Diet and seed dispersal of bearded capuchin monkeys (Sapajus libidinosus) in Brasilia National Park.

The dietary ecology of a species can provide information on habitat requirements, food resources, and trophic interactions, important to guide conservation efforts of wildlife populations in endangered habitats. In this study, we investigated the dietary ecology of bearded capuchin monkeys (Sapajus libidinosus) in Brasilia National Park, in the endangered Cerrado biome of central Brazil. To obtain diet composition and evaluate the role of these primates as seed dispersers of local tree species, fecal sample collections and feeding observations were performed for a 7-month period. To determine whether seeds germinated better after passing through a primate gut, we conducted germination trials with (i) pulped seeds from trees, (ii) depulped seeds from trees, (iii) seeds from feces planted with feces, and (iv) seeds from feces planted without feces. During experimental procedures, 7308 seeds from 8 families and 10 species were planted. We found that S. libidinosus spent more time feeding on fruits than on any other food item and the diet consisted of 33 plant species from 21 families. However, 20% of their diet consisted of anthropic food. Most seeds planted with feces germinated faster compared to seeds in other experimental treatments, suggesting that passing through the gut and being deposited with fecal material is advantageous. The bearded capuchins also defecated many medium- (5 species) and large-sized (2 species) seeds that may be inaccessible to smaller arboreal frugivores. The results obtained emphasize the important role of bearded capuchins as seed dispersers for the maintenance and conservation of the endangered Cerrado biome.

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 quantified in vivo bite forces and gapes across ontogeny and examined these data in relation to body mass and cranial measurements in captive tufted capuchins, Sapajus spp. Bite force and gape were also compared across geometric and mechanical properties of mechanically challenging foods to investigate relationships between bite force, gape 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 with 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.

Homosexual Courtship in Young Wild Capuchin Monkeys: A Case Study.

In primates, many species exhibit same-sex sexual behaviors (SSB), defined as "genital contact or genital manipulation between same-sex individuals." Several sociosexual functions have been proposed, including proceptivity enhancement, receptivity reduction, dominance assertion, practice for heterosexual copulation, tension regulation, reconciliation, and alliance formation. Capuchin monkeys are known for their rich and flexible sexual behavioral repertoire and elaborated courtships. At present, the few reports of SSB in capuchin monkeys (genera Sapajus and Cebus) focused on mounting. Here, we describe the case observed in a population of wild yellow-breasted capuchin monkeys (Sapajus xanthosternos) in which two young males, aged 5-6 years and 19 months, performed a 15-min uninterrupted sequence of courtship behaviors and mounting. Comparing with a previously established ethogram of 20 behaviors typical for heterosexual behavior of tufted capuchins, we show that these males performed 16 of them. Thus, SSBs are already present in the repertoire of young individuals and the practice may serve to create or strengthen bonds. Although same-sex mounting and genital inspection are common in capuchins' play and other social interactions, the almost entire array of courtship behaviors has never been observed in youngsters. Additionally, this example supports the notion that primate (homo)sexual behavior is not limited to genitalia and copulation, since the observed courtship included diverse behaviors different from genital contact. Thus, we propose a broader definition of sexual behavior.

Observation of Masturbation After Visual Sexual Stimuli From Conspecifics in a Captive Male Bearded Capuchin (Sapajus libidinosus).

Masturbation is part of the natural behavioral repertoire of primates, with visual sexual stimuli known to trigger this behavior. Here, we report masturbation events triggered by visual sexual stimulus (VSS) in the South American primate Sapajus libidinosus. We observed a multi-male multi-female captive colony of 17 bearded capuchins between January and October 2014. Over this period, we registered 11 copulation events, 68 attempt copulations, and five masturbation events. The same low-ranking male (named Fu) performed all masturbation events. Fu directly looked at other individuals engaged in sexual displays while he masturbated in three events. The masturbation events associated with VSS lasted up to 2 min and 40 s. Our observations show that VSS can trigger masturbation in capuchin monkeys. The low hierarchy rank of the male, and the consequent lack of mating opportunities in the multi-male multi-female recently formed group in captivity, may have prompted the masturbation events.

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.

Pathological findings associated with Dipetalonema spp. (Spirurida, Onchocercidae) infection in two species of Neotropical monkeys from Brazil.

Among vector-borne helminths, filarioids of the genus Dipetalonema (Spirurida: Onchocercidae) localize in several tissues and body cavities of several animal species, causing mild to moderate lesions. The pathological findings associated with Dipetalonema spp. infection in Neotropical monkeys from southern Brazil are herein described, along with a fatal case due to filarial polyserositis and entrapment of an intestinal segment. At necropsy, nematodes were observed in abdominal and thoracic cavities, or in the pericardium of 37 (31.3%) out of the 118 individuals examined (i.e., 35 Alouatta guariba clamitans and two Sapajus nigritus). In addition, at histology, 27.0% of positive animals presented microfilarie (inside blood vessels of lung, spleen, liver, and brain) and 8.1% presented adult nematodes in the heart, lung, and liver. In two cases, cross-sections of filarioids were associated with areas of epicardial thickening with intense fibrosis and pyogranulomatous inflammation in the brain, heart, liver, lungs, or spleen. The DNA fragment was amplify using the cox1 gene, sequenced and analyzed to identify the nematode species collected; presence of Wolbachia was assessed in the filarioids using the 16S rRNA gene. At BLAST analysis of the cox1 gene, 10 sequences showed 91.7% nucleotide identity with Dipetalonema gracile, and two with D. gracile (98.5%) and Dipetalonema graciliformis (98.3%). Phylogenetic analyses clustered sequences of the cox1 obtained in this study in two clades corresponding with the host species. Wolbachia sp. endosymbiont was detected in four samples. Data herein reported provide a description of pathological lesions associated with the infection by Dipetalonema spp., suggesting that they may cause disease in Neotropical monkeys. In addition, a better understanding of diversity and biology of Dipetalonema spp. in South America is needed to assess the impact they may cause in native non-human primates from Brazil.

Antimicrobial resistance profile of gram-positive isolates belonging to the microbiota of non-human primates.

BACKGROUND: The aim of this work was to identify gram-positive bacteria and their respective resistance profiles of free-living capuchin monkeys. METHODS: For this, 15 Sapajus nigritus were captured in a municipal urban park in the northern region of the state of Paraná, Brazil, and under pharmacological restraint, samples were collected with sterile swabs from the oral, rectal, ocular, nasal, and auricular regions. After isolation of the 22 gram-positive bacteria, each isolate was subjected to the catalase and coagulase tests for presumptive identification. Subsequently, phenotypic tests for bacterial resistance were performed using the agar diffusion disc method. The samples resistant to oxacillin were submitted to the PCR technique to search for the mecA gene. RESULTS: Of the 22 gram-positive cocci of these two (9.09%) are Streptococcus spp. and twenty (90.91%) Staphylococcus spp. Among Staphylococcus spp. three (13.64%) were coagulate-negative (CoNS) and seventeen (86.36%) coagulate-positive (CoPS). Of the antimicrobials tested, enrofloxacin had the best performance, with only one (04.54%) isolate resistant to it, on the other hand, the antimicrobials with the lowest performance were cefotaxime and penicillin with 19 (82.36%) and 18 (81.81%) resistant isolates, respectively. Only five isolates had MAR less than 0.2, being one ocular, one oral, and three nasal, they had multiple resistance index varied between 0.07 and 0.92, with an average of 0.45 and a mode of 0.3. Among the samples with the highest resistance index, a positive coagulase Staphylococcus stood out, being intermediate to gentamicin and resistant to other antibiotics and an intermediate streptococcus to gentamicin, enrofloxacin, and resistant to other antibiotics. No sample was positive to mecA gene. CONCLUSIONS: Future studies should be conducted to identify the Staphylococcus species, the high rate of antimicrobial resistance of the monkeys in this study suggests that Grooming's behavior may be contributing to the sharing of the resistant microorganism among the members of this group of primates.

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.

Facial malformations, including cleft lip and palate, in wild primates in Paraguay.

Nine individual Alouatta caraya and Sapajus cay displaying facial malformations were observed across three sites in Paraguay. Six had cleft lip (with or without cleft palate), and three had malformations of the lower lip. This is the first record of cleft lip and/or palate in the genus Alouatta.

Grooming site preferences in black capuchin monkeys: Hygienic vs. social functions revisited.

When primates groom each other, they tend to concentrate on those parts of the body they cannot efficiently self-groom (i.e., not visually accessible), and prefer to intensify grooming in areas with high hair density, thus suggesting a hygienic function. However, preferences for some body sites over others during social grooming may also result from different degrees of social bonding and relative dominance. To assess the relative importance of physical (hygienic) and social factors, we examined grooming interactions in two groups of wild black capuchin monkeys (Sapajus nigritus) during 15 nonconsecutive months. We evaluated the distribution of social grooming across body sites according to their accessibility by self-grooming and hair density. At the same time, we assessed whether the degree of dyadic social bonding affects the relative body orientation between groomer and groomee and the access to vulnerable body sites (e.g., face, throat, groin) during grooming. As expected, capuchins preferentially groomed inaccessible body sites (e.g., back and head), with a disproportionate effort directed to the tufts of their partners. We found that dyadic social bond strength, together with rank distance, significantly affected the proportion of grooming in ventro-ventral body relative orientation only in dominant-subordinate groomer-groomee dyads. This may indicate that, when two individuals differ in rank but are strongly bonded, the level of uncertainty related to the social context is already resolved and thus grooming per se is no longer perceived by the subordinate as an uncertain/risky situation. We found no effect of social bonding on grooming vulnerable body sites for any type of dyad. Our findings suggest that grooming site preferences in black capuchin monkeys simultaneously reflect hygienic and social functions.

Against all odds: Numerical assessment by tufted capuchin monkeys.

When competitors are able to assess the asymmetry in the resource holding potential before interacting, individuals or groups should avoid interacting with stronger opponents, thereby avoiding the energy costs and risk of injury associated with aggressive intergroup encounters. Thus, escalated aggression is expected only between closely matched competitors. Among Argentine tufted capuchin monkeys (Sapajus nigritus), intergroup dominance is decided by the asymmetry in male group size. Using playback experiments, I simulated intergroup encounters with neighboring groups, manipulating both the apparent numerical asymmetry and the resource context. During experimental trials, I recorded the approach behavior of the focal individual, as well as changes in neighbor density and individual travel speed following the presentation of the playback stimulus, to assess whether individual willingness to participate in resource defense was affected by the probability of winning the encounter. In spite of the competitive disadvantage, neither males nor females showed a decreased probability of approach when the numerical odds strongly favored the opposing group. Instead decisions regarding whether to participate appear to be driven primarily by the resource context. Nevertheless, changes in individual behavior during approaches suggest that tufted capuchin monkeys are sensitive to the relative odds. Individuals accelerated less when approaching a larger group, although no changes in neighbor density were apparent. The absence of an effect of the numerical asymmetry on willingness to approach the playback speaker suggests that subordinate groups benefit from engaging in intergroup aggression with larger neighbors, despite the high probability of losing. These encounters may serve to assess the current subjective resource valuation of the neighboring group or limit territorial expansion by large groups by decreasing the marginal value of home range exclusivity. Because these encounters are riskier, however, individuals appear to alter their approaches, becoming more tentative as the numerical odds increasingly favor the opposing group.

A longitudinal assessment of behavioral development in wild capuchins: Personality is not established in the first 3 years.

Animal personality is defined as consistent individual differences across time and situations, but little is known about how or when those differences are established during development. Likewise, several studies described the personality structure of adult capuchin monkeys, without assessing the ontogeny of these personality traits. We analyzed the behavioral repertoire of 12 wild infants (9 males, 3 females) yellow-breasted capuchin monkeys (Sapajus xanthosternos), in Una Biological Reserve (Bahia, Brazil). Each infant was observed and filmed weekly from birth until 36 months, through daily focal sampling. We analyzed the behavior of each individual in 10 developmental points. By means of component reduction (principal component analysis), we obtained four behavioral traits: Sociability, Anxiety, Openness, and Activity. We investigated whether there were developmental effects on those traits by fitting regression models for the effect of time on behavioral traits, controlling for monkey identity, sex, and cohort. Sociability (decreasing) and Anxiety (increasing) changed significantly along development. By means of repeatability analysis, we did not find intra-individual consistency across time in those traits, so we cannot discriminate stable personality traits in early ontogeny. Our results show that the personality structure of capuchin monkeys is not established during early development, in agreement with the literature on human personality.

Ultrasonographic appearance and measurement of abdominal structures in healthy Capuchin monkeys (Sapajus spp.).

BACKGROUND: Previous ultrasonographic studies of Sapajus apella to determine the normal anatomy and physiology are incomplete. The aim of this study was to determine normal ultrasonographic appearance and measurements of all abdominal organs and structures of interest. METHODS: Twelve adult monkeys were recruited considered healthy on the basis of history, physical examination, and general blood work. To avoid additional anesthesia, the ultrasonographic examinations were performed during routine screening, annually scheduled by the Unit of Cognitive Primatology & Primate Center, CNR-Rome, where the animals were housed. Ultrasound data were processed offline by two experienced ultrasonographers. RESULTS: Topography, morphology and echostructure were described for almost all organs and descriptive statistics were provided. CONCLUSION: To the author's knowledge, this is the most complete ultrasonographic study in Capuchin monkeys.

Manual skills for processing plant underground storage organs by wild bearded capuchins.

OBJECTIVES: Wild Sapajus libidinosus exploit underground storage organs (USOs) that require extraction and extensive processing before consumption. Since capuchin monkeys are small-sized extractive foragers that cannot perform forceful precision grips, we expected that: (a) they would use other body parts together with their hands, (b) older (and larger) capuchins would be more efficient than younger (and smaller) ones, and (c) capuchins would invest greater effort/time to exploit USOs than other foods. MATERIALS AND METHODS: We recorded 178 episodes of USO processing performed by 20 individuals. The behavior was videotaped and scored frame-by-frame. RESULTS: We identified six sequential stages of processing: Excavation, extraction, soil removal, transport, peeling, and fragmenting the inner tissues. Capuchins made frequent use of forceful hand postures and manipulation in which the hands were strongly supported by other body parts, principally the mouth. Older capuchins were more efficient than younger individuals in pulling the USOs out of the ground. Finally, exploiting USOs was time-consuming, lasting more than 4 min per item, on average. DISCUSSION: Despite having smaller body-mass and greater manual constraints than catarrhine extractive foragers, capuchins, even smaller individuals, mastered USO processing thanks to their behavioral flexibility and persistence. Our findings reveal that precision grips are not essential for forceful actions during complex food processing and that, unlike catarrhines, capuchins, especially adults, rarely use thumb opposition during forceful grasping of food. In contrast, extended sustained attention and varied manual behavior appear to be convergent features of platyrrhine and catarrhine extractive foragers.

A competitive drive? Same-sex attentional preferences in capuchins.

In primates, faces provide information about several characteristics of social significance, including age, physical health, and biological sex. However, despite a growing literature on face processing and visual attention in a number of primate species, preferences for same- or opposite-sex faces have not yet been examined. In the current study, we explore the role of conspecific sex on visual attention in two groups of capuchin monkeys. Subjects were shown a series of image pairs on a Tobii Pro TX300 eye tracker, each depicting an unfamiliar male and an unfamiliar female face. Given the behavioral evidence of mate choice in both sexes, we hypothesized that capuchins would preferentially attend to images of unfamiliar conspecifics of the opposite sex. Our alternative hypothesis was that capuchins would preferentially attend to same-sex individuals to assess potential competitors. Our results provide support for our alternative hypothesis. When comparing attention to each stimuli type across sexes, females spent significantly larger percentages of time than males looking at female photos, whereas males spent significantly larger percentages of time than females looking at male photos. Within each sex, females looked for significantly larger percentages of time to female versus male images. Males also looked for larger percentages of time to same-sex images, though not significantly. To our knowledge, these data are the first to demonstrate significant sex-biased attentional preferences in adult primates of any species, and suggest that, for capuchins, potential competitors garner more attention than potential mates. In addition, our findings have implications for studies of visual attention and face processing across the primate order, and suggest that researchers need to control for these demographic factors in their experimental designs.

Bearded capuchin monkeys use joint synergies to stabilize the hammer trajectory while cracking nuts in bipedal stance.

The transition from occasional to obligate bipedalism is a milestone in human evolution. However, because the fossil record is fragmentary and reconstructing behaviour from fossils is difficult, changes in the motor control strategies that accompanied this transition remain unknown. Quadrupedal primates that adopt a bipedal stance while using percussive tools provide a unique reference point to clarify one aspect of this transition, which is maintaining bipedal stance while handling massive objects. We found that while cracking nuts using massive stone hammers, wild bearded capuchin monkeys (Sapajus libidinosus) produce hammer trajectories with highly repeatable spatial profiles. Using an uncontrolled manifold analysis, we show that the monkeys used strong joint synergies to stabilize the hammer trajectory while lifting and lowering heavy hammers. The monkeys stringently controlled the motion of the foot. They controlled the motion of the lower arm and hand rather loosely, showing a greater variability across strikes. Overall, our findings indicate that while standing bipedally to lift and lower massive hammers, an arboreal quadrupedal primate must control motion in the joints of the lower body more stringently than motion in the joints of the upper body. Similar changes in the structure of motor variability required to accomplish this goal could have accompanied the evolutionary transition from occasional to obligate bipedalism in ancestral hominins.

Unique perceptuomotor control of stone hammers in wild monkeys.

We analysed the patterns of coordination of striking movement and perceptuomotor control of stone hammers in wild bearded capuchin monkeys, Sapajus libidinosus as they cracked open palm nut using hammers of different mass, a habitual behaviour in our study population. We aimed to determine why these monkeys cannot produce conchoidally fractured flakes as do contemporary human knappers or as did prehistoric hominin knappers. We found that the monkeys altered their patterns of coordination of movement to accommodate changes in hammer mass. By altering their patterns of coordination, the monkeys kept the strike's amplitude and the hammer's velocity at impact constant with respect to hammer mass. In doing so, the hammer's kinetic energy at impact-which determines the propagation of a fracture/crack in a nut-varied across hammers of different mass. The monkeys did not control the hammer's kinetic energy at impact, the key parameter a perceiver-actor should control while knapping stones. These findings support the hypothesis that the perceptuomotor control of stone hammers in wild bearded capuchin monkeys is inadequate to produce conchoidally fractured flakes by knapping stones, as do humans.

Age-related changes in the social behavior of tufted capuchin monkeys.

The effects of aging on the social behavior of nonhuman primates is little understood, especially in New World monkeys. We studied the members of a colony of tufted capuchin monkeys (Sapajus sp.) in order to evaluate age related changes in their social behavior. We conducted observations on 25 subjects aged 4-36 years, living in captive social groups. We found that affiliative interactions (grooming and proximity) decreased with age, and that grooming was increasingly directed to a single preferred partner. Manipulation of objects in the environment also decreased with age, while locomotion and aggression showed no change. Overall, these results concur with previous findings on both human and nonhuman primates, and cast doubts on interpretations of age associated changes in human social behavior that rely of uniquely human advanced cognitive capacities.

Do sexual calls in female black capuchin monkeys (Sapajus nigritus) vary with fertility? An acoustic analysis.

Females across a range of animal taxa produce vocalizations and signals uniquely associated with periods of mating. While such signals may ultimately function to increase female attractivity to males, conflicting findings challenge the extent to which these signals co-vary in accordance with the probability of conception. Female black capuchin monkeys (Sapajus nigritus) display an elaborate repertoire of both vocal and visual components as part of their socio-sexual behavior, and previous analyses have shown that the rates of production of visual, but not vocal, components provide graded information on female ovulation. It remains possible, however, that the acoustic parameters of these sexual calls, rather than their rate of productions, co-vary with female fertility. To test this, we analyzed structural and temporal call parameters from estrous calls and post-copulatory calls recorded over five consecutive mating seasons in 12 sexually mature females at Iguazú National Park, Argentina. Calls given during the fertile phase of the female ovarian cycle were compared with those given during the non-fertile phase, as determined by profiles of female reproductive hormones. Similarly, within the fertile phase, we tested whether temporal or spectral acoustic parameters of calls gradually change with the approach of ovulation. We did not find any significant relationship between call parameters and the two measures of female fertility in either female estrous calls or post-copulatory calls. However, some differences between pre- and post-copulatory calls were apparent. Overall, our results indicate that sexual calls in black capuchin females do not provide precise information about the timing of ovulation, but may allow listeners to make probabilistic inferences about whether copulations have taken place. This, combined with previous findings, suggests that females in our study may use signals in different modalities to convey information about their fertility and sexual behavior with varying degrees of precision.

Fragmentation dynamics and loss of area of potential occupancy within the distribution limits of the endangered crested capuchin monkey (Sapajus robustus).

Habitat loss is one of the main threats to biodiversity. Fragmentation resulting from this process may restrict available habitat for primates, limiting their persistence in a given region. In this study, we aimed to quantify deforestation and fragmentation by identifying forest remnants capable of maintaining populations of the endangered crested capuchin monkey (Sapajus robustus) within its distributional limits in the states of Bahia, Espírito Santo, and Minas Gerais, Brazil. We used Landsat images from 1985 to 2010 to generate three time-interval mosaics classified by natural and non-natural vegetation. We then calculated the size of the forest remnants and the distance of each fragment of natural vegetation to its nearest neighbor. Between the first (1985-1990) and second (1995-2000) mosaics there was a vegetation loss of 41.4%, and between the second and third (2005-2010) mosaics there was a natural vegetation gain of 1%. The third mosaic showed smaller and more isolated fragments in comparison to the first mosaic. Across the three periods, Bahia was the state with the highest rate of deforestation. While Espírito Santo had fewer identified forest remnants, it retained the most natural vegetation within these small fragments. The landscape within the currently recognized distributional limits of the crested capuchin monkey is dominated by agriculture and livestock. Both decreasing fragment size and increasing species isolation by distance between fragments can negatively affect primate populations, increasing their risk of extinction. Isolation makes it difficult for migration and recolonization events to occur. Therefore, habitat restoration should be prioritized to reduce isolation between populations. Our findings may serve as a resource for future conservation efforts and management of the crested capuchin monkey.