Wild capuchin monkeys use stones and sticks to access underground food.

Primates employ different tools and techniques to overcome the challenges of obtaining underground food resources. Humans and chimpanzees are known to tackle this problem with stick tools and one population of capuchin monkeys habitually uses stone tools. Although early hominids could have used stones as digging tools, we know little about when and how these could be useful. Here, we report a second primate population observed using stone tools and the first capuchin monkey population to habitually use the 'stick-probing' technique for obtaining underground resources. The bearded capuchin monkeys (Sapajus libidinosus) from Ubajara National Park, Brazil, use 'hands-only' and 'stone-digging' techniques for extracting underground storage organs and trapdoor spiders. Males also use 'stick-probing' and 'stone-stick' techniques for capturing trapdoor spiders. Tool use does not increase success in obtaining these resources. Stone-digging is less frequent in this population than in the only other known population that uses this technique. Females use stones in a lower proportion of their digging episodes than males in both populations. Ecological and cultural factors potentially influence technique choice and sex differences within and between populations. This population has a different pattern of underground food exploration using tools. Comparing this population with others and exploring the ecological and cultural factors under which capuchin monkeys employ different tools and techniques will allow us to better understand the pressures that may have shaped the evolution of those behaviors in primates.

Interactions with humans reduce the success of foraging for anthropogenic food by capuchin monkeys (Sapajus libidinosus) in Brasília National Park, Brazil.

The progressive growth of urban environments has increasingly forced populations of nonhuman primates to coexist with humans in many cities, which has resulted in problems such as behavioral alterations, conflicts with humans, and threats to the health of the monkeys, due to their consumption of anthropogenic foodstuffs. These anthropogenic foods, which are rich in calories, are the principal driver of the proximity between humans and primates, even though the acquisition of these foods tends to be risky for the monkeys and involve a variety of challenges derived from specific features of the urban environment. The present study evaluated the success/risk relationship of foraging for anthropogenic food by tufted capuchins (Sapajus libidinosus) in Brasília National Park. The data were analyzed using a binary logistic regression, with the backward-stepwise Wald method, to investigate the factors related to the foraging success of the capuchins, considering variables such as their sex and age, the type of approach and its context, and interactions with humans. The capuchins were influenced by the anthropogenic context, which affected their foraging strategies and diet. Interactions with humans reduced the success of foraging for anthropogenic foods. Conflicts between humans and the capuchins were common, especially in the context of access to food. The capuchins thus preferred to access feeding resources directly, probably due to the reduced human interference, which resulted in greater foraging success for unattended food brought by park visitors and the raiding of trash cans. Based on the observed behavior patterns, a number of measures can be proposed to mitigate these conflicts. These recommendations include not bringing food into areas frequented by the capuchins, not reacting to approaching animals, and removing all trash generated during a visit. A cleaning team dedicated to the maintenance of the visitation area free of anthropogenic waste is also be recommended.

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

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

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

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

Adult and juvenile bearded capuchin monkeys handle stone hammers differently during nut-cracking.

Wild bearded capuchin monkeys (Sapajus libidinosus) habitually use stone hammers to crack open palm nuts and seeds on anvils. This activity requires strength, balance, and precise movement of a large stone with respect to the item placed on an anvil. We explored how well young monkeys cope with these challenges by examining their behavior and the behavior of adults while they cracked palm nuts using a stone. Using video records, we compared actions of six juvenile (2-5 years) and six adult (7+ years) wild monkeys during their first 20 strikes with one unfamiliar ellipsoid, quartzite stone (540 g), and the outcomes of these strikes. Compared with adults, juveniles cracked fewer nuts, performed a more diverse set of exploratory actions, and less frequently placed one or both hands on top of the stone on the downward motion. Adults and juveniles displayed similar low frequencies of striking with a slanted trajectory, missing the nut, and losing control over the nut or stone after striking. These findings indicate that young monkeys control the trajectory of a stone adequately but that is not sufficient to crack nuts as effectively as adults do. Compared with juveniles, adults more quickly perceive how to grip the stone efficiently, and they are able to adjust their grip dynamically during the strike. Young monkeys develop expertise in the latter aspects of cracking nuts over the course of several years of regular practice, indicating that perceptual learning about these aspects of percussion occurs slowly. Juvenile and adult humans learning to use stones to crack nuts also master these features of cracking nuts very slowly.

Compound grips in tufted capuchin monkeys (Sapajus spp and Sapajus libidinosus).

An experimental study with captive individuals and study of video recordings of wild monkeys explored whether and how tufted capuchin monkeys use onehand to hold one or more objects with multiple grips (compound grips). A task designed to elicit compound grip was presented to five captive tufted capuchin monkeys (Sapajus spp). The monkeys held one to four balls in onehand and dropped the balls individually into a vertical tube. Multiple simple grips and independent digit movements enabled separate control of multiple objects in one hand. Monkeys always supported the wrist on the horizontal edge of the tube before releasing the ball. Increasing the number of balls decreased the likelihood that the monkeys managed the task. Wild bearded capuchins (Sapajus libidinosus) used compound grips spontaneously to store multiple food items. Compound grips have been described in macaques, gorillas, chimpanzees, and humans, and now in a New World primate. We predict that any primate species that exhibits precision grips and independent digit movement can perform compound grips. Our findings suggest many aspects of compound grip that await investigation.

Distinct perceptuomotor features of percussive tooling in humans (Homo sapiens) and wild bearded capuchin monkeys (Sapajus libidinosus).

Adjustment of percussive movements to match the energetic requirements of the task serves as an index of skill in stone-knapping and nut-cracking. In this study, we compared strike-by-strike adjustment of percussive movements in expert bearded capuchin monkeys (Sapajus libidinosus) and (novice and expert) humans cracking palm nuts (Astrocaryum spp.) using stone hammers of varying mass. The monkeys regulated each strike's amplitude and hammer's velocity at impact to a small degree based on the propagation of a fracture in the nut's shell but overall struck a nut with consistent kinetic energy for a given hammer. They showed the smallest movement variability across strikes among all groups. Novice humans took the most strikes to crack a nut among all groups. Expert humans took the fewest strikes among all groups while showing the largest variation in hammer's kinetic energy at impact and largest movement variability across strikes. Overall, our findings confirm that expert humans can adjust their strikes more precisely to meet variable task demands and are more efficient than monkeys or novice humans in cracking nuts, but the findings also show a surprising advantage for expert monkeys over novice humans. The monkeys' strategy of striking with consistent amplitude and velocity is advantageous when hammer mass is adequate to generate sufficient kinetic energy at impact and crack open a nut in few strikes without requiring fine adjustments, explaining why the monkeys are particularly attentive to a stone's mass when choosing it as a hammer. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Positional behavior and substrate use in wild adult bearded capuchin monkeys (Sapajus libidinosus).

Natural selection for positional behavior (posture and locomotion) has at least partially driven the evolution of anatomical form and function in the order Primates. Examination of bipedal behaviors associated with daily activity patterns, foraging, and terrestrial habitat use in nonhuman primates, particularly those that adopt bipedal postures and use bipedal locomotion, allows us to refine hypotheses concerning the evolution of bipedalism in humans. This study describes the positional behavior of wild bearded capuchins (Sapajus libidinosus), a species that is known for its use of terrestrial substrates and its habitual use of stones as tools. Here, we test the association of terrestrial substrate use with bipedal posture and locomotion, and the influence of sex (which co-varies with body mass in adults of this species) on positional behavior and substrate use. Behavior and location of 16 wild adult bearded capuchins from two groups were sampled systematically at 15 s intervals for 2 min periods for 1 year (10,244 samples). Despite their different body masses, adult males (average 3.5 kg) and females (average 2.1 kg) in this study did not differ substantially in their positional behaviors, postures, or use of substrates for particular activities. The monkeys used terrestrial substrates in 27% of samples. Bipedal postures and behaviors, while not a prominent feature of their behavior, occurred in different forms on the two substrates. The monkeys crouched bipedally in trees, but did not use other bipedal postures in trees. While on terrestrial substrates, they also crouched bipedally but occasionally stood upright and moved bipedally with orthograde posture. Bearded capuchin monkeys' behavior supports the suggestion from anatomical analysis that S. libidinosus is morphologically better adapted than its congeners to adopt orthograde postures.

How bearded capuchin monkeys (Sapajus libidinosus) prepare to use a stone to crack nuts.

Bearded capuchin monkeys crack nuts with naturally varying stone hammers, suggesting they may tune their grips and muscular forces to each stone. If so, they might use discrete actions on a stone before lifting and striking, and they would likely use these actions more frequently when the stone is larger and/or less familiar and/or when first initiating striking. We examined the behavior of (a) four monkeys (all proficient at cracking nuts) with two larger (1 kg) and two smaller (0.5 kg) stones, (b) 12 monkeys with one 1 kg stone, and (c) one monkey during its first 100 strikes with an initially unfamiliar 1 kg stone. Bearded capuchin monkeys used three discrete actions on the stone before striking, all more often with the larger stones than the smaller stones. We infer that the first discrete action (Spin) aided the monkey in determining where to grip the stone, the second (Flip) allowed it to position the stone on the anvil ergonomically before lifting it, and the third (Preparatory Lift) readied the monkey for the strenuous lifting action. The monkey that provided 100 strikes with one initially unfamiliar stone performed fewer Spins in later strikes but performed Flip and Preparatory Lift at consistent rates. The monkeys gripped the stone with both hands along the sides to lift it, but usually moved one or both hands to the top of the stone at the zenith of the lift for the downward strike. The findings highlight two new aspects of the capuchins' nut-cracking: (a) Anticipatory actions with the stone before striking, especially when the stone is larger or unfamiliar, and when initiating striking and (b) shifting grips on the stone during a strike. We invite researchers to investigate if other taxa use anticipatory actions and shift their grips during percussive activity.

Competition during sugarcane crop raiding by blond capuchin monkeys (Sapajus flavius).

Shifting to fallback food (FBF) consumption and crop raiding are behavioral adjustments that support primates' ability to endure in human-altered habitats. Nutritional models predict that the consumption of preferred foods leads to increased competition, while consumption of staple fallback foods results in decreased competition. We analyzed the competitive regime faced by individuals in a group of 133 blond capuchin monkeys (Sapajus flavius), an endangered species that inhabits a 270-ha fragment of Atlantic forest in northeast Brazil. During the study year, quantitative analyses show that fruits were a preferred food, while sugarcane was used as a staple FBF. As predicted by primate fallback foraging models, the consumption of sugarcane helped the group to survive in this fragment by providing these animals with half of the food they consumed throughout the year. Contrary to predictions, group dispersion increased with greater fruit abundance, while direct competition peaked during the consumption of sugarcane. We suggest that, although it is abundant and scattered in the area, the long handling time required to process sugarcane before consumption facilitates the direct competition. Overall, the pattern found indicates that consumption of a staple FBF does not directly translate into decreased competition and increased stability of social groups in forest fragments.

Determination of baseline values for routine ophthalmic tests in bearded capuchin (Sapajus libidinosus).

BACKGROUND: Establish baseline values for ophthalmic diagnostic tests in Sapajus libidinosus. METHODS: Ophthalmic diagnostic tests, namely Schirmer tear test 1 (STT-1), intraocular pressure (IOP), B-mode ultrasound, culture of the bacterial conjunctival microbiota, and conjunctival exfoliative cytology, were performed in 15 S. libidinosus. RESULTS: Mean values found were as follows: 2.50 ± 2.94 mm/min for the STT-1; 13.3 ± 3.32 mm Hg for the IOP; 2.47 ± 0.41 mm for the depth of the anterior chamber; 2.86 ± 0.96 mm for the axial length of the lens; 10.97 ± 0.48 mm for the depth of the vitreous chamber; and 16.32 ± 1.24 mm for the axial length of the eyeball. The bacterial genus most frequently found was Staphylococcus spp. Conjunctival cytology showed intermediate epithelial, squamous superficial epithelial, and keratinized cells. CONCLUSIONS: Determination of baseline values for eye measurements and ophthalmic tests will assist in the diagnosis of eye diseases in S. libidinosus monkeys.

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.

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.

Hand preferences and differences in extractive foraging in seven capuchin monkey species.

Tool use and extractive foraging could be drivers for right hand use preference. The robust capuchins, Sapajus, are more specialized for destructive and extractive foraging than the gracile capuchins, Cebus. Thus, we predicted them to show right-hand preference and higher rates of extractive foraging when compared to the gracile capuchins. We hypothesized that capuchins that evolved in dry habitats are predisposed to show higher rates of extractive foraging and right-hand preference. We employed the tube task (152 individuals) and an extractive foraging task (212 individuals) in seven species of capuchins in captive settings. Data on hand preference and extractive foraging were collected using focal and scan sampling, respectively. Contrary to our hypothesis, S. libidinosus showed significant left hand preference, while S. robustus and S. flavius showed a right hand preference. The species S. xanthosternos, S. flavius, and S. robustus engaged in extractive foraging significantly more often than S. apella, S. libidinosus, and Cebus albifrons. As expected, the gracile capuchins showed significant higher left-hand bias when compared to the robust capuchins. The findings from this study is the first indication of left-hand population level laterality in S. libidinosus, a species that evolved in an environment selecting for increased tool use. Although tool use has been associated with population level right handedness, or a strong trend to use the right hand, our results suggest the link between tool use and right-hand preference is simplistic, at least in Sapajus. The ultimate explanation for the differences in hand preference across species might be due to differences in use of key food resources. We suggest that capuchin monkeys from the Atlantic forest evolved under a stronger selective pressure for high reliance on bimanual feeding and extractive foraging, which requires more sequential actions and planning, than those species from the Amazonia forest and Caatinga/Cerrado dry forest.

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.

Foraging and inter-individual distances of bearded capuchin monkeys.

Extractive foraging is a skill young capuchin monkeys learn over time. A key unknown is whether unskilled individuals occupy spatial positions that increase their opportunities to learn. We observed the spatial positions of individuals in a group of capuchin monkeys in Northeastern Brazil. To improve our understanding of the relationship between learning by young capuchin monkeys and inter-individual distance, we investigated the associations between the proximity of individuals and their age, activity, and proficiency at extractive foraging. To do this, we used one form of extractive foraging, opening palm nuts, as an index of proficiency at all types of extractive foraging. Our results indicate that, in the subset of the data where dyads consisted of one proficient individual and a partner with any level of proficiency, the distance between individuals was predicted by their foraging activity (i.e., extractive foraging, other foraging, or not foraging). In those dyads, the proficiency of the partner did not significantly improve prediction of inter-individual distances, indicating that spatial proximity of proficient individuals to others does not function primarily to increase opportunities for unskilled individuals to observe extractive foraging. Dyads in which both individuals were engaged in similar foraging activities (e.g., both "extractive foraging") exhibited the shortest inter-individual distances. Proximity between individuals engaged in similar foraging activities may result from the spatial distribution of resources or from social learning mechanisms, such as local or stimulus enhancement.

Urinary oxytocin in capuchin monkeys: Validation and the influence of social behavior.

In highly social species, like primates, oxytocin plays an important role in cooperation, and in the formation and maintenance of social relationships. Despite recent interest in the relationship between oxytocin and social behavior in nonhuman primates, relatively little is known about endogenous oxytocin in social New World Monkeys. In this paper, we investigate the relationship between oxytocin and affiliative behaviors in socially-housed captive capuchin monkeys (Sapajus [Cebus] apella) by first validating methods of analysis of urinary oxytocin in this species and, second, examining the effects of grooming and fur-rubbing behavior on oxytocin concentrations and further affiliative behavior. In the validation, we found that intranasal exogenous oxytocin significantly increased urinary oxytocin 15-60 min post-administration. Oxytocin was also implicated in both grooming and fur-rubbing behaviors. We found that oxytocin concentrations increased after subjects engaged in grooming or fur-rubbing. In addition, we found that fur-rubbing influenced affiliative behaviors, both during and after a social fur-rubbing bout. While individuals spent more time in contact and proximity while fur-rubbing, immediately following the fur-rubbing event (15-30 min afterwards) all affiliative behaviors decreased. This supports previous research that oxytocin may, in fact, initially be related to increased social distance in this species. Yet, an increase in all affiliative behaviors 30-45 min after the onset of fur-rubbing suggests that fur-rubbing, like grooming, may ultimately function to strengthen social relationships. Overall, these results support a critical role for oxytocin in affiliative behaviors that maintain and strengthen social relationships in capuchin monkeys, and highlight the complexity of the interactions among oxytocin, affiliative behaviors, and social bonding.

Stone tool use by wild capuchin monkeys (Sapajus libidinosus) at Serra das Confusões National Park, Brazil.

Capuchin monkeys (Sapajus spp.) are proficient tool users, and the use of stone tools occurs in several populations, mostly to crack open encased foods. Two well-studied Brazilian populations of Sapajus libidinosus inhabit Fazenda Boa Vista and Serra da Capivara National Park and present different behavioral sets regarding tool use. Serra das Confusões National Park (SCoNP) lies between those sites, but little is known about the capuchin monkey population that lives there. To begin unraveling the capuchin behavior in this area, we conducted a brief survey for tool use sites. We found indirect evidence that capuchin monkeys at SCoNP use stone hammers to crack open at least four species of seeds and fruits. Plant reproductive parts there are processed with stone tools in a similar pattern to the other sites. Further study is needed to directly observe tool use by capuchin monkeys at SCoNP, verify the occurrence of other possible types of tool use in this population, and thus fully compare their tool use repertoire to that of other populations.

Small but wise: Common marmosets (Callithrix jacchus) use acoustic signals as cues to avoid interactions with blonde capuchin monkeys (Sapajus flavius).

Vocalizations are often used by animals to communicate and mediate social interactions. Animals may benefit from eavesdropping on calls from other species to avoid predation and thus increase their chances of survival. Here we use both observational and experimental evidence to investigate eavesdropping and how acoustic signals may mediate interactions between two sympatric and endemic primate species (common marmosets and blonde capuchin monkeys) in a fragment of Atlantic Rainforest in Northeastern Brazil. We observed 22 natural vocal encounters between the study species, but no evident visual or physical contact over the study period. These two species seem to use the same area throughout the day, but at different times. We broadcasted alarm and long distance calls to and from both species as well as two control stimuli (i.e., forest background noise and a loud call from an Amazonian primate) in our playback experiments. Common marmosets showed anti-predator behavior (i.e., vigilance and flight) when exposed to blonde capuchin calls both naturally and experimentally. However, blonde capuchin monkeys showed no anti-predator behavior in response to common marmoset calls. Blonde capuchins uttered long distance calls and looked in the direction of the speaker following exposure to their own long distance call, whereas they fled when exposed to their own alarm calls. Both blonde capuchin monkeys and common marmosets showed fear behaviors in response to the loud call from a primate species unknown to them, and showed no apparent response to the forest background noise. Common marmoset responses to blonde capuchin calls suggests that the latter is a potential predator. Furthermore, common marmosets appear to be eavesdropping on calls from blonde capuchin monkeys to avoid potentially costly encounters with them.

Food or threat? Wild capuchin monkeys (Sapajus libidinosus) as both predators and prey of snakes.

Snakes present a hazard to primates, both as active predators and by defensive envenomation. This risk might have been a selective pressure on the evolution of primate visual and cognitive systems, leading to several behavioral traits present in human and non-human primates, such as the ability to quickly learn to fear snakes. Primates seldom prey on snakes, and humans are one of the few primate species that do. We report here another case, the wild capuchin monkey (Sapajus libidinosus), which preys on snakes. We hypothesized that capuchin monkeys, due to their behavioral plasticity, and cognitive and visual skills, would be capable of discriminating dangerous and non-dangerous snakes and behave accordingly. We recorded the behavioral patterns exhibited toward snakes in two populations of S. libidinosus living 320 km apart in Piauí, Brazil. As expected, capuchins have a fear reaction to dangerous snakes (usually venomous or constricting snakes), presenting mobbing behavior toward them. In contrast, they hunt and consume non-dangerous snakes without presenting the fear response. Our findings support the tested hypothesis that S. libidinosus are capable of differentiating snakes by level of danger: on the one hand they protect themselves from dangerous snakes, on the other hand they take opportunities to prey on non-dangerous snakes. Since capuchins and humans are both predators and prey of snakes, further studies of this complex relationship may shed light on the evolution of these traits in the human lineage.