species is of great interest in unique health. The objective of the present article was to carry out a survey of the oral microbiota of Sapajus libidinosus, kept in captivity, in the Zoobotanical Park of Teresina (PI, Brazil). Ten chemically immobilized primates were used. Samples were collected from the oral mucosa along the maxillary muco-gingival transition, and these samples were sent to culture and microbiological identification. Most of the microorganisms found were Gram negative and E.coli was the most frequent, followed by Enterobacter spp, Klebsiella spp, Proteus mirabilis, Citrobacter spp.,Morganella morganii, as well as Gram positive bacteria of the type Staphylococcus spp. The data obtained demonstrated the presence of bacterial strains with potential risk of transmission to other animals kept in the park as well as humans in contact with these animals.

Isotopic and elemental corroborates for wild bearded capuchin (Sapajus libidinosus) omnivorous dietary adaptation at Fazenda Boa Vista, Brazil.

This study analyzes variability in the diets of wild bearded capuchin monkeys, Sapajus libidinosus, by analyzing stable carbon (δ13 C) and nitrogen (δ15 N) isotope ratios and elemental concentrations (%C and %N) of fecal samples and food items. Developing isotopic and elemental correlates for diets of habituated subjects is a necessary step towards applying similar methods to interpret diets of unhabituated or cryptic subjects. Fecal samples from wild capuchins and their foods were collected at Fazenda Boa Vista, Brazil. Fecal samples from laboratory-housed Sapajus spp. and their foods were analyzed to establish diet-feces offsets for δ13 C, δ15 N, %C, and %N. Samples were dried, powdered, and measured for isotopic and elemental values. A Bayesian mixing model commutes isotopic and elemental data from wild capuchins into likely proportions of different food categories. The captive study shows small diet-feces spaces for Sapajus spp. of -0.8 ± 0.7‰ for δ13 C, -0.2 ± 0.4‰ for δ15 N, -6.1 ± 1.7% for %C, and -1.0 ± 0.6% for %N. The wild study shows omnivorous diets based on C3 , C4 , and CAM plants, and fauna. Subject diets are highly varied within and between days. Fecal data show age-related differences in diet and crop-raiding. There is no consistent isotopic or elemental difference between mothers and infants. Fecal stable isotope and elemental evidence employed in a Bayesian mixing model reflects the highly varied diets of capuchin monkeys in an isotopically heterogeneous environment. The isotopic and elemental variability reported here will aid similar diet reconstructions among unhabituated subjects in the future, but precludes tracking weaning isotopically among capuchins in this environment.