Wild Capuchin Monkeys Research Articles

Wild capuchin monkeys spontaneously adjust actions when using hammer stones of different mass to crack nuts of different resistance.

Expert tool users are known to adjust their actions skillfully depending on aspects of tool type and task. We examined if bearded capuchin monkeys cracking nuts with stones of different mass adjusted the downward velocity and the height of the stone when striking palm nuts. During a field experiment carried out in FBV (Piauí, Brazil), eight adult wild capuchin monkeys (five males) cracked Orbygnia nuts of varied resistance with hammer stones differing in mass. From recorded videos, we identified the highest strike per nut-cracking episode, and for this strike, we calculated the height to which the monkey lifted the stone, the maximum velocity of the stone during the downward phase, the work done on the stone, and the kinetic energy of the strike. We found that individual capuchins achieved average maximum kinetic energy of 8.7-16.1 J when using stones between 0.9 and 1.9 kg, and maximum kinetic energy correlated positively with mass of the stone. Monkeys lifted all the stones to an individually consistent maximum height but added more work to the stone when using lighter stones. One male and one female monkey lifted stones higher when they cracked more resistant nuts. The high resistance of the Orbygnia nut elicits production of maximum kinetic energy, which the monkeys modulate to some degree by adding work to lighter stones. Capuchin monkeys, like chimpanzees, modulate their actions in nut-cracking, indicating skilled action, although neither species regulates kinetic energy as precisely as skilled human stone knappers. Kinematic analyses promise to yield new insights into the ways and extent to which nonhuman tool users develop expertise. Am J Phys Anthropol 161:53-61, 2016. © 2016 Wiley Periodicals, Inc.

When and where to practice: social influences on the development of nut-cracking in bearded capuchins (Sapajus libidinosus).

The habitual use of tools by wild capuchin monkeys presents a unique opportunity to study the maintenance and transmission of traditions. Young capuchins spend several years interacting with nuts before cracking them efficiently with stone tools. Using a two-observer method, we quantified the magnitude of the social influences that sustain this long period of practice. During five collection periods (over 26 months), one observer recorded the behavior of 16 immature monkeys, and another observer concurrently recorded behavior of group members in the focal monkey's vicinity. The two-observer method provides a means to quantify distinct social influences. Data show that immatures match the behavior of the adults in time and especially in space. The rate of manipulation of nuts by the immatures quadrupled when others in the group cracked and ate nuts, and immatures were ten times more likely to handle nuts and 40 times more likely to strike a nut with a stone when they themselves were near the anvils. Moreover, immature monkeys were three times more likely to be near an anvil when others were cracking. We suggest a model for social influence on nut-cracking development, based on two related processes: (1) social facilitation from observing group members engaged in nut-cracking, and (2) opportunity for practice provided by the anvils, hammer stones and nut shells available on and around the anvils. Nut-cracking activities by others support learning by drawing immatures to the anvils, where extended practice can take place, and by providing materials for practice at these places.

Sexual bias in probe tool manufacture and use by wild bearded capuchin monkeys

Here we examine data from a two-year research on the use of sticks as probes by two groups of wild capuchin monkeys (Sapajus libidinosus) in Serra da Capivara National Park (PI), Brazil. The use of sticks as probes is not usually observed among wild tufted capuchin (Sapajus spp.) populations, having been reported as a customary behavior only in SCNP groups. Probe tools are used to access small prey (insects or lizards) in rock cracks or tree trunks, or honey from wasps’ nests, and also to poke toads and poisonous snakes. Probe use is, so far, the only known case in which wild capuchins modify objects used as tools: branches are trimmed off, and tips, thinned. Tool preparation episodes involved up to four modification steps. Contrary to the stone tools used to crack hard nuts, probe tools don’t present any weight constraint for use by females, but there is nevertheless a strong male bias (97%) in the occurrence of probe tool use. There are also no diet biases that could explain this difference. Although males hunt more often than females, the latter main prey items are lizards, which are also the main targets of probe tool use. One possibility is that females may have fewer social opportunities to learn about probe tools.

Archaeology meets primate technology

A study of wild capuchin monkeys that crack nuts using stone hammers reveals temporal and spatial patterning of the relics of their technological efforts, confirming that such behaviours can be studied from an archaeological perspective.

Artifact and Artifact Categorization: Comparing Humans and Capuchin Monkeys

We aim to show that far-related primates like humans and the capuchin monkeys show interesting correspondences in terms of artifact characterization and categorization. We investigate this issue by using a philosophically-inspired definition of physical artifact which, developed for human artifacts, turns out to be applicable for cross-species comparison. In this approach an artifact is created when an entity is intentionally selected and some capacities attributed to it (often characterizing a purpose). Behavioral studies suggest that this notion of artifact is not specific to the human kind. On the basis of the results of a series of field observations and experiments on wild capuchin monkeys that routinely use stone hammers and anvils, we show that the notions of intentional selection and attributed capacity appear to be at play in capuchins as well. The study also suggests that functional criteria and contextualization play a fundamental role in terms of artifact recognition and categorization in nonhuman primates.

Non-random walks in monkeys and humans

Principles of self-organization play an increasingly central role in models of human activity. Notably, individual human displacements exhibit strongly recurrent patterns that are characterized by scaling laws and can be mechanistically modelled as self-attracting walks. Recurrence is not, however, unique to human displacements. Here we report that the mobility patterns of wild capuchin monkeys are not random walks, and they exhibit recurrence properties similar to those of cell phone users, suggesting spatial cognition mechanisms shared with humans. We also show that the highly uneven visitation patterns within monkey home ranges are not entirely self-generated but are forced by spatio-temporal habitat heterogeneities. If models of human mobility are to become useful tools for predictive purposes, they will need to consider the interaction between memory and environmental heterogeneities.

Tool choice on the basis of rigidity in capuchin monkeys

Wild capuchin monkeys select stone tools to crack open nuts on the basis of their weight and friability, two non-visual functional properties. Here, we investigated whether they would select new stick-like tools on the basis of their rigidity. In Experiment 1, subjects faced an out-of-reach reward and a choice of three unfamiliar tools differing in color, diameter, material, and rigidity. In order to retrieve the reward, capuchins needed to select the rigid tool exemplar. Capuchins gathered information regarding tools' pliability either by (1) manipulating the tools themselves (manipulation condition), (2) observing a human demonstrator repeatedly bending the tools (observation condition), or (3) seeing the tools placed on a platform without any manipulation taking place (visual static condition). Subjects selected the rigid tool above chance levels in both the manipulation and observation conditions, but not in the visual static condition. In Experiment 2, subjects needed to select and use a flexible tool to access a liquid reward (as opposed to the rigid tool, as in previous experiment). Again, capuchins selected above chance levels the appropriate tool (i.e., flexible), thus demonstrating a good appreciation of the relation between the tool properties and the task requirements.

Stone tool use by adult wild bearded capuchin monkeys ( Cebus libidinosus). Frequency, efficiency and tool selectivity

Chimpanzees have been the traditional referential models for investigating human evolution and stone tool use by hominins. We enlarge this comparative scenario by describing normative use of hammer stones and anvils in two wild groups of bearded capuchin monkeys ( Cebus libidinosus) over one year. We found that most of the individuals habitually use stones and anvils to crack nuts and other encased food items. Further, we found that in adults (1) males use stone tools more frequently than females, (2) males crack high resistance nuts more frequently than females, (3) efficiency at opening a food by percussive tool use varies according to the resistance of the encased food, (4) heavier individuals are more efficient at cracking high resistant nuts than smaller individuals, and (5) to crack open encased foods, both sexes select hammer stones on the basis of material and weight. These findings confirm and extend previous experimental evidence concerning tool selectivity in wild capuchin monkeys ( Visalberghi et al., 2009b; Fragaszy et al., 2010b). Male capuchins use tools more frequently than females and body mass is the best predictor of efficiency, but the sexes do not differ in terms of efficiency. We argue that the contrasting pattern of sex differences in capuchins compared with chimpanzees, in which females use tools more frequently and more skillfully than males, may have arisen from the degree of sexual dimorphism in body size of the two species, which is larger in capuchins than in chimpanzees. Our findings show the importance of taking sex and body mass into account as separate variables to assess their role in tool use.

Inducing traditions in captive capuchin monkeys ( Cebus apella)

Potential foraging and social traditions have been identified in groups of wild capuchin monkeys (Cebus spp.). Verification of traditions requires documentation that socially mediated learning contributes to acquisition by new practitioners. We investigated the emergence and maintenance of a foraging tradition in two generations of infant tufted capuchins (Cebus apella) in captive social groups. In baseline, we provided the first cohort of infants with a foraging apparatus that dispensed juice via two methods inside a small enclosure away from adult interference (the creche). Later in phase 1, we provided a second apparatus to all group members with only one method of solution available (in the group setting); the creche apparatus, with both methods available, remained accessible to infants only. Two years later (phase 2), we replicated phase 1 with a new cohort of infants from the same social groups. As adult activity and expertise with the apparatus increased across baseline (no adult activity), phase 1 (initially unskilled) and phase 2 (initially skilled), the proportion of infants in each cohort that acquired the foraging skill increased and their latency to skill acquisition decreased. Despite ambiguous evidence that the infants conformed to the specific method of solution common in their group, the social context clearly contributed to the development and maintenance of a general foraging tradition. The results provide support for the existence of traditions in wild capuchin groups.

In-Group Conformity Sustains Different Foraging Traditions in Capuchin Monkeys (Cebus apella)

BackgroundDecades of research have revealed rich cultural repertoires encompassing multiple traditions in wild great apes, a picture crucially complemented by experimental simulations with captive apes. Studies with wild capuchin monkeys, the most encephalized simian species, have indicated a New World convergence on these cultural phenomena, involving multiple traditions and tool use. However, experimental studies to date are in conflict with such findings in concluding that capuchins, like other monkeys, show minimal capacities for social learning.Methodology/Principal FindingsHere we report a new experimental approach in which the alpha male of each of two groups of capuchins was trained to open an artificial foraging device in a quite different way, using either a slide or lift action, then reunited with his group. In each group a majority of monkeys, 8 of 11 and 13 of 14, subsequently mastered the task. Seventeen of the successful 21 monkeys discovered the alternative action to that seeded in the group, performing it a median of 4 times. Nevertheless, all 21 primarily adopted the technique seeded by their group's alpha male. Median proportions of slide versus lift were 0.96 for the group seeded with slide versus 0. 01 for the group seeded with lift.Conclusions/SignificanceThese results suggest a striking effect of social conformity in learned behavioral techniques, consistent with field reports of capuchin traditions and convergent on the only other species in which such cultural phenomena have been reported, chimpanzees and humans.

First record of tool use by wild populations of the yellow‐breasted capuchin monkey (Cebus xanthosternos) and new records for the bearded capuchin (Cebus libidinosus)

Reports on use of stones as hammers and anvils to open hard nuts by wild capuchin monkeys are scarce and limited to Cebus libidinosus. Here, we report for the first time data on tool use-stones as hammer and anvils to open nuts-in wild C. xanthosternos and a description of new tool using sites for C. libidinosus. Our records were made by visiting anvil sites and by information obtained from local residents. We surveyed three different biomes: Caatinga (dry forest and thorn scrub), Cerrado (Brazilian bush savannah), and Atlantic forest (wet forest), all records of tool use were from Caatinga or transitional areas between habitats. The behavior is suggested to be routinely performed and widespread among several populations. The fruits of six plant species in different localities were opened with hammer stones by C. xanthosternos. Hammer stones were of similar weigh as those described in other studies of C. libidinosus. Conditions found in Caatinga, such as a more frequent use of the ground by the monkeys and/or food scarcity, may play an important role in the acquisition of nut-cracking behavior. The absence of more reports of nut cracking and other forms of tool use in other species of wild Cebus is likely to result from a lack of surveys in very dry and food-limited habitats or intrinsic characteristics of other Cebus species.

Distribution of potential suitable hammers and transport of hammer tools and nuts by wild capuchin monkeys

Selection and transport of objects to use as tools at a distant site are considered to reflect planning. Ancestral humans transported tools and tool-making materials as well as food items. Wild chimpanzees also transport selected hammer tools and nuts to anvil sites. To date, we had no other examples of selection and transport of stone tools among wild nonhuman primates. Wild bearded capuchins (Cebus libidinosus) in Boa Vista (Piauí, Brazil) routinely crack open palm nuts and other physically well-protected foods on level surfaces (anvils) using stones (hammers) as percussive tools. Here we present indirect evidence, obtained by a transect census, that stones suitable for use as hammers are rare (study 1) and behavioral evidence of hammer transport by twelve capuchins (study 2). To crack palm nuts, adults transported heavier and harder stones than to crack other less resistant food items. These findings show that wild capuchin monkeys selectively transport stones of appropriate size and hardness to use as hammers, thus exhibiting, like chimpanzees and humans, planning in tool-use activities.

The enhanced tool‐kit of two groups of wild bearded capuchin monkeys in the Caatinga: tool making, associative use, and secondary tools

The use of stones to crack open encapsulated fruit is widespread among wild bearded capuchin monkeys (Cebus libidinosus) inhabiting savanna-like environments. Some populations in Serra da Capivara National Park (Piauí, Brazil), though, exhibit a seemingly broader toolkit, using wooden sticks as probes, and employing stone tools for a variety of purposes. Over the course of 701.5 hr of visual contact of two wild capuchin groups we recorded 677 tool use episodes. Five hundred and seventeen of these involved the use of stones, and 160 involved the use of sticks (or other plant parts) as probes to access water, arthropods, or the contents of insects' nests. Stones were mostly used as "hammers"--not only to open fruit or seeds, or smash other food items, but also to break dead wood, conglomerate rock, or cement in search of arthropods, to dislodge bigger stones, and to pulverize embedded quartz pebbles (licking, sniffing, or rubbing the body with the powder produced). Stones also were used in a "hammer-like" fashion to loosen the soil for digging out roots and arthropods, and sometimes as "hoes" to pull the loosened soil. In a few cases, we observed the re-utilization of stone tools for different purposes (N=3), or the combined use of two tools-stones and sticks (N=4) or two stones (N=5), as sequential or associative tools. On three occasions, the monkeys used smaller stones to loosen bigger quartz pebbles embedded in conglomerate rock, which were subsequently used as tools. These could be considered the first reports of secondary tool use by wild capuchin monkeys.

Physical properties of palm fruits processed with tools by wild bearded capuchins (Cebus libidinosus)

Habitually, capuchin monkeys access encased hard foods by using their canines and premolars and/or by pounding the food on hard surfaces. Instead, the wild bearded capuchins (Cebus libidinosus) of Boa Vista (Brazil) routinely crack palm fruits with tools. We measured size, weight, structure, and peak-force-at-failure of the four palm fruit species most frequently processed with tools by wild capuchin monkeys living in Boa Vista. Moreover, for each nut species we identify whether peak-force-at-failure was consistently associated with greater weight/volume, endocarp thickness, and structural complexity. The goals of this study were (a) to investigate whether these palm fruits are difficult, or impossible, to access other than with tools and (b) to collect data on the physical properties of palm fruits that are comparable to those available for the nuts cracked open with tools by wild chimpanzees. Results showed that the four nut species differ in terms of peak-force-at-failure and that peak-force-at-failure is positively associated with greater weight (and consequently volume) and apparently with structural complexity (i.e. more kernels and thus more partitions); finally for three out of four nut species shell thickness is also positively associated with greater volume. The finding that the nuts exploited by capuchins with tools have very high resistance values support the idea that tool use is indeed mandatory to crack them open. Finally, the peak-force-at-failure of the piassava nuts is similar to that reported for the very tough panda nuts cracked open by wild chimpanzees; this highlights the ecological importance of tool use for exploiting high resistance foods in this capuchin species.

Experimental field study of hand preference in wild black-horned (Cebus nigritus) and white-faced (Cebus capucinus) capuchins: evidence for individual and species differences

In this experimental field investigation, we compare the degree to which wild capuchins in Brazil (Cebus nigritus) and Costa Rica (Cebus capucinus) exhibit individual- and population-level handedness during three visually-guided tasks. These tasks required reaching to remove a large leaf covering a hidden food reward, seizing the food reward, and manipulating a tool (pulling a wooden dowel) in order to obtain access to an embedded food reward. Studies in some populations of captive capuchins indicate evidence for both individual hand preferences and population-level handedness. In this study, six of eight wild C. capucinus and six of seven wild C. nigritus exhibited a significant hand preference during individual tasks, but no individual exhibited a consistent preference across all three tasks. Task-specialization, or the tendency for most individuals in the same group or population to use the same hand to accomplish a particular task, also was evaluated. Cebus nigritus showed a significant bias toward the use of the right hand in removing the leaf. Although the number of individual capuchins in both species that manipulated the dowels was limited (N = 7), each individual that manipulated the dowels in eight or more instances had a positive handedness index, suggesting a greater use of the right hand to accomplish this task. Overall, our results provide preliminary support for individual- and population-level handedness in wild capuchin monkeys.

Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella).

It has been reported that wild capuchin monkeys exhibit several group-specific behavioural traditions. By contrast, experiments have found little evidence for the social learning assumed necessary to support such traditions. The present study used a diffusion chain paradigm to investigate whether a novel foraging task could be observationally learned by capuchins (Cebus apella) and then transmitted along a chain of individuals. We used a two-action paradigm to control for independent learning. Either of two methods (lift or slide) could be used to open the door of a foraging apparatus to retrieve food. Two chains were tested (N1=4; N2=5), each beginning with an experimenter-trained model who demonstrated to a partner its group-specific method for opening the foraging apparatus. After the demonstration, if the observer was able to open the apparatus 20 times by either method, then it became the demonstrator for a new subject, thus simulating the spread of a foraging tradition among 'generations' of group members. Each method was transmitted along these respective chains with high fidelity, echoing similar results presently available only for chimpanzees and children. These results provide the first clear evidence for faithful diffusion of alternative foraging methods in monkeys, consistent with claims for capuchin traditions in the wild.

Paracoccidioidomycosis in wild monkeys from Paraná State, Brazil

The aim of this study was to evaluate the seroprevalence of Paracoccidioides brasiliensis infection in wild New World monkeys (Cebus sp. and Alouatta caraya). A total of 93 animals (Cebus sp., n = 68 and Alouatta caraya, n = 25) were captured in the Paraná River basin, Paraná State, Brazil and the serum samples were analyzed by ELISA and immunodiffusion using P. brasiliensis gp43 and exoantigen as antigens, respectively. The seropositivity observed by ELISA was 44.1% and 60% for Cebus sp. and A. caraya, respectively, while by immunodiffusion test Cebus sp. showed positivity of 2.9% only. No significant difference was observed in relation to age and sex. This is the first report of paracoccidioidomycosis in wild capuchin monkeys and in wild-black and golden-howler monkeys. The high positivity to P. brasiliensis infection in both species evaluated in our study and the positivity by immunodiffusion test in Cebus sp. suggest that natural disease may be occurring in wild monkeys living in paracoccidioidomycosis endemic areas.

Experimental evidence for route integration and strategic planning in wild capuchin monkeys

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group's choices in ways consistent with foraging theory or principles of operant psychology. The group's site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer 'detour' through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging.

Cross‐genus adoption of a marmoset (Callithrix jacchus) by wild capuchin monkeys (Cebus libidinosus): case report

We report a case of interspecies adoption of an infant marmoset (Callithrix jacchus) by wild capuchin monkeys (Cebus libidinosus). The marmoset was an infant when it was first observed in the capuchin group on 3 March 2004. Since it first appeared it has been observed informally and frequently. In January 2005 systematic observations were made of the marmoset and a capuchin of similar age. Throughout its period of adoption the marmoset appeared to be socially integrated into the group, benefiting from nurturant behaviors exhibited by two successive adoptive "mothers" and pronounced tolerance from all members of the group. This case highlights the flexibility of both Callithrix and Cebus in accommodating variable social behaviors and other characteristics (including size) of social partners.

Sero-epidemiological survey for toxoplasmosis in wild New World monkeys ( Cebus spp.; Alouatta caraya) at the Paraná river basin, Paraná State, Brazil

In this study, we captured 60 wild New World monkeys ( Cebus spp.; Alouatta caraya) at the Paraná river basin, Paraná State, Brazil, and modified agglutination test (MAT) was performed to evaluate anti- Toxoplasma gondii antibodies. Prevalence was 30.2% (13/43) in Cebus spp. (capuchin monkeys) and 17.6% (3/17) for A. caraya (black and golden howler monkeys). MAT showed antibody titers of 16 (15/16) and 64 (1/16). Herein, we have observed an odds ratio (OR) = 4.67 (1.06 < OR < 21.42, p < 0.01) among monkeys with presumed risk of human contact. There were not any statistical differences among age, species and sex ( p > 0.05). The present work is the first report on serum occurrence of anti- T. gondii antibodies in wild capuchin monkeys and in wild black and golden howler monkeys.