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.     

Ultra-rapid categorization of fourier-spectrum equalized natural images: macaques and humans perform similarly

Background

Comparative studies of cognitive processes find similarities between humans and apes but also monkeys. Even high-level processes, like the ability to categorize classes of object from any natural scene under ultra-rapid time constraints, seem to be present in rhesus macaque monkeys (despite a smaller brain and the lack of language and a cultural background). An interesting and still open question concerns the degree to which the same images are treated with the same efficacy by humans and monkeys when a low level cue, the spatial frequency content, is controlled.

Methodology/Principal Findings

We used a set of natural images equalized in Fourier spectrum and asked whether it is still possible to categorize them as containing an animal and at what speed. One rhesus macaque monkey performed a forced-choice saccadic task with a good accuracy (67.5% and 76% for new and familiar images respectively) although performance was lower than with non-equalized images. Importantly, the minimum reaction time was still very fast (100 ms). We compared the performances of human subjects with the same setup and the same set of (new) images. Overall mean performance of humans was also lower than with original images (64% correct) but the minimum reaction time was still short (140 ms).

Conclusion

Performances on individual images (% correct but not reaction times) for both humans and the monkey were significantly correlated suggesting that both species use similar features to perform the task. A similar advantage for full-face images was seen for both species. The results also suggest that local low spatial frequency information could be important, a finding that fits the theory that fast categorization relies on a rapid feedforward magnocellular signal.     

Testing for divergent transmission histories among cultural characters: a study using Bayesian phylogenetic methods and Iranian tribal textile data

Background

Archaeologists and anthropologists have long recognized that different cultural complexes may have distinct descent histories, but they have lacked analytical techniques capable of easily identifying such incongruence. Here, we show how Bayesian phylogenetic analysis can be used to identify incongruent cultural histories. We employ the approach to investigate Iranian tribal textile traditions.

Methods

We used Bayes factor comparisons in a phylogenetic framework to test two models of cultural evolution: the hierarchically integrated system hypothesis and the multiple coherent units hypothesis. In the hierarchically integrated system hypothesis, a core tradition of characters evolves through descent with modification and characters peripheral to the core are exchanged among contemporaneous populations. In the multiple coherent units hypothesis, a core tradition does not exist. Rather, there are several cultural units consisting of sets of characters that have different histories of descent.

Results

For the Iranian textiles, the Bayesian phylogenetic analyses supported the multiple coherent units hypothesis over the hierarchically integrated system hypothesis. Our analyses suggest that pile-weave designs represent a distinct cultural unit that has a different phylogenetic history compared to other textile characters.

Conclusions

The results from the Iranian textiles are consistent with the available ethnographic evidence, which suggests that the commercial rug market has influenced pile-rug designs but not the techniques or designs incorporated in the other textiles produced by the tribes. We anticipate that Bayesian phylogenetic tests for inferring cultural units will be of great value for researchers interested in studying the evolution of cultural traits including language, behavior, and material culture.     

When the transmission of culture is child's play

Background

Humans frequently engage in arbitrary, conventional behavior whose primary purpose is to identify with cultural in-groups. The propensity for doing so is established early in human ontogeny as children become progressively enmeshed in their own cultural milieu. This is exemplified by their habitual replication of causally redundant actions shown to them by adults. Yet children seemingly ignore such actions shown to them by peers. How then does culture get transmitted intra-generationally? Here we suggest the answer might be ‘in play’.

Principal Findings

Using a diffusion chain design preschoolers first watched an adult retrieve a toy from a novel apparatus using a series of actions, some of which were obviously redundant. These children could then show another child how to open the apparatus, who in turn could show a third child. When the adult modeled the actions in a playful manner they were retained down to the third child at higher rates than when the adult seeded them in a functionally oriented way.

Conclusions

Our results draw attention to the possibility that play might serve a critical function in the transmission of human culture by providing a mechanism for arbitrary ideas to spread between children.     

Meaningful Gesture in Monkeys? Investigating whether Mandrills Create Social Culture

Background

Human societies exhibit a rich array of gestures with cultural origins. Often these gestures are found exclusively in local populations, where their meaning has been crafted by a community into a shared convention. In nonhuman primates like African monkeys, little evidence exists for such culturally-conventionalized gestures.

Methodology/Principal Findings

Here I report a striking gesture unique to a single community of mandrills (Mandrillus sphinx) among nineteen studied across North America, Africa, and Europe. The gesture was found within a community of 23 mandrills where individuals old and young, female and male covered their eyes with their hands for periods which could exceed 30 min, often while simultaneously raising their elbow prominently into the air. This ‘Eye covering’ gesture has been performed within the community for a decade, enduring deaths, removals, and births, and it persists into the present. Differential responses to Eye covering versus controls suggested that the gesture might have a locally-respected meaning, potentially functioning over a distance to inhibit interruptions as a ‘do not disturb’ sign operates.

Conclusions/Significance

The creation of this gesture by monkeys suggests that the ability to cultivate shared meanings using novel manual acts may be distributed more broadly beyond the human species. Although logistically difficult with primates, the translocation of gesturers between communities remains critical to experimentally establishing the possible cultural origin and transmission of nonhuman gestures.     

Dynamics of alliance formation and the egalitarian revolution

Background

Arguably the most influential force in human history is the formation of social coalitions and alliances (i.e., long-lasting coalitions) and their impact on individual power. Understanding the dynamics of alliance formation and its consequences for biological, social, and cultural evolution is a formidable theoretical challenge. In most great ape species, coalitions occur at individual and group levels and among both kin and non-kin. Nonetheless, ape societies remain essentially hierarchical, and coalitions rarely weaken social inequality. In contrast, human hunter-gatherers show a remarkable tendency to egalitarianism, and human coalitions and alliances occur not only among individuals and groups, but also among groups of groups. These observations suggest that the evolutionary dynamics of human coalitions can only be understood in the context of social networks and cognitive evolution.

Methodology/Principal Findings

Here, we develop a stochastic model describing the emergence of networks of allies resulting from within-group competition for status or mates between individuals utilizing dyadic information. The model shows that alliances often emerge in a phase transition-like fashion if the group size, awareness, aggressiveness, and persuasiveness of individuals are large and the decay rate of individual affinities is small. With cultural inheritance of social networks, a single leveling alliance including all group members can emerge in several generations.

Conclusions/Significance

We propose a simple and flexible theoretical approach for studying the dynamics of alliance emergence applicable where game-theoretic methods are not practical. Our approach is both scalable and expandable. It is scalable in that it can be generalized to larger groups, or groups of groups. It is expandable in that it allows for inclusion of additional factors such as behavioral, genetic, social, and cultural features. Our results suggest that a rapid transition from a hierarchical society of great apes to an egalitarian society of hunter-gatherers (often referred to as “egalitarian revolution”) could indeed follow an increase in human cognitive abilities. The establishment of stable group-wide egalitarian alliances creates conditions promoting the origin of cultural norms favoring the group interests over those of individuals.     

Genetic immunisation by liver stage antigen 3 protects chimpanzees against malaria despite low immune responses

Background

The true interest of genetic immunisation might have been hastily underestimated based on overall immunogenicity data in humans and lack of parallelism with other, more classical immunisation methods.

Principal Findings

Using malaria Liver Stage Antigen-3 (LSA-3), we report that genetic immunization induces in chimpanzees, the closest relative of humans, immune responses which are as scarce as those reported using other DNA vaccines in humans, but which nonetheless confer strong, sterile and reproducible protection. The pattern was consistent in 3/4 immunized apes against two high dose sporozoite challenges performed as late as 98 and 238 days post-immunization and by a heterologous strain.

Conclusions

These results should, in our opinion, lead to a revisiting of the value of this unusual means of immunisation, using as a model a disease, malaria, in which virulent challenges of volunteers are ethically acceptable.     

A New Approach for Monitoring Ebolavirus in Wild Great Apes

Background

Central Africa is a “hotspot” for emerging infectious diseases (EIDs) of global and local importance, and a current outbreak of ebolavirus is affecting multiple countries simultaneously. Ebolavirus is suspected to have caused recent declines in resident great apes. While ebolavirus vaccines have been proposed as an intervention to protect apes, their effectiveness would be improved if we could diagnostically confirm Ebola virus disease (EVD) as the cause of die-offs, establish ebolavirus geographical distribution, identify immunologically naïve populations, and determine whether apes survive virus exposure.

Methodology/Principal findings

Here we report the first successful noninvasive detection of antibodies against Ebola virus (EBOV) from wild ape feces. Using this method, we have been able to identify gorillas with antibodies to EBOV with an overall prevalence rate reaching 10% on average, demonstrating that EBOV exposure or infection is not uniformly lethal in this species. Furthermore, evidence of antibodies was identified in gorillas thought previously to be unexposed to EBOV (protected from exposure by rivers as topological barriers of transmission).

Conclusions/Significance

Our new approach will contribute to a strategy to protect apes from future EBOV infections by early detection of increased incidence of exposure, by identifying immunologically naïve at-risk populations as potential targets for vaccination, and by providing a means to track vaccine efficacy if such intervention is deemed appropriate. Finally, since human EVD is linked to contact with infected wildlife carcasses, efforts aimed at identifying great ape outbreaks could have a profound impact on public health in local communities, where EBOV causes case-fatality rates of up to 88%.     

Campanulaceae: a family with small seeds that require light for germination

Background and Aims

The Campanulaceae is a large cosmopolitan family, but is understudied in terms of germination, and seed biology in general. Small seed mass (usually in the range 10–200 µg) is a noteworthy trait of the family, and having small seeds is commonly associated with a light requirement. Thus, the purpose of this study was to investigate the effect of light on germination in 131 taxa of the Campanulaceae family, from all five continents of its distribution.

Methods

For all taxa, seed germination was tested in light (8 or 12 h photoperiod) and continuous darkness under constant and alternating temperatures. For four taxa, the effect of light on germination was examined over a wide range of temperatures on a thermogradient plate, and the possible substitution of the light requirement by gibberellic acid and nitrate was examined in ten taxa.

Key Results

For all 131 taxa, seed germination was higher in light than in darkness for every temperature tested. Across species, the light requirement decreased significantly with increasing seed mass. For larger seeded species, germination in the dark reached higher levels under alternating than under constant temperatures. Gibberellic acid promoted germination in darkness whereas nitrates partially substituted for a light requirement only in species showing some dark germination.

Conclusions

A light requirement for germination, observed in virtually all taxa examined, constitutes a collective characteristic of the family. It is postulated that smaller seeded taxa might germinate only on the soil surface or at shallow depths, while larger seeded species might additionally germinate when buried in the soil if cued to do so by fluctuating temperatures.     

The Maintenance of Traditions in Marmosets: Individual Habit,Not Social Conformity? A Field Experiment

Background

Social conformity is a cornerstone of human culture because it accelerates and maintains the spread of behaviour within a group. Few empirical studies have investigated the role of social conformity in the maintenance of traditions despite an increasing body of literature on the formation of behavioural patterns in non-human animals. The current report presents a field experiment with free-ranging marmosets (Callithrix jacchus) which investigated whether social conformity is necessary for the maintenance of behavioural patterns within groups or whether individual effects such as habit formation would suffice.

Methods

Using a two-action apparatus, we established alternative behavioural patterns in six family groups composed of 36 individuals. These groups experienced only one technique during a training phase and were thereafter tested with two techniques available. The monkeys reliably maintained the trained method over a period of three weeks, despite discovering the alternative technique. Three additional groups were given the same number of sessions, but those 21 individuals could freely choose the method to obtain a reward. In these control groups, an overall bias towards one of the two methods was observed, but animals with a different preference did not adjust towards the group norm. Thirteen of the fifteen animals that discovered both techniques remained with the action with which they were initially successful, independent of the group preference and the type of action (Binomial test: exp. proportion: 0.5, p<0.01).

Conclusions

The results indicate that the maintenance of behavioural patterns within groups 1) could be explained by the first rewarded manipulation and subsequent habit formation and 2) do not require social conformity as a mechanism. After an initial spread of a behaviour throughout a group, this mechanism may lead to a superficial appearance of conformity without the involvement of such a socially and cognitively complex mechanism. This is the first time that such an experiment has been conducted with free-ranging primates.     

Type II collagen antibody response is enriched in the synovial fluid of rheumatoid joints and directed to the same major epitopes as in collagen induced arthritis in primates and mice

Introduction

Antibodies towards type II collagen (CII) are detected in patients with rheumatoid arthritis (RA) and in non-human primates and rodents with collagen induced arthritis (CIA). We have previously shown that antibodies specific for several CII-epitopes are pathogenic using monoclonal antibodies from arthritic mice, although the role of different anti-CII epitopes has not been investigated in detail in other species. We therefore performed an inter-species comparative study of the autoantibody response to CII in patients with RA versus monkeys and mice with CIA.

Methods

Analysis of the full epitope repertoire along the disease course of CIA was performed using a library of CII triple-helical peptides. The antibody responses to the major CII epitopes were analyzed in sera and synovial fluid from RA patients, and in sera from rhesus monkeys (Macaca mulatta), common marmosets (Callithrix jacchus) and mice.

Results

Many CII epitopes including the major C1, U1, and J1 were associated with established CIA and arginine residues played an important role in the anti-CII antibody interactions. The major epitopes were also recognized in RA patients, both in sera and even more pronounced in synovial fluid: 77% of the patients had antibodies to the U1 epitope. The anti-CII immune response was not restricted to the anti-citrulline protein antibodies (ACPA) positive RA group.

Conclusion

CII conformational dependent antibody responses are common in RA and are likely to originate from rheumatoid joints but did not show a correlation with ACPA response. Importantly, the fine specificity of the anti-CII response is similar with CIA in monkeys and rodents where the recognized epitopes are conserved and have a major pathogenic role. Thus, anti-CII antibodies may both contribute to, as well as be the consequence of, local joint inflammation.     

Evidence of a link between taboos and sacrifices and resource scarcity of ritual plants

Background

One of the main obstacles for the mainstreaming of religious traditions as tools for the conservation of nature is the limited applicability of research results in this field. We documented two different restrictions implemented by local people (taboos and sacrifices) related to the use of ritual plants in Benin (West Africa) and Gabon (Central Africa).

Methods

To see whether these restrictions reflected plant scarcity from an etic perspective (official threat status) and an emic viewpoint (perceived scarcity by local people), we conducted 102 interviews with traditional healers and adepts of traditional faiths.

Results

We documented a total of 618 ritual plants, from which 52 species were used in both countries. In Benin, the use of 63 of the 414 ritual plant species was restricted; while in Gabon 23 of the 256 ritual plants were associated with taboos and sacrifices. In Benin, restricted plants were significantly more often officially threatened, perceived as scarce, and actively protected than non-restricted plants. In the more forested and less densely populated Gabon, plants that were perceived as scarce were more often associated to local restrictions than officially threatened species.

Conclusions

These results prove the presence of a form of adaptive management where restrictions are related to resource scarcity and protection of ritual plant species. By providing baseline data on possibly endangered species, we demonstrate how plant use in the context of religious traditions can yield important information for conservation planning.

Electronic supplementary material

The online version of this article (doi:10.1186/1746-4269-11-5) contains supplementary material, which is available to authorized users.     

Tool use in Cebus

This paper summarizes early anecdotal information and systematic studies of tool use in capuchin monkeys (Cebus spp.). Tool use in capuchins is neither context specific nor stereotyped. The success of capuchins in using tools and in exploiting a variety of food resources in the wild derives from several factors: their manipulative abilities, interest in external objects and a tendency to explore the environment. In using tools, capuchins are similar to apes and more proficient than other monkey species. A cognitive approach indicates, however, that (in contrast with chimpanzees) they never develop an understanding of the requirements of the tool tasks presented.     

Experimental set up for the irradiation of biological samples and nuclear track detectors with UV C

Aim

In this work we present a methodology to produce an “imprint” of cells cultivated on a polycarbonate detector by exposure of the detector to UV C radiation.

Background

The distribution and concentration of ¹⁰B atoms in tissue samples coming from BNCT (Boron Neutron Capture Therapy) protocols can be determined through the quantification and analysis of the tracks forming its autoradiography image on a nuclear track detector. The location of boron atoms in the cell structure could be known more accurately by the simultaneous observation of the nuclear tracks and the sample image on the detector.

Materials and Methods

A UV C irradiator was constructed. The irradiance was measured along the lamp direction and at different distances. Melanoma cells were cultured on polycarbonate foils, incubated with borophenylalanine, irradiated with thermal neutrons and exposed to UV C radiation. The samples were chemically attacked with a KOH solution.

Results

A uniform irradiation field was established to expose the detector foils to UV C light. Cells could be seeded on the polycarbonate surface. Both imprints from cells and nuclear tracks were obtained after chemical etching.

Conclusions

It is possible to yield cellular imprints in polycarbonate. The nuclear tracks were mostly present inside the cells, indicating a preferential boron uptake.     

Serotonin Transporter Genotype Modulates Social Reward and Punishment in Rhesus Macaques

Background

Serotonin signaling influences social behavior in both human and nonhuman primates. In humans, variation upstream of the promoter region of the serotonin transporter gene (5-HTTLPR) has recently been shown to influence both behavioral measures of social anxiety and amygdala response to social threats. Here we show that length polymorphisms in 5-HTTLPR predict social reward and punishment in rhesus macaques, a species in which 5-HTTLPR variation is analogous to that of humans.

Methodology/Principal Findings

In contrast to monkeys with two copies of the long allele (L/L), monkeys with one copy of the short allele of this gene (S/L) spent less time gazing at face than non-face images, less time looking in the eye region of faces, and had larger pupil diameters when gazing at photos of a high versus low status male macaques. Moreover, in a novel primed gambling task, presentation of photos of high status male macaques promoted risk-aversion in S/L monkeys but promoted risk-seeking in L/L monkeys. Finally, as measured by a “pay-per-view” task, S/L monkeys required juice payment to view photos of high status males, whereas L/L monkeys sacrificed fluid to see the same photos.

Conclusions/Significance

These data indicate that genetic variation in serotonin function contributes to social reward and punishment in rhesus macaques, and thus shapes social behavior in humans and rhesus macaques alike.     

A TMA de-arraying method for high throughput biomarker discovery in tissue research

Background

Tissue MicroArrays (TMAs) represent a potential high-throughput platform for the analysis and discovery of tissue biomarkers. As TMA slides are produced manually and subject to processing and sectioning artefacts, the layout of TMA cores on the final slide and subsequent digital scan (TMA digital slide) is often disturbed making it difficult to associate cores with their original position in the planned TMA map. Additionally, the individual cores can be greatly altered and contain numerous irregularities such as missing cores, grid rotation and stretching. These factors demand the development of a robust method for de-arraying TMAs which identifies each TMA core, and assigns them to their appropriate coordinates on the constructed TMA slide.

Methodology

This study presents a robust TMA de-arraying method consisting of three functional phases: TMA core segmentation, gridding and mapping. The segmentation of TMA cores uses a set of morphological operations to identify each TMA core. Gridding then utilises a Delaunay Triangulation based method to find the row and column indices of each TMA core. Finally, mapping correlates each TMA core from a high resolution TMA whole slide image with its name within a TMAMap.

Conclusion

This study describes a genuine robust TMA de-arraying algorithm for the rapid identification of TMA cores from digital slides. The result of this de-arraying algorithm allows the easy partition of each TMA core for further processing. Based on a test group of 19 TMA slides (3129 cores), 99.84% of cores were segmented successfully, 99.81% of cores were gridded correctly and 99.96% of cores were mapped with their correct names via TMAMaps. The gridding of TMA cores were also extensively tested using a set of 113 pseudo slide (13,536 cores) with a variety of irregular grid layouts including missing cores, rotation and stretching. 100% of the cores were gridded correctly.     

Implementation of LED Fluorescence Microscopy for Diagnosis of Pulmonary and HIV-Associated Tuberculosis in a Hospital Setting in Indonesia

Background

Fluorescence microscopy (FM) has not been implemented widely in TB endemic settings and little evaluation has been done in HIV-infected patients. We evaluated diagnostic performance, time and costs of FM with light-emitting diodes technology (LED-FM), compared with conventional (Zieh-Neelsen) microscopy in a hospital in Indonesia which acts as referral centre for HIV-infected patients.

Method

We included pulmonary tuberculosis suspects from the outpatient and HIV clinic. Direct and concentrated sputum smears were examined using LED-FM and ZN microscopy by two technicians who were blinded for the HIV-status and the result of the comparative test. Mean reading time per slide was recorded and cost of each slide was calculated. Mycobacteria culture served as the reference standard.

Results

Among 404 tuberculosis suspects from the outpatient clinic and 256 from the HIV clinic, mycobacteria culture was positive in 12.6% and 27%, respectively. The optimal sensitivity of LED-FM was achieved by using a threshold of ≥2 AFB/length. LED-FM had a higher sensitivity (75.5% vs. 54.9%, P<0.01) but lower specificity (90.0% vs 96.6%, P<0.01) compared to ZN microscopy. HIV was associated with a lower sensitivity but similar specificity. The average reading time using LED-FM was significantly shorter (2.23±0.78 vs 5.82±1.60 minutes, P<0.01), while costs per slide were similar.

Conclusion

High sensitivity of LED-FM combined with shorter reading time of sputum smear slides make this method a potential alternative to ZN microscopy. Additional data on specificity are needed for effective implementation of this technique in high burden TB laboratories.     

Genetic substructure in cynomolgus macaques (Macaca fascicularis) on the island of Mauritius

Background

Nonhuman primates are commonly used in biomedical research as animal models of human disease and behavior. Compared to common rodent models, nonhuman primates are genetically, physiologically, behaviorally and neurologically more similar to humans owing to more recent shared ancestry and therefore provide the advantage of greater translational validity in preclinical studies. The cynomolgus macaque (Macaca fascicularis) is one of the most commonly used nonhuman primates in academic and industry settings, yet population genetic research has revealed significant substructure throughout the species distribution that may confound studies. Cynomolgus monkeys introduced to Mauritius specifically have previously been thought to maintain the least genetic heterogeneity of all cynomolgus monkeys, although recent work, including work from our lab, suggests macaques from Mauritius too may harbor cryptic substructure.

Results

To evaluate putative substructure in Mauritian cynomolgus macaques, we designed a panel of 96 single nucleotide polymorphisms based on preliminary findings from previous work to screen 246 of cynomolgus monkeys from two primary suppliers. Results from this study support substructure in Mauritian macaques and suggest a minimum of two populations and maybe three on Mauritius, with moderate admixture.

Conclusion

These findings inform the natural history of these monkeys suggesting either a previously unrecognized physical or ecological barrier to gene flow on Mauritius and/or the breakdown of historic substructure resulting from the history of macaque introduction to the island. These findings are relevant to ongoing research using these models in part because of increased appreciation of segregating common variation with functional effects and may be used to better inform animal selection in preclinical research.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-748) contains supplementary material, which is available to authorized users.     

Extraction of hermit crabs from their shells by white-faced capuchin monkeys (<Emphasis Type="Italic">Cebus capucinus</Emphasis>)

We observed two capuchin monkeys (Cebus capucinus) feeding on hermit crabs (Coenobita compressus) on the coast, and the tactics they used to extract this well-protected prey. The observations took place during the dry season at Playa Escondida beach, Puntarenas, Costa Rica. The capuchins descended from trees at the back edge of the beach to capture passing hermit crabs. Both capuchins extracted the hermit crabs from their protective shells by holding the shell with one hand and pulling the crab out with the other. Even though this was accomplished within seconds, the extraction of hermit crabs from their shells did not appear to be a straightforward task. Once the capuchins succeeded in pulling the crabs out of their shells, they consumed the soft abdomen and discarded the rest of the crab's body. To our knowledge, the consumption of hermit crabs has not been previously reported for any capuchin monkey (Cebus or Sapajus). Our observations provide a new example of extractive foraging by capuchins, and thus an additional natural context for which fine motor skills (which are highly developed in capuchins) are necessary.