Cebus Apella Research Articles

Tree holes as a source of water for primate species in an Amazonian Forest fragment, northern Brazil

Abstract. Water is an essential nutrient for living beings and is fundamental to metabolic processes. Under free-living conditions, primate individuals can use different strategies, skills, and resources to access water. Here, we report on observations of water consumption in Ateles chamek and Sapajus apella; describe the environmental conditions in which such events were observed, as well as the behavior of the individuals; and compare these observations with similar records in neotropical primates. Water consumption was observed during primate surveys in a forest fragment of approximately 52 ha bordered by the Jaru River, located southwest of the Brazilian Amazon, Vale do Paraíso municipality, state of Rondônia, Brazil. To access water, individuals of A. chamek used their tails, whereas S. apella used a leaf as a tool. Our observations suggest that tree holes may be important water sources for primates in forest fragments and that individuals of different species use different strategies to collect water from tree holes. Access and consumption strategies are directly associated with different cognitive skills and behaviors, which may include using tools, as in the case of capuchins. As water consumption records are limited, these findings highlight the need for continuous reporting to better understand water acquisition. Such reports are especially needed in the context of fragmented and degraded habitats, where water availability is affected by edge effects and the reduction in both fleshy fruits and moisture, which are important for primate species.

Body Mass Gain in Wild Brown Capuchins (Sapajus apella) in Relation to Fruit Production and Social Dominance.

In ecological contexts natural selection might favor individuals with a larger body mass to monopolize resources; however, there is wide variation in body mass within populations and potential factors. In this study, we evaluated whether fruit production limits body mass in one group of Sapajus apella, its effects on behavior, and whether there is a relationship between social status and body mass. We recorded activity patterns using focal follows (20 min), body mass (using a modified Ohaus scale), and community wide fruit production estimates (from 60 fruit traps). Body mass remained relatively stable during periods of food scarcity, but in periods of abundance most individuals gained weight, as indicated by their relative growth rates (RGR). Subordinate subadults showed the highest RGR, as expected by their age. In periods of high fruit production activities as traveling, grooming, and playing were more frequent than during fruit scarcity, suggesting energy maximization and potential energetic constraints. We found differences in behavior within the group, as the alpha male was observed feeding more frequently (and for longer periods of time), was more aggressive (e.g., feeding trees), and received more grooming than other individuals. In addition, the alpha male was 60% heavier than the group's average body mass. Our study supports the hypothesis that body weight gain is related to fruit abundance and that body size is associated with social dominance; however, large individuals (both males and females) seem to incur in high metabolic or reproductive costs, as they do not gain much weight as smaller individuals.

A nonhuman primate model for genital herpes simplex virus 2 infection that results in vaginal vesicular lesions, virus shedding, and seroconversion.

The most commonly used animal models for evaluating the efficacy of HSV-2 candidate vaccines are mice and guinea pigs. While numerous HSV-2 vaccine candidates have been tested in these animals and were effective in reducing disease and mortality, these results did not predict the effectiveness of the vaccines in human trials. Infection of rhesus macaques rarely results in lesions or HSV-2 specific antibody responses. In seeking an animal model that better recapitulates human disease and that might be more predictive of the efficacy of prophylactic vaccines than mice and guinea pigs, we evaluated Cebus apella (C. apella), a New World primate, in an HSV-2 genital infection model. Infectious HSV-2 was cultured from vaginal swabs from all 4 animals for 9-14 days after intravaginal inoculation of HSV-2 seronegative monkeys. Two of 4 monkeys had vesicular lesions in the vagina or vulva. No neurological symptoms were noted. Recurrent lesions and HSV-2 DNA shedding after acute disease resolved was infrequent. UV irradiation of the genital area did not induce recurrent genital lesions or virus shedding. All 4 monkeys developed HSV-2 neutralizing antibodies as well as virus-specific CD4 and CD8 T cell responses. Reinfection of animals 15 to 19 months after primary infection did not result in lesions; animals had reduced virus shedding and a shorter duration of shedding compared with that during primary infection, suggesting that primary infection induced protective immunity. Primary fibroblasts from C. apella monkeys supported the growth of HSV-2 in vitro; in contrast, HSV-2 did not replicate above the titer of the input inoculum in fibroblasts from rhesus macaques. These observations suggest that the C. apella monkey has potential to serve as a model for evaluating the efficacy of prophylactic vaccines, antivirals, or monoclonal antibodies to HSV-2.

Salivary cortisol captures endocrine response to an acute stressor in captive female tufted capuchin monkeys (Sapajus apella).

Measuring glucocorticoids such as cortisol is a useful tool for exploring relationships among behavior, physiology, and well-being in primates. As cortisol circulates in blood, it moves into biological matrices such as hair, urine, feces, and saliva. Saliva sampling is a simple, noninvasive method to measure cortisol that can be easily implemented by training animals to voluntarily provide samples. The temporal lag between elevation of cortisol in the blood and elevation of cortisol in saliva likely varies by species and must be characterized to identify appropriate sampling regimens. In the present study we characterized the time course of cortisol changes in saliva following an acute psychological stressor in captive tufted capuchin monkeys (Sapajus apella). We trained eight free-moving female tufted capuchin monkeys to voluntarily produce clean saliva samples. We exposed them to the acute stressor of a veterinary catch net and observed behavior pre and post exposure. We collected salivary samples immediately pre exposure (0 min) and 30, 45, 60, 75, 90, and 120 min after exposure. Salivary cortisol was quantified using a Salimetrics kit. Behavioral and cortisol measures were compared within individuals to a control condition in which no stressor was presented. Capuchins showed a clear behavioral response to the stressor by demonstrating increased freezing and pacing, decreased feed foraging, nonsocial play, and scratching, and decreased willingness to provide saliva samples after stressor presentation. After stressor presentation, average salivary cortisol began to increase at 30 min and continued to increase through the 120 min sample period. There was individual variation in absolute cortisol levels, the timing of the cortisol increase, and the timing of the peak. Our results suggest that no single time-point can be reliably used to evaluate salivary cortisol response to an acute stressor across individuals, and instead we recommend the collection of a prolonged time series.

The Impact of Land Conversion on Primate Habitats: Refining the Extent of Occurrence Data for Four Capuchin Species in North and Northeastern Brazil

AbstractConversion of primate forest habitat is a global concern with significant implications for primate populations. Although the geospatial Extent of Occurrence (EOO) data provided for primates by the International Union for the Conservation of Nature are widely used, they do not accurately reflect the existing extent of primate species because of ongoing habitat loss. We focused on four capuchin monkey species (Sapajus apella, S. flavius, S, libidinosus, and S. xanthosternos), all native to North and Northeastern Brazil, to prioritize research by the Capuchin Action Network. We refined the EOOs for the four primate species using MapBiomas land cover data. We accounted for areas of agriculture, urban, and mining and updated the EOOs of the four species. Additionally, we evaluated the Conservation Units in each EOO. Conservation Units are protected areas critical to mitigating habitat loss in Brazil. Our results show that S. apella has lost the smallest amount of its EOO (13%), while S. flavius has lost the most (77%). Agriculture was the leading cause of land cover change, followed by urbanization and mining. We provide an updated EOO for the four capuchin species and highlight the need for conservation efforts to address the challenges posed by human activities in the capuchin species’ habitats.

Capuchin monkeys' (Sapajus [Cebus] apella) categorization of photos of unknown male conspecifics suggests attention to fWHR and a dominance bias.

The ability to quickly perceive others' rank minimizes costs by helping individuals behave appropriately when interacting with strangers. Indeed, humans and at least some other species can quickly determine strangers' rank or dominance based only on physical features without observing others' interactions or behavior. Nonhuman primates can determine strangers' ranks by observing their interactions, and some evidence suggests that at least some cues to dominance, such as facial width-to-height ratio (fWHR), are also present in other primates. However, it is unknown whether they can determine strangers' rank simply by looking at their faces, rather than observing their interactions. If so, this would suggest selective pressure across the primates on both cues to dominance and the ability to detect those cues accurately. To address this, we examined the ability of male and female tufted capuchin monkeys (Sapajus [Cebus] apella) to categorize images of the faces of unknown conspecifics (Sapajus from different colonies) and humans (computer-generated and real) as dominant or nondominant based only on still images. Capuchins' categorization of unknown conspecific faces was consistent with fWHR, a cue to dominance, although there was a strong tendency to categorize strangers as dominant, particularly for males. This was true despite the continued correct categorization of known individuals. In addition, capuchins did not categorize human strangers in accordance with external pre-ratings of dominance by independent human raters, despite the availability of the same cue, fWHR. We consider these results in the context of capuchin socio-ecology and what they mean for the evolution of rapid decision-making in social contexts.

Analysis of intestinal bacterial diversity and its gene function prediction in black-capped capuchin (Sapajus apella)

ABSTRACT In this study, we used high-throughput sequencing technology to analyze the diversity and predict gene function of intestinal bacteria from captive black-capped capuchin in two wildlife parks. The results showed that the composition of intestinal gut bacterial diversity was significantly higher in black-capped capuchins monkeys from ES than HT. Moreover, high similarity of intestinal bacteria of black-capped capuchins at the same site was found by sample stratum clustering. Black-capped capuchins intestinal bacteria can be clustered into 2296 ASVs, belonging to 16 phyla, 99 families and 210 genera, respectively. The dominant phyla were Bacteroidota and Firmicutes in the intestinal bacteria of black-capped capuchins, but there were differences in the dominant bacterial families and dominant bacterial genera between ES and HT, and the bacterial families with significant differences had correspondence with bacterial genera. The results provide a basis for the study of intestinal bacteria in black-capped capuchins and the isolation and purification of dominant bacteria. The results of this study fill the gap in the study of intestinal bacterial diversity and its gene functions in black-capped capuchins, and provide a reference for the isolation of dominant bacteria in black-capped capuchins’ intestinal microbes and the discovery and study of novel functional genes.

The Joint Simon task is not joint for capuchin monkeys

Human cooperation can be facilitated by the ability to create a mental representation of one’s own actions, as well as the actions of a partner, known as action co-representation. Even though other species also cooperate extensively, it is still unclear whether they have similar capacities. The Joint Simon task is a two-player task developed to investigate this action co-representation. We tested brown capuchin monkeys (Sapajus [Cebus] apella), a highly cooperative species, on a computerized Joint Simon task and found that, in line with previous research, the capuchins' performance was compatible with co-representation. However, a deeper exploration of the monkeys’ responses showed that they, and potentially monkeys in previous studies, did not understand the control conditions, which precludes the interpretation of the results as a social phenomenon. Indeed, further testing to investigate alternative explanations demonstrated that our results were due to low-level cues, rather than action co-representation. This suggests that the Joint Simon task, at least in its current form, cannot determine whether non-human species co-represent their partner’s role in joint tasks.

From imaging to precision: low cost and accurate determination of stereotactic coordinates for brain surgery Sapajus apella using MRI.

The capuchin monkey (Sapajus apella), a New World monkey species, exhibits prominent characteristics that make it an ideal model for neuroscience research. These characteristics include its phylogenetic traits, telencephalization coefficient, anatomical structures and pathways, genetic profile, immune responses, cognitive abilities, and complex behavioral repertoires. Traditionally, methodologies for stereotactic neurosurgery in research models have relied on the use of brain atlases. However, this approach can lead to errors due to the considerable variation in brain size and shape among individual monkeys. To address this issue, we developed a protocol for deriving individual coordinates for each monkey using a straightforward and relatively inexpensive method involving MRI imaging. Our protocol utilizes a specially designed, 3D-printed stereotactic head-holder that is safe to use with an MR magnet, non-invasive placement of fiducial markers, and post-processing with open-source software. This approach enhances MRI data visualization, improves anatomical targeting, and refines the design of neurosurgical experiments. Our technique could also prove beneficial in other areas of neuroscience research that require accurate calculation of stereotaxic coordinates. Furthermore, it could be useful for other nonhuman primate species for which brain atlases are typically unavailable.

Intestinal parasites infecting captive non-human primates in Italy.

Non-human primates (NHPs) living in captive conditions are susceptible to intestinal parasites that can contribute to mortality and morbidity, and cause zoonotic infections. Thus, parasite surveys on NHP populations under human care are relevant as part of the evaluation of NHPs welfare and in the zoonotic disease risk assessment, as well as in the exploration of parasite transmission pathways, according to the One-Health concept. This study aimed to identify intestinal parasites infecting NHPs living in two wildlife recovery centers and in a zoological garden, in Italy. Ninety-three fecal samples from Macaca tonkeana, Macaca fascicularis, Sapajus apella, Chlorocebus aethiops, Macaca fuscata, Macaca sylvanus, and Cebus capucinus were collected at Piano dell'Abatino Park (Lazio), and fecal smears and flotation were performed in order to identify parasites according to morphological keys. Additionally, one carcass of M. fuscata from the Bioparco Zoological Garden of Rome (Lazio) and one of M. fascicularis from the Center for the Recovery of Exotic and Maremma Wild Animals (Tuscany) were necropsied and intestinal adult nematodes were collected and characterized at morphological and molecular level, using the mitochondrial cox1 and rrnL markers. Protozoans (Entamoeba coli, Iodamoeba bütschlii, Dientamoeba fragilis-like, Giardia sp.), chromists (Balantidium/Buxtonella sp.) and nematodes (Capillaria sp., Trichuris sp., strongyliform larvae and Oesophagostomum sp.) were found through fecal smears and flotation. The collected adult nematodes from dead NHPs were morphologically identified as whipworms (genus Trichuris). Phylogenetic analyses grouped Trichuris specimens into the Trichuris trichiura complex of species, with specimens from M. fuscata clustering into a host-specific branch, and whipworms from M. fascicularis clustering within a clade formed by Trichuris infecting several primate species, including humans. The results here collected revealed the presence of potentially zoonotic parasites circulating in captive primates in Italy, providing useful information for the formulation of management and care plans for captive NHPs, and for the elaboration of safety measures for visitors and animal keepers.

Detection and Genotyping of Trypanosoma cruzi Samples in Species of Genus Rhodnius from Different Environments in the Brazilian Amazon.

Background: In the Amazon region, several species of triatomines occur in the natural environments. Among them, species of the genus Rhodnius are a risk to human populations due to their high rates of infection with Trypanosoma cruzi. The aim of this study was to identify the T. cruzi genotypes in Rhodnius specimens and their relationship with sylvatic hosts from different environments in the Brazilian Amazon. Methods: A total of 492 triatomines were collected from the municipalities of Monte Negro, Rondônia state, and Humaitá, Amazonas state, 382 of them being nymphs and 110 adults. Genotyping of T. cruzi in six discrete typing units (DTUs) was performed using conventional multilocus PCR. The triatomines that were positive for T. cruzi and engorged with blood were also targeted for amplification of the cytochrome B (cytB) gene to identify bloodmeal sources. Results: Of the 162 positive samples, the identified DTUs were TcI (87.65%) and TcIV (12.35%). It was observed that 102 specimens were engorged with a variety of bloodmeals. Triatomines infected with TcI were associated with DNA of all identified vertebrates, except Plecturocebus brunneus. TcIV was detected in triatomines that fed on Coendou prehensilis, Didelphis marsupialis, Mabuya nigropunctata, P. brunneus, Pithecia irrorata, Sapajus apella, and Tamandua tetradactyla. Conclusion: Results highlight the need to understand the patterns of T. cruzi genotypes in Rhodnius spp. and their association with sylvatic hosts to better elucidate their role in the transmission of Chagas disease in the Amazon region.

Disputes over provisioned resources are no more intense between groups than within groups in free-ranging Sapajus libidinosus.

Socioecological models predict that disputes between primate groups will be more intense than those within groups, given that the systematic loss of contests over a given resource will restrict the access of all of the members of that group to that resource. Higher levels of aggression are also expected for provisioned resources that have a more lucrative cost:benefit ratio. The levels of aggression in and between two free-ranging tufted capuchin monkey (Sapajus libidinosus) groups in the context of daily provisioning with bananas were evaluated. The aim of a complementary analysis was to identify possible predictors of the frequency of disputes at the site of the provisioned resource. The disputes were recorded using all-events sampling, while the social behaviour of the study groups was recorded by instantaneous scan sampling. The data were analysed using t-test, Mann-Whitney's U, and generalised linear modelling. Between-group disputes were no more intense than within-group events, and did not involve more individuals, or more adult females. The frequency of disputes increased as the number of individuals eating bananas increased. No evidence was found that disputes between groups were any more intense than those within groups. Dominance patterns may have affected these findings, by mediating intergroup disputes. An increase in the number of competitors affected the frequency of disputes at the site of the provisioned resource.

Gape drives regional variation in temporalis architectural dynamics in tufted capuchins.

Dynamic changes in jaw movements and bite forces depend on muscle architectural and neural factors that have rarely been compared within the same muscle. Here we investigate how regional muscle architecture dynamics-fascicle rotation, shortening, lengthening and architectural gear ratio (AGR)-vary during chewing across a functionally heterogeneous muscle. We evaluate whether timing in architecture dynamics relates to gape, food material properties and/or muscle activation. We also examine whether static estimates of temporalis fibre architecture track variation in dynamic architecture. Fascicle-level architecture dynamics were measured in three regions of the superficial temporalis of three adult tufted capuchins (Sapajus apella) using biplanar videoradiography and the XROMM workflow. Architecture dynamics data were paired with regional fine-wire electromyography data from four adult tufted capuchins. Gape accounted for most architectural change across the temporalis, but architectural dynamics varied between regions. Mechanically challenging foods were associated with lower AGRs in the anterior region. The timing of most dynamic architectural changes did not vary between regions and differed from regional variation in static architecture. Collectively these findings suggest that, when modelling temporalis muscle force production in extant and fossil primates, it is important to account for the effects of gape, regionalization and food material properties. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Measurement of Salivary Cortisol in Two New World Primate Species.

Glucocorticoids (GCs) are mammalian steroid hormones involved in a variety of physiological processes, including metabolism, the immune response, and cardiovascular functions. Due to their link to the physiological stress response, GC measurement is a valuable tool for conservation and welfare assessment in animal populations. GC levels can be measured from different matrices, such as urine and feces. Moreover, especially in captive settings, measuring GCs from saliva samples proved particularly useful as those samples can be collected non-invasively and easily from trained animals. Salivary GC levels can be measured using a variety of analytical methods, such as enzyme immunoassays. However, it is crucial to validate the analytical method for each specific application and species when using a new matrix. Using high-pressure liquid chromatography and a cortisol enzyme immunoassay, we show that the main glucocorticoids secreted in the saliva of squirrel monkeys and brown capuchin monkeys are cortisol and cortisone. Our biological validation found the expected salivary cortisol level to decline throughout the day. Our findings support the reliability of salivary cortisol measurements and their potential to be used as a valid tool in research and welfare assessment for these non-human primates.

Hand preference in wild crab-eating capuchin monkeys (Sapajus libidinosus) in the coastal area of Northest Brazil.

Handedness is a fundamental human trait, although recent research, especially on nonhuman primates, has shown that it is displayed by other animals as well (e.g., chimpanzees, gorillas). In this study, we explore hand preference in wild crab-eating tufted capuchin monkeys (Sapajus libidinosus) inhabiting a mangrove forest located on the coastal area of Northeast Brazil (Maranhão State). Tufted capuchin monkeys at our site use facultatively wooden tools to crack open crabs. We observed hand preference in 12 subjects who spontaneously participated in experiment sessions, in which we provided crabs and tools on wooden platforms. We recorded (using events and bouts) two unimanual tasks, (tool or crab) grabbing and (tool or crab) pounding, and one bimanual task, crab pulling, where one hand kept the crab in place while the other pulled off parts of the crab. Hand preference increased with greater strength needed to perform the task and its complexity. While only 17%-25% of capuchins showed hand preference during grabbing, 44%-64% showed hand preference during pounding, and most subjects 64%-80% displayed a right-hand preference when performing the bimanual task, for which all lateralized individuals were right-handed. Hand preference did not vary between adults and juvenile individuals and was not consistent across tasks. Group-level hand preference was found only for the bimanual task, for which all lateralized individuals were right-handed. Our findings are in concordance with those of other primate studies showing the emergence of hemispheric specialization for bimanual actions, highlight the importance of conducting such studies on diverse type of tasks, and show the feasibility to conduct experimental manipulation under natural conditions.

Incidence of leptospirosis in non-human primates at the santarém zoo, Pará, Brazil

Leptospirosis is an infectious disease that affects practically all domestic and wild animals, which can become carriers and, as a consequence, will contribute to the spread of the microorganism in nature. The present study aims to detect the occurrence of leptospirosis against by the microscopic serum agglutination test in animals at the Zoo of the Centro Universitário da Amazônia (ZOOUNAMA). 26 adult animals of both sexes and of the following species: 9 Sapajus apella, 2 Cebus kaapori, 3 Ateles marginatus, 10 Ateles paniscus, 1 Chiropetes satanas, 1 Allouata belzebul. Of the animals studied, 3 (11.5%) were reagents to be taken against Leptospira spp. The serovars found in the different species were: Icterohaemorragiae, Balum, Hardjo and Grippothyphosa. SAM proved to be efficient to detect against leptospira in non-human primates. Icterohaemorragiae type serum occurred with research results showing that it is also important in leptospirosis in non-human primates.

Ontogenetic changes in bite force and gape in tufted capuchins.

Bite force and gape are two important performance metrics of the feeding system, and these metrics are inversely related for a given muscle size because of fundamental constraints in sarcomere length-tension relationships. How these competing performance metrics change in developing primates is largely unknown. Here we quantify in vivo bite forces and gapes across ontogeny and examine these data in relation to body mass and cranial measurements in captive tufted capuchins, Sapajus spp. Bite forces and gapes were also compared across geometric and mechanical properties of mechanically challenging foods to investigate relationships between bite forces, gapes, and food accessibility (defined here as the ability to breach shelled nuts). Bite forces at a range of gapes and feeding behavioral data were collected from a cross-sectional ontogenetic series of 20 captive and semi-wild tufted capuchins at the Núcleo de Procriação de Macacos-Prego Research Center in Araçatuba, Brazil. These data were paired with body mass, photogrammetric measures of jaw length and facial width, and food geometric and material properties. Tufted capuchins with larger body masses had absolutely higher in vivo bite forces and gapes, and animals with wider faces had absolutely higher bite forces. Bite forces and gapes were significantly smaller in juveniles compared to subadults and adults. These are the first primate data to empirically demonstrate the gapes at which maximum active bite force is generated and to demonstrate relationships to food accessibility. These data advance our understanding of how primates meet the changing performance demands of the feeding system during development.

Do tufted capuchin monkeys, Sapajus spp., experience regret in decision making under risk?

Do tufted capuchin monkeys, Sapajus spp., experience regret in decision making under risk?

Consumption of muscovy duck eggs by brown capuchin monkeys in a peri-urban forest in the Amazon

Relatamos a captura e consumo de ovos de pata doméstica Cairina moschata (Linnaeus, 1758) por macaco-prego Sapajus apella (Linnaeus, 1758) em um ambiente peri-urbano próximo à cidade de Porto Velho, Brasil. Observamos um jovem de macaco-prego tirando dois ovos de um ninho. Ele posicionou um ovo entre os membros posteriores, mordendo-o com o dente canino, levando-o até a boca e virando para sugar o conteúdo. Este é o primeiro registro com informações detalhadas sobre como os macacos-prego capturam e consomem os ovos. O consumo de animais domésticos pode representar uma ameaça, já que os macacos-prego podem ser retaliados por isso.

Clinical and histopathological investigation of symmetrical alopecia with associated chronic pruritus in tufted capuchin monkeys (Sapajus apella apella).

Symmetrical alopecia is a common symptom of endocrine and autoimmune diseases, which are rarely manifested with pruritus. Increased levels of stress in primates have been presented with increased levels of pruritus and alopecia appearance. A pruritic and alopecic disease was investigated in a group of tufted capuchin monkeys (N = 12), but due to ethical reasons, four random animals were further investigated by numerous diagnostic methods. The impact of food and enclosure enrichment was assessed and observed over a 2-year period. Histopathology of four random tufted capuchin monkeys revealed lymphocytic perifolliculitis, with an appearance of a "swarm of bees" which was suggestive of alopecia areata. Etiological classification of pruritus excluded dermatological, systemic, and neurological causes, making it behavioral. Enclosure and food enrichment had a beneficial impact on pruritus (12/12) and alopecia (10/12). The findings were suggestive of alopecia areata, while the pruritus was considered behavioral in origin. Alopecia and pruritus improved upon enclosure and food enrichment.