Apparent digestibility and nutritional status of capuchin monkeys (Sapajus sp.) under human care.

BACKGROUND: Studing the nutritional needs and dietary habits of primates is essential to ensure their health and well-being. This includes the understanding of the use of nutrients and its correlation with health parameters. METHODS: Diet and nutritional parameters of 13 captive capuchin monkeys (Sapajus sp.) were assesed. Apparent digestibility of dry matter and nutrients were evaluated. Nutritional status was established based on body condition score (BCS) and muscle mass score (MMS). RESULTS: High apparent digestibility coefficients (ADC) were observed for crude protein and ether extract, but low for minerals and crude fiber. The ADC of EE and CF were related to MMS, and the biochemical parameters did not correlate with the AD coefficients obtained in the group. The nutritional status of the animals remained inadequate in 84.6% of the individuals, suggesting a reformulation of the diet and nutritional management.

Molecular detection of Sarcocystis sp. in a kept under human care black capuchin monkey (Sapajus nigritus., Goldfuss 1809) with necrotizing encephalitis.

A senile male black capuchin monkey (Sapajus nigritus) kept under human care in a Zoo was found dead after 2 weeks presenting signals of weight loss and hyporexia. Histopathological revealed a necrotizing encephalitis. Although it was not observed microscopically, Sarcocystis sp infection was detected in brain tissue from molecular assays. These infections have been rarely described in neotropical primates, particularly associated with tissue lesions.

Guidelines and considerations for capturing and collaring wild primates: a case study with capuchin monkeys (Sapajus nigritus cucullatus).

Many aspects of the ecology, evolution and social behavior of wild-living primates remain un-explored and require further investigation. While long-term field studies are crucial for addressing conservation concerns for many primates' species, acquiring the necessary data is often challenging, often due to difficulties in locating study groups. Radio-telemetry has significantly facilitated the study of primates and other animals living in tropical forests. However, there are important practical challenges in the process of capturing and releasing animals after placement of telemetry collars. In this study, we report guidelines and considerations for capturing and collaring wild capuchin monkeys, Sapajus nigritus cucullatus, in the Atlantic Forest of Argentina. Our ultimate goal is to contribute to making captures safer, preventing harm and stress to animals when using radio-telemetry in monitoring strategies for conservation of this primate species. These methods can be useful for researchers using field capture and radio-telemetry for monitoring groups or populations of wild primates, specifically wild Sapajus.

Radiographic measurements of the hind limbs in capuchin monkeys (Sapajus spp.).

BACKGROUND: Radiographic measurements are a useful tool to assess skeletal health and development in primates. This study aimed to perform radiographic measurements of hind limbs in capuchin monkeys. METHODS: Twelve Sapajus spp. were used; ten adults and two sub-adults, nine females and three males. RESULTS AND CONCLUSIONS: The pelvimetry showed that the pelvic inlet area presented mean values of 7.63, 10.23, and 5.43 cm2 for adult males, adult females, and sub-adult females, respectively. The mean inclination angle was 129.45° and the mean values for the mechanical lateral proximal and distal femoral angles were 102.32° and 90.93°, respectively. The mean values for the anatomic lateral proximal and distal femoral angles were 104.59° and 85.98°, respectively. In conclusion, the radiographic measurements proved feasible for hind limb evaluation in Sapajus spp. and can be used for comparison with animals presenting orthopedic lesions.

Anesthetic effects of isoflurane and fentanyl infusion in capuchin monkeys (Sapajus sp) undergoing salpingectomy or deferentectomy, previously chemically restrained with ketamine-midazolam or ketamine-dexmedetomidine.

BACKGROUND: This study evaluated the anesthetic and cardiorespiratory effects of two anesthetic protocols for salpingectomy or deferentectomy in capuchin monkeys (Sapajus sp). MATERIALS AND METHODS: Five capuchin monkeys (5 per group) received ketamine (20 mg/kg) combined with midazolam (0.5 mg/kg; group KM) or dexmedetomidine (5 µg/kg; group KD) intramuscularly. Anesthesia is induced with propofol intravenously and maintained with isoflurane. Before the start of surgery, fentanyl 3 µg/kg was administered IV, and continuous infusion (10 µg/kg/min) IV was started. Times and quality of anesthetic recovery were evaluated postoperatively. RESULTS: KM and KD resulted in adequate chemical restraint. KD resulted in bradycardia. Intraoperative heart rate and systolic blood pressure were higher in KM than in KD. Both groups had smooth recovery. Time to standing was longer in KM than in KD. CONCLUSION: Both protocols allowed the performance of surgeries, with few cardiorespiratory effects. Anesthetic recovery was smooth and shorter in KD group.

Climate change effects on the distribution of yellow-breasted capuchin monkey (Sapajus xanthosternos (Wied-Neuwied, 1826)).

The magnitude of recent climatic changes has no historical precedent and impacts biodiversity. Climatic changes may displace suitable habitats (areas with suitable climates), leading to global biodiversity decline. Primates are among the most affected groups. Most primates depend on forests and contribute to their maintenance. We evaluated the potential effects of climatic change on the distribution of Sapajus xanthosternos, a critically endangered primate whose geographical range encompasses three Brazilian biomes. We evaluated changes between baseline (1970-2000) and future (2081-2100) climates using multivariate analysis. Then, we compared current and future (2100) climatic suitability projections for the species. The climatic changes predicted throughout the S. xanthosternos range differed mostly longitudinally, with higher temperature increases in the west and higher precipitation reductions in the east. Climatic suitability for S. xanthosternos is predicted to decline in the future. Areas with highest current climatic suitability occur as a narrow strip in the eastern part of the geographic range throughout the latitudinal range. In the future, areas with highest values are projected to be located as an even narrower strip in the eastern part of the geographical range. A small portion of forest remnants larger than 150 ha located in the east has larger current and future suitability values. At this large scale, the spatial heterogeneity of the climate effects reinforce the importance of maintenance of current populations in different areas of the range. The possibility that phenotypic plasticity helps primates cope with reduced climatic suitability may be mediated by habitat availability, quality, and connectivity.

State-dependent risky choices in primates: Variation in energy budget does not affect tufted capuchin monkeys' (Sapajus spp.) risky choices.

Economic models predict that rational decision makers' choices between a constant, "safe" option and a variable, "risky" option leading, on average, to the same payoff, should be random. However, a wealth of research has revealed that, when faced with risky decisions, both human and nonhuman animals deviate from economic rationality. According to the risk-sensitivity theory, individuals should prefer a safe option when they are in a positive energy state and a risky option when they are in a negative energy state. The abundance/risk hypothesis proposes that individuals should prefer risky options when diet quality exceeds their nutritional requirements. We tested how energy budget affects decision making under risk by presenting 22 capuchins belonging to two colonies (IT: N = 12, US: N = 10) with a risky choice task. Capuchins had to choose between a constant option (always four food items) and a variable option (one or seven food items with a 50% probability) in two conditions. In the Low-energy condition capuchins were tested before their main meal, whereas in the High-energy condition they were tested following a high-caloric meal. In neither colony did we find a significant difference between conditions, suggesting that the energy budget did not affect risk preferences. However, we found differences between colonies in their general response to risky choices: US capuchins were more risk-prone after selecting a safe option than a risky option and after selecting a bad (one food item) than a good (seven food items) risky option, whereas this did not hold true in IT capuchins. Furthermore, in the IT colony, males were more risk-prone under the High-energy condition compared to the Low-energy condition. Subtle differences in individual characteristics, management conditions, or stochastic founder effects may be implied, with relevant consequences for the outcomes of research on risky decision-making across laboratories.

Planning actions with a magnetic tool: how initial tool orientation and number of functional ends influence motor planning abilities in capuchin monkeys (Sapajus spp.).

The way in which animals grasp objects to perform subsequent action execution allows studying their anticipatory abilities. We examined whether 11 capuchin monkeys (Sapajus spp.) were able to prospectively grasp a magnetic dowel to use it as a tool to retrieve a baited metallic container from a plexiglas box placed in front of them. We investigated whether and how initial dowel orientation (horizontal vs vertical) affected grasping and using the dowel to retrieve the container in two testing conditions: (1) 2-FE condition in which the dowel had two functional magnetic ends; (2) 1-FE condition in which the dowel had only one functional magnetic end. In the 2-FE condition, capuchins had to take into account the initial dowel orientation since both ends were functional, whereas in the 1-FE condition capuchins had also to take into account the initial functional end position when grasping the dowel. Capuchins were trained to grasp the dowel to put one functional end in contact with the metallic container. However, they did not learn to associate the functional end of the 1-FE dowel to successful retrieval. Capuchins showed better anticipatory planning (1) in 2-FE than in 1-FE condition and (2) when the dowel was initially positioned on the horizontal plane than on the vertical one. Moreover, hand preferences affected planning in the 1-FE condition. Results were discussed within the frameworks of primates' abilities to use abstract cues and on their abilities to process functional features and spatial cues and to perform mental rotations.

Spontaneous disseminated T-cell lymphoma in a buff-headed capuchin (Sapajus xanthosternos).

Reports of spontaneous hematopoietic neoplasms in Platyrrhines species are scarce. We present the gross, histological, and immunohistochemical findings of disseminated T-cell lymphoma in a male 25-year-old Sapajus xanthosternos kept in a Brazilian conservation center. No molecular evidence of betaherpesvirus or gammaherpesvirus was associated with the occurrence of this neoplasm.

Identification and evolutionary analysis of papillomavirus sequences in New World monkeys (genera Sapajus and Alouatta) from Argentina.

OBJECTIVE: In this study, we investigated the occurrence of papillomavirus (PV) infection in non-human primates (NHPs) in northeastern Argentina. We also explored their evolutionary history and evaluated the co-speciation hypothesis in the context of primate evolution. METHODS: We obtained DNA samples from 57 individuals belonging to wild and captive populations of Alouatta caraya, Sapajus nigritus, and Sapajus cay. We assessed PV infection by PCR amplification with the CUT primer system and sequencing of 337 bp (112 amino acids) of the L1 gene. The viral sequences were analyzed by phylogenetic and Bayesian coalescence methods to estimate the time to the most common recent ancestor (tMRCA) using BEAST, v1.4.8 software. We evaluated viral/host tree congruence with TreeMap v3.0. RESULTS: We identified two novel putative PV sequences of the genus Gammapapillomavirus in Sapajus spp. and Alouatta caraya (SPV1 and AcPV1, respectively). The tMRCA of SPV1 was estimated to be 11,941,682 years before present (ybp), and that of AcPV1 was 46,638,071 ybp, both before the coalescence times of their hosts (6.4 million years ago [MYA] and 6.8 MYA, respectively). Based on the comparison of primate and viral phylogenies, we found that the PV tree was no more congruent with the host tree than a random tree would be (P > 0.05), thus allowing us to reject the model of virus-host coevolution. CONCLUSION: This study presents the first evidence of PV infection in platyrrhine species from Argentina, expands the range of described hosts for these viruses, and suggests new scenarios for their origin and dispersal.

Metabolomic Profiling of Phloem Sap from Different Pine Species and Implications on Black Capuchin.

In most commercial pine farms in southern Brazil, black capuchin causes damage to wood and financial losses when it removes bark from some pine species to feed upon underlying vascular tissues. Therefore, this study aimed to evaluate the variability of the primary metabolites of phloem saps from 10 different species of pine by NMR spectroscopy, as well as the aroma compounds using SPME-GC-MS. Each technique provided a different set of metabolites that we can correlate to monkey predilection. The PCA showed monosaccharide (detected by NMR) and α-pinene (pine-like and resinous flavor descriptors) as attractive compounds for monkeys. On the other hand, the low content of monosaccharide and the high content of ß-phellandrene (citrus odor descriptor) was observed in less attacked pine species (P. patula). The data fusion on primary metabolites and aroma compounds corroborated the individual analyses, complementing the comprehension of the monkey predilection. Thus, P. elliottii was an avoided tree even with high content of sugars possibly due to its high content of ß-phellandrene (citrus odor). The results are useful for further behavioral studies to determine the role that each highlighted metabolite plays in chemically mediated animal-plant interactions.

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.

Dominance and social interaction patterns in brown capuchin monkey (Cebus [Sapajus] apella) social networks.

Strong, stable social bonds in primates are characterized by high levels of social affiliation, low levels of aggression, minimal stress, and affiliative reciprocity within the dyad. In relatively well-studied catarrhine monkeys, these bonds tend to form most frequently between kin, animals close in age, and animals close in rank. This results in patterns of affiliation in which kin, similarly aged animals, and like-ranked animals tend to affiliate and patterns of aggression and submission where animals tend to aggress more toward nonkin and closely ranked animals, and submit more toward distantly ranked animals. However, literature on how affiliative and agonistic relationships are organized in platyrrhine primate species like brown capuchin monkeys is limited and conflicting. In this study, we used social network analyses to characterize how age, sex, maternal kinship, and dominance rank relate to the patterns of submissive, aggressive, contact, and grooming interactions in a group of captive brown capuchin monkeys. Like catarrhine monkeys, brown capuchin monkeys showed a steep linear dominance hierarchy, tended to affiliate with kin, similarly aged animals, and like-ranked animals, and tended to aggress more toward nonkin. However, our monkeys showed a pattern of affiliation and grooming down the hierarchy that is inconsistent with grooming up the hierarchy patterns often seen in catarrhine monkey groups, suggesting that brown capuchins do not compete for access to higher ranking social partners. Higher ranking monkeys were most central to the aggression network, and lower ranking monkeys were most central to the submission network. Mid-ranking monkeys were the most central to the contact network, suggesting that they may play an important role in the affiliative cohesion of the group. These results inform our understanding of brown capuchin social behavior specifically, and of how demographic factors relate to social organization in platyrrhine primates generally.

Urine washing in urban robust capuchin monkeys (Sapajus sp.): The relation with visitors.

In primates, urine washing (UW) is a behavior in which individuals intentionally deposit urine on their bodies. Social and nonsocial hypotheses have been proposed to explain the adaptive function of this behavior. For capuchins, different functions have been assigned for UW, suggesting it as a flexible behavior, but studies have been mainly in captivity. However, no investigations have been performed in urban environments, where these animals can modify their behavior. Our goal was to study UW in a semi-provisioned group of an introduced unknown robust capuchin species (Sapajus sp.) living in a tiny urban fragment in Foz do Iguaçu, Brazil, where they have contact with humans. We assessed the influence of social (sexual, agonistic, and anointing behaviors) and environmental (temperature, relative air humidity, height of the monkeys in the trees, number of people present in the fragment, and human-monkey interactions) variables, the influence of behavior before and after UW, and the influence of sex-age classes, on the frequency of UW. We observed 75 records of UW in 300 h of observations, where urine was mostly deposited on hands and passed on to feet (95%). There were no significant differences in the frequency of the behavior between sex-age classes nor in the behaviors before and after UW. Around 50% of UW took place in the late morning and we found no correlation between UW and temperature, relative air humidity, nor the heights of the monkeys in the trees. However, we found a significant association between UW and the daily number of people in the fragment, but not between UW and human-monkey interactions, anointing, agonisms, and sexual behavior. Our study increases the scope of UW flexibility by identifying the presence of visitors affecting the occurrence of this behavior. We discussed different possibilities through which people could influence the capuchins to display UW.

Diet diversity and seasonality of robust capuchins (Sapajus sp.) in a tiny urban forest.

Capuchins are omnivorous neotropical primates that can survive in urban forests by supplementing their diet with human foods. However, few studies have analyzed the impact of these resources on their diet diversity and feeding seasonality. We aimed to assess the patterns of foraging, feeding, and diet diversity of urban capuchins (Sapajus sp.) that live in a tiny urban forest in Foz do Iguaçu, Brazil, where humans frequently feed them. We predicted that forest degradation and human foods could decrease diet diversity, though capuchins may, conversely, reduce their selectivity and expand their food repertoire. We followed the animals from dawn to dusk between May 2018 and April 2019 to list and quantify the species and items consumed. We used diversity indexes and cluster analysis to understand similarities and differences in the diet composition over the study period. We recorded 58 plant species (being 14 exotics) consumed by the monkeys, and nonconventional items, with low diet diversity overall. The diet consisted mainly of plants (69.8%), animal matter (20.6%), and processed foods (9.5%). Capuchins consumed more food from the anthropic environment (57.5%) than from the forest (42.4%), while their food from the forest included more invertebrates (47.8%) than fruits (40%). The cluster analysis showed two main groups of feeding months, in accordance with the seasons of high and low food production in local forests. Monkeys did not vary the frequencies of foraging or feeding between seasons, probably due to the omnipresent availability of human foods. Despite the high consumption of human foods, capuchins responded to the seasonality of the forest, expanding their feeding diversity in the drier period. Future studies should analyze the correspondence between food consumption and local phenology, as well as the potential role of capuchins as seed dispersers in this depauperate community.

Size reduction and skull shape parallelism following the evolutionary forest-to-savanna transition in Platyrrhini monkeys.

There are strong physiological and behavioral differences that allow animals to live in forests versus savannas. For example, terrestrial forest-dwelling mammals tend to be small compared to species living in savannas. Robust capuchin monkeys (genus Sapajus) are widespread in tropical South America, occurring in both forest and savanna environments, with forest species considered basal in an evolutionary context. Whether or not skull shape and size variations are associated with variation in resource use remains unknown, particularly for the two species living in savanna (Sapajus libidinosus and S. cay). Here we show that savanna species present convergent size and skull characteristics that may facilitate living in this new environment. Geometric morphometric methods were used to assess skull size and shape variation for 184 Sapajus specimens distributed across South America. We used phylogenetic generalized least squares to test size against environmental variables and multivariate morphological trajectories/partial least square analyses on the skull shape to detect shape differences in specimens between forest and savanna biomes. Our findings reveal Sapajus size reduction in the evolutionary transition from forest to savanna, a process related to increasing seasonality. Moreover, we found morphological parallelism in the skull (e.g., muzzle shortening) and (large) molars in the two savanna species, features that may facilitate the processing of harder food such as fallback resources. We associate these phenotypic differences to the evolutionary process of colonizing the savannas by primates (including early hominins), leading to morphological adaptations to tolerate stressful, seasonal environments, such as body size reduction and ingestion and mastication of tough foods.

Demographic changes in an Atlantic Forest primate community following a yellow fever outbreak.

We investigated demographic changes in three primate species (Alouatta guariba, Sapajus nigritus, and Callithrix flaviceps) at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala, Caratinga, Minas Gerais, Brazil, following a yellow fever outbreak (YFO) by comparing their population sizes before (2015) and after the outbreak (2017-2018), and by monitoring the size, composition, and reproductive status of groups from 2017 to 2021. Comparisons of pre- and post-YFO census data indicate the A. guariba population declined by 86.6%, from an estimated minimum of 522 individuals to 70 individuals. However, by October 2021, the population had grown to at least 86 individuals, with an adult sex ratio (N = 53) that was female-biased (0.61). Eleven of the 13 groups being monitored systematically were reproductively active with high survivorship to 12 months of age. S. nigritus declined by 40%, from 377 to 226 individuals. The sex ratio of 33 adult S. nigritus is also female-biased (0.71), and at least 8 of 15 groups being monitored are reproductively active. C. flaviceps declined by 80%, from 85 individuals to the 15-17 individuals observed from 2017 to 2021. The female-biased adult sex ratio and presence of infants and juveniles in the A. guariba and S. nigritus groups are encouraging signs, but there is still great concern, especially for C. flaviceps. Continued monitoring of the demographics of these primates is needed as their persistence appears to still be at risk.

Comparative anatomy of the brachial plexus and shoulder nerves of the Sapajus.

BACKGROUND: The capuchin is a neotropical primate that presents easy reproduction in captivity and is used in scientific research. The objective of this work was to describe the structure and the branching pattern of the brachial plexus of the capuchin and to compare the results with data from the literature for humans, chimpanzees, baboons and Callithrix. METHODS: Twelve specimens were used: eight males and four females. No animals were killed for the purpose of this study. RESULTS: The brachial plexus of Sapajus sp was constituted mainly from the ventral roots of the last four cervical spinal nerves, from C5 to C8, mainly, and the first thoracic nerve (T1). CONCLUSIONS: The pattern of formation of the brachial plexus of the capuchin monkey was more similar to that of Callithrix and baboons, perhaps because they are the only primates in this study to be essentially quadrupedal.

Differences among the forelimb arteries in groups of primates and a mathematical model explanation.

BACKGROUND: Recently, some studies about primates have claimed the importance of the vessels to maintain the muscles working; in fact, the arterial supply could suggest how strenuous the muscular performance is associated to locomotor behavior. The aim of this work was to study the anatomy of the arteries of the forelimbs of different groups of primates to evidence a general arterial model in comparative terms. METHODS: We propose a biophysical explanation for the arterial pattern of the forelimbs of primates' groups. RESULTS: Three pattern of the forelimb arteries in Primates were descript and the differences were explained using mathematical formulas. CONCLUSIONS: The anatomical study about the comparative anatomy of the arteries of the forelimbs of primates provided hypothesis about the three observed models, mainly in relation to brachial artery division and the number of the palmar arches, in mathematical models' terms.

Serological survey and DNA screening of Leptospira spp. in free-living adult tufted capuchin monkeys (Cebus apella nigritus) in a forest reserve Southeast São Paulo State, Brazil.

BACKGROUND: Leptospirosis is an important anthropozoonosis. The study investigated the presence of anti-Leptospira antibodies and detection of Leptospira spp DNA in the urine as well as the biochemical profile in Neotropical wild primates living in a forest reserve from Southeast São Paulo State, Brazil. METHODS: Blood samples were obtained from 50 adult tufted capuchin monkeys (Cebus apella nigritus). Urine samples were obtained only from male primates. The screening for antibodies against Leptospira spp was evaluated by microscopic agglutination test (MAT). Leptospira DNA in the urine was evaluated by polymerase chain reaction (PCR) considering the target gene LipL32. Biochemical profile was evaluated by using a spectrophotometer. RESULTS: The MAT results included 39 (78%) serum reactive animals with the proportions of 28/39 males and 11/39 females. The most frequent reactive serogroups were Icterohemorrhagiae, Canicola, and Autumnalis. All urine samples were negative for leptospiral DNA. There were no significant differences between sexes for aspartate aminotransferase (AST) and alkaline phosphatase values, but alanine aminotransferase (ALT), creatinine, glucose, and urea were significantly higher in males. CONCLUSIONS: Tufted capuchin monkeys were sera reactive against leptospirosis. Prevalence was similar for the 2 sexes. Leptospiral DNA was not detected in the urine of sera reactive primates tested by the MAT method. ALT, creatinine, glucose, and urea values were higher in male animals.