Ontogenesis of sociability of wild immature capuchin monkeys (Sapajus libidinosus): Sex more than personality explains interindividual variation.

Sociability is a fundamental trait that social animals need to survive and reproduce in societies. Sociability predicts how an individual can consistently interact with its conspecifics across time and situations. By studying capuchin monkeys (Sapajus libidinosus), a neotropical primate with complex social behavior and high cognitive capacity, our research aims to analyze the development of the social axis of personality of immature individuals, from birth to the third year of life. We studied wild monkeys belonging to a group with infants, juveniles, and adults of both sexes that inhabits northeastern Brazil. We analyzed the behavior of 12 immature capuchins (6 males and 6 females) in 94 h of videos recorded weekly from birth until 36 months, through daily focal sampling. We verified whether there was intraindividual consistency throughout development by fitting regression models for the effect of age on initiating affiliative social behaviors, controlling for monkey identity and sex. Our results indicate that the individuals of this study exhibit high variation in the initiation of behaviors at the beginning of infancy; there was low repeatability and high intra-individual variation during the first 3 years of life of these individuals, indicating that the social personality is not consolidated in this period. Immature females were more sociable than immature males. Therefore, differences in sociability in early life of bearded capuchin monkeys are best explained by sex rather than personality. We suggest that the high initial behavioral variation in the social axis of personality allows for plasticity influenced by the environment throughout development. The high sociability of females in infancy may be related to female philopatry and their high sociability in adulthood.

Comparative morphofunctional analysis of axial skeleton excluding the skull of primates based on the anatomical, radiographic, and tomographic description of the black-striped capuchin (Sapajus libidinosus Spix, 1823).

Comparative anatomy the basis for studies of evolution, and radiographic and tomographic aspects, as auxiliary methods in the investigation of anatomical particularities, reinforce evolutionary research. Therefore, the aim of this study was to describe the vertebrae, sternum, and ribs of the capuchin monkey (Sapajus libidinosus) by means of anatomical dissection and radiographic and tomographic images. To this purpose, four cadavers were used in the anatomical analysis and five living animals for the imaging exams. The bones were described and compared with data from other primates species found in literature. Student's t-test for independent samples was performed. The vertebral column of the comprises seven cervical, 13 or 14 thoracic, five or six lumbar, two or three sacral, and 23 or 24 caudal vertebrae. The atlas is characterized by three foramina on the wing. The seventh cervical vertebra had a transverse foramen in one specimen. The anticlinal vertebra is always the penultimate thoracic one, the ninth pair of ribs is always the last sternal pair, and the last two are buoyant. The sternal was composed of five or six sternebrae. The lumbar vertebrae showed a bifurcated spinous process. Three different sacral morphologies were observed. The structures identified macroscopically could be well determined through radiographic and tomographic images. S. libidinosus presented anatomical characteristics more similar to those of man and of platirrinos monkeys. The knowledge obtained by macroscopic anatomy and tomographic and radiological exams contributes significantly to comparative evolutionary studies.

Influence of landscape structure on previous exposure to Leptospira spp. and Brucella abortus in free-living neotropical primates from southern Brazil.

The environments in which neotropical primates live have been undergoing an intense fragmentation process, constituting a major threat to the species' survival and causing resource scarcity, social isolation, and difficulty in dispersal, leaving populations increasingly vulnerable. Moreover, the proximity of wild environments to anthropized landscapes can change the dynamics of pathogens and the parasite-host-environment relationship, creating conditions that favor exposure to different pathogens. To investigate the previous exposure of free-living primates in Rio Grande do Sul State (RS), southern Brazil, to the bacterial agents Leptospira spp. and Brucella abortus, we investigated agglutinating antibodies against 23 serovars of Leptospira spp. using the microscopic agglutination test and B. abortus acidified antigen test in primate serum samples; 101 samples from primates captured between 2002 and 2016 in different forest fragments were used: 63 Alouatta caraya, 36 Alouatta guariba clamitans, and 02 Sapajus nigritus cucullatus. In addition, the forest remnants where the primates were sampled were characterized in a multiscale approach in radii ranging from 200 to 1400 m to investigate the potential relationship of previous exposure to the agent with the elements that make up the landscape structure. The serological investigation indicated the presence of antibodies for at least one of the 23 serovars of Leptospira spp. in 36.6% (37/101) of the samples analyzed, with titers ranging from 100 to 1600. The most observed serovars were Panama (17.8%), Ballum (5.9%), Butembo (5.9%), Canicola (5.9%), Hardjo (4.9%), and Tarassovi (3.9%); no samples were seropositive for Brucella abortus. Decreased forest cover and edge density were the landscape factors that had a significant relationship with Leptospira spp. exposure, indicating that habitat fragmentation may influence contact with the pathogen. The data generated in this study demonstrate the importance of understanding how changes in landscape structure affect exposure to pathogenic microorganisms of zoonotic relevance. Hence, improving epidemiological research and understanding primates' ecological role in these settings can help improve environmental surveillance and conservation strategies for primate populations in different landscapes.

Osteology applied to image diagnosis of the forelimb of the black-striped capuchin (Sapajus libidinosus Spix, 1823).

Macroscopic bone analysis and evaluation through imaging methods are essential in the recognition of natural and altered structures. Therefore, this study aimed at describing the osteology the thoracic limb of Sapajus libidinosus in bone pieces, identifying them in radiographic and tomographic images. For this, four cadavers were used in the macroscopic analysis and five animals for the imaging exams, of which four were euthanized and added to the macroscopic stage. For imaging exams, the animals were kept anesthetized. All bones were documented, structures described, and compared with literature data from human and nonhuman primates. There was no statistical difference between males and females regarding the length of the forelimb bones. Most of the bone structures of the scapula were well identified in the imaging methods, being more restricted in the ventrodorsal projection. The clavicle presented very limited visualization. The humerus, as well as the radius and ulna, were not well portrayed in their proximal and distal epiphyses by radiography. However, they were well identified on tomography. All structures described in the macroscopic image of the carpal and metacarpal bones could be identified through radiography and tomography, and the radiographic examination of this region is an excellent method for identifying fractures. The glenoid notch of the scapula was not visualized by any imaging method. S. libidinosus presented anatomical characteristics more similar to those of neotropical primates and man, being a great indicator of an experimental model for studies in these species.

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.

A robust tool kit: First report of tool use in captive crested capuchin monkeys (Sapajus robustus).

Primate tool use is of great interest but has been reported only in a limited number of species. Here we report tool use in crested capuchin monkeys (Sapajus robustus), an almost completely unstudied robust capuchin species. Crested capuchins and their sister species, the yellow-breasted capuchin, diverged from a common ancestor over 2 million years ago, so this study fills a significant gap in understanding of tool use capacity and variation within the robust capuchin monkey radiation. Our study group was a captive population of seven individuals at the Santa Ana Zoo in California. The monkeys were given no prior training, and they were provided with a variety of enrichment items, including materials that could be used as tools as well as hard-to-access resources, for open-ended interactions. In 54 observation hours, monkeys performed eleven tool use actions: digging, hammering, probing, raking, sponging, striking, sweeping, throwing, waving, wedging, and wiping. We observed tool modification, serial tool use, and social learning opportunities, including monkeys' direct observation of tool use and tolerated scrounging of foods obtained through tool use. We also observed significant individual skew in tool use frequency, with one individual using tools daily, and two individuals never using tools during the study. While crested capuchins have never been reported to use tools in the wild, our findings provide evidence for the species' capacity and propensity for tool use, highlighting the urgent need for research on this understudied, endangered primate. By providing detailed data on clearly identified S. robustus individuals, this study marks an effort to counteract the overgeneralization in the captive literature in referring to any robust capuchins of unknown provenance or ancestry as Cebus apella, a practice that obfuscates potential differences among species in tool use performance and repertoire in one of the only species-rich tool-using genera in the world.

Anatomy applied to image diagnosis of the hind limb in the black-striped capuchin (Sapajus libidinosus Spix, 1823).

The knowledge of anatomy and imaging exams emerges as an important tool in the study of evolutionary processes of a species, in the elaboration of diagnosis, and the successful choice of the appropriate clinical and surgical procedures. Therefore, this study aims to describe the osteology of the hind limb of Sapajus libidinosus by means of gross, radiographic, and tomographic images. Four cadavers were used in the macroscopic analysis and five animals for the imaging exams, of which four were eventually euthanized and added to the macroscopic study. For imaging exams, they were kept anesthetized. All bones of the hind limb were documented, their structures were described, and compared with data in the literature from human and nonhuman primates. We have performed Student's t test for independent samples. There was no statistical difference between the sexes regarding the length of the hind limb bones. The coxal bone was largely well described using imaging methods. A small penile bone was present at the tip of the penis and it could be identified by all analysis methods. The femur, as well as the tibia and fibula, were not well portrayed in their proximal and distal epiphyses by radiography (Rx). However, they were well identified on tomography. No third trochanter was observed in the femur and the patella had a triangular shape. All the structures described by gross anatomy of the tarsus and metatarsus could be identified by Rx and tomography. More subtle structures, such as the popliteal notch on the tibia, and the gluteal tuberosity pectineal line and facies aspera on the coxal bone, were not identified by medical imaging. S. libidinosus presented anatomical characteristics that were similar to those of larger New World and Old World monkeys, including man. This suggests it's value as an experimental model for studies in recent primates.

Diet, activity patterns, and home range use in forest and cultivated areas for one wild group of endangered crested capuchin monkeys (Sapajus robustus) in Reserva Natural Vale, Espírito Santo, Brazil.

Robust capuchin monkeys (Sapajus spp.) are distributed widely in the Neotropics and may be able to survive in modified landscapes because of their omnivorous, opportunistic diet. The poorly known and endangered crested capuchin monkey (Sapajus robustus) is endemic to the Atlantic Forest in Bahia, Minas Gerais and Espírito Santo states, Brazil. We collected data on diet and home range for a crested capuchin group with access to forest and cultivated areas. We hypothesized that with access to cultivated exotic fruit, capuchins would use cultivated areas more for feeding during the season of fruit scarcity in the surrounding forest and have a small home range size because of higher fruit availability. Both the forest and the cultivated areas peaked in fruit availability in the wet season, with a low proportion of trees producing fruit in the dry season; cultivated areas had a higher proportion of trees in fruit compared to the forest throughout the study. While monkeys consumed exotic fruits like jackfruit and oil palm, we recorded more samples of them eating forest fruits than exotic fruits in all but 1 month, and they consumed a more diverse array of forest fruits (56 species) but only six exotic species. Home range size was relatively small compared with other studies: 120.5 ha across the year (wet season 102 ha, dry season 111.5 ha). Natural and human-intensified fruit sources in a protected area without hunting may have allowed monkeys to maintain a smaller home range size. The group composition changed during the study; this also likely influenced home range use. Studies focused on robust capuchin groups that utilize agricultural or cultivated foods may underestimate home range needs for groups without access to human-intensified food sources. Studying crested capuchin ecology in additional locations will be important for establishing a sound species conservation program.

Time budget and foraging strategies of two provisioned groups of tufted capuchin monkeys, Sapajus libidinosus, in a small, seasonal urban forest fragment.

Studies of urban monkeys provide important insights into the behavioral flexibility of primate species. We studied two provisioned groups of capuchin monkeys that inhabit a small forest fragment in the city of Goiânia, Brazil. One of the groups was dominant and had priority of access to both native and provisioned resources. Anthropic resources were available in two relatively small areas within this forest, but varied in their quality. We hypothesized that intergroup dominance and the seasonality of native resources would have different impacts on the foraging strategies and use of space by the two study groups. Data on the location of the members of the two groups, their behavior, and consumption of different food items were collected during five dry season and five rainy season months. The members of the dominant group spent more time in the provisioned area where anthropic food was less costly to obtain and consumed more provisioned fruit and vegetables than the members of the subordinate group. The differences between groups were exacerbated during the dry season, when sources of native fruit were less abundant. The results of the present study illustrate how capuchins may respond to the variation in proximate factors, such as intergroup dominance and seasonality. These factors were determinants to the variation in the diet and the use of space observed between the two study groups.

Haematology, physiological parameters, morphometry and parasitological status of rescued bearded capuchin monkeys (Sapajus libidinosus).

BACKGROUND: There are few studies on the physiology and haematology of rescued bearded capuchin monkeys. These are necessary to better understand the health and welfare status of the animals, including when performing reintroductions, and to avoid zoonoses. METHODS: We aimed to obtain physiological and haematological values, morphometry and parasitological status of 26 bearded capuchins in two rescue centres in Northeast Brazil. RESULTS: We found sex- and age-related differences in respiratory rate, body weight and body mass index, but not haematology. The haematological values obtained were significantly different from published data but within the reference intervals for the species. Animals infected with Ancylostoma spp. had significantly lower values in the parameters: haemoglobin concentration, mean corpuscular volume and mean corpuscular haemoglobin concentration than non-infected individuals. CONCLUSION: Physiological and haematological values of rescued capuchins were similar to those found in previous studies. Ancylostomiasis appears to cause alterations to haematological values of this species.

Changes in Intraspecific Diversity of the Arbuscular Mycorrhizal Community Involved in Plant-Plant Interactions Between Sporobolus robustus Kunth and Prosopis juliflora (Swartz) DC Along an Environmental Gradient.

The intensification of biological processes coping with salt stress became a major issue to mitigate land degradation. The Sine-Saloum Delta in Senegal is characterized by salt-affected soils with vegetation dominated by salt-tolerant grass Sporobolus robustus and shrubs like Prosopis juliflora. Plant experiments in controlled conditions suggested that arbuscular mycorrhizal (AM) fungi might be the key actors of facilitation process observed between S. robustus and P. juliflora, but the AM fungal community determinants are largely unknown. The current field-based study aimed at (1) characterizing the environmental drivers (rhizosphere physico-chemical properties, plant type and season) of the AM fungal community along an environmental gradient and (2) identifying the AM fungal taxa that might explain the S. robustus-mediated benefits to P. juliflora. Glomeraceae predominated in the two plants, but a higher richness was observed for S. robustus. The pH and salinity were the main drivers of AM fungal community associated with the two plants, negatively impacting richness and diversity. However, while a negative impact was also observed on mycorrhizal colonization for S. robustus, P. juliflora showed opposite colonization patterns. Furthermore, no change was observed in terms of AM fungal community dissimilarity between the two plants along the environmental gradient as would be expected according to the stress-gradient and complementary hypotheses when a facilitation process occurs. However, changes in intraspecific diversity of shared AM fungal community between the two plants were observed, highlighting 23 AM fungal OTUs associated with both plants and the highest salinity levels. Consequently, the increase of their abundance and frequency along the environmental gradient might suggest their potential role in the facilitation process that can take place between the two plants. Their use in ecological engineering could also represent promising avenues for improving vegetation restoration in saline Senegalese's lands.

Prevalence and description of dental disorders in skulls of free-living wild primates from Paraná State, Brazil.

BACKGROUND: Non-human primates can present oral diseases. However, differences among the dentition of the various species make it difficult to understand their dental features and associated diseases. This research hypothesizes that the prevalence of dental disorders varies in the species studied according to distinct types of diet. METHODS: Forty-five syncraniums of the species Alouatta caraya, Alouatta guariba clamitans, Sapajus nigritus, Callithrix jacchus, and Callithrix penicillata were evaluated by visual inspection, magnifying glasses, and on cone-beam computed tomography. RESULTS: Disorders identified consisted of missing teeth before death, agenesis, dental calculus, dental wear, dental staining, dental fracture, exposure of pulp chamber, alveolar bone resorption, tooth discoloration, and persistence of deciduous teeth. Alouatta guariba clamitans presented the most disorders. CONCLUSIONS: The results suggest that neotropical primates have a high prevalence of dental changes, even in free-living conditions, and that the differences observed among them may be associated with different diet patterns.

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.

Black capuchin monkeys dynamically adjust group spread throughout the day.

Variation in group spread can affect communication between individuals, synchrony of activity and collective decision-making. Most studies have measured this variation in large time scales, but the variables that influence group spread change as the social unit ranges over different areas throughout the day. Thus, our aim was to analyze the diurnal variation in group spread of a group of black capuchin monkeys (Sapajus nigritus) inhabiting an area within the southeastern Brazilian Atlantic Forest, the Carlos Botelho State Park. We measured group spread as the distance between the coordinates of the location of the two most distant group members every 5 min during entire days. Using time series analysis, we found that the group spread varied within short periods of time (15 min) throughout the day, revolving around the average group spread distance of 36 m. Group members tended to decrease the interindividual distance over time when they were more than 36 m apart, and to increase the distance when they were at a distance of less than 36 m. In addition, group spread was higher when monkeys were eating fruit than during other activities. We conclude that the variation in group spread may reflect competition for discrete food resources and that increasing cohesion several times throughout the day can be a way of resuming social contact between individuals.

Ontogeny and sex differences in object manipulation and probe tool use by wild tufted capuchin monkeys (Sapajus libidinosus).

Tufted capuchin monkeys (Sapajus spp.) are the only Neotropical Primates that regularly use tools in the wild, but only one population of bearded capuchin monkeys (Sapajus libidinosus) is known to habitually use sticks as probes. In this population, males are typically the only sex to use stick tools, something unexpected, since there are no obvious physical constraints, and females do use stone tools in the wild and sticks in experimental conditions. We investigated the development of probe tool use in eight infants to clarify whether social influences on learning varied between the sexes, as tool use learning by capuchin monkeys is a socially biased process. We found that in the first 10 months of age, females manipulate sticks as much as males, but after 10-12 months of age, males begin to manipulate them at higher frequencies. We examined if social connections-as opportunities for social learning-could explain this difference and verified that, on close distance social networks, infant males and females have similar connections with older males. However, males observe probe tool use events more often than females when close to such events. The higher frequency of manipulation of sticks, as well as the higher rates of probe tool use observation, appear to be the key to understand why only males are probe tool users in this population. Since there are only male potential models of probe use, a sex motivational bias could explain the sex difference in observation; a bias in observation could explain the differences in manipulation-and manipulation rates would certainly influence the chances of individual, trial-and-error learning (a case of "local/stimulus enhancement").

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.

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.

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'.