Patrícia Izar

Watching the best nutcrackers: what capuchin monkeys (Cebus apella) know about others’ tool-using skills

The present work is part of a decade-long study on the spontaneous use of stones for cracking hard-shelled nuts by a semi-free-ranging group of brown capuchin monkeys (Cebus apella). Nutcracking events are frequently watched by other individuals - usually younger, less proficient, and that are well tolerated to the point of some scrounging being allowed by the nutcracker. Here we report findings showing that the choice of observational targets is an active, non-random process, and that observers seem to have some understanding of the relative proficiency of their group mates, preferentially watching the more skilled nutcrackers, which enhances not only scrounging payoffs, but also social learning opportunities.

Female social relationships of cebus apella nigritus in a southeastern Atlantic forest: An analysis through ecological models of primate social evolution

Theoretical models about female relationships within primate social groups hypothesise that food abundance and distribution are important factors determining the variation of patterns observed among species and populations. Despite some common premises, models formulated by van Schaik (1989) and Sterck et al. (1997) and by Isbell (1991) differ with respect to the importance of predation risk, the co-variation of contest and scramble competition and causes of female dispersal. In this study, data from a population of Cebus apella nigritus from Brazilian Atlantic Forest are analysed using predictions from these models. Competition among females, both within and between groups, is strong and related to food abundance and distribution. Females can transfer between groups, as well as males. Female dispersal is related to a significant reduction in per capita energy intake by group foragers during fruit scarcity periods. The data from this study are not conclusive about the importance of predation in causing variation of female relationships but favour the assumption from van Schaik and Sterck et al. that contest and scramble competition within and between groups can vary independently; and also favour the formulation from Isbell & Van Vuren (1996) on female dispersal. The exact pattern of female social relationships is not sufficiently explained by ecological causes alone. Social benefits provided by the dominant male also seem to be important.

The fourth dimension of tool use: temporally enduring artefacts aid primates learning to use tools

All investigated cases of habitual tool use in wild chimpanzees and capuchin monkeys include youngsters encountering durable artefacts, most often in a supportive social context. We propose that enduring artefacts associated with tool use, such as previously used tools, partly processed food items and residual material from previous activity, aid non-human primates to learn to use tools, and to develop expertise in their use, thus contributing to traditional technologies in non-humans. Therefore, social contributions to tool use can be considered as situated in the three dimensions of Euclidean space, and in the fourth dimension of time. This notion expands the contribution of social context to learning a skill beyond the immediate presence of a model nearby. We provide examples supporting this hypothesis from wild bearded capuchin monkeys and chimpanzees, and suggest avenues for future research.

Kinematics and Energetics of Nut-Cracking in Wild Capuchin Monkeys (Cebus libidinosus) in Piaui´, Brazil

Wild bearded capuchins (Cebus libidinosus, quadrupedal, medium-sized monkeys) crack nuts using large stones. We examined the kinematics and energetics of the nut-cracking action of two adult males and two adult females. From a bipedal stance, the monkeys raised a heavy hammer stone (1.46 and 1.32 kg, from 33 to 77% of their body weight) to an average height of 0.33 m, 60% of body length. Then, they rapidly lowered the stone by flexing the lower extremities and the trunk until the stone contacted the nut. A hit consisting of an upward phase and a downward phase averaged 0.74 s in duration. The upward phase lasted 69% of hit duration. All subjects added discernable energy to the stone in the downward phase. The monkeys exhibited individualized kinematic strategies, similar to those of human weight lifters. Capuchins illustrate that human-like bipedal stance and large body size are unnecessary to break tough objects from a bipedal position. The phenomenon of bipedal nut-cracking by capuchins provides a new comparative reference point for discussions of percussive tool use and bipedality in primates.

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. Am. J. Primatol. 70:884–891, 2008.

How wild bearded capuchin monkeys select stones and nuts to minimize the number of strikes per nut cracked

Wild bearded capuchin monkeys, Cebus libidinosus, use stone tools to crack palm nuts to obtain the kernel. In five experiments, we gave 10 monkeys from one wild group of bearded capuchins a choice of two nuts differing in resistance and size and/or two manufactured stones of the same shape, volume and composition but different mass. Monkeys consistently selected the nut that was easier to crack and the heavier stone. When choosing between two stones differing in mass by a ratio of 1.3:1, monkeys frequently touched the stones or tapped them with their fingers or with a nut. They showed these behaviours more frequently before making their first selection of a stone than afterward. These results suggest that capuchins discriminate between nuts and between stones, selecting materials that allow them to crack nuts with fewer strikes, and generate exploratory behaviours to discriminate stones of varying mass. In the final experiment, humans effectively discriminated the mass of stones using the same tapping and handling behaviours as capuchins. Capuchins explore objects in ways that allow them to perceive invariant properties (e.g. mass) of objects, enabling selection of objects for specific uses. We predict that species that use tools will generate behaviours that reveal invariant properties of objects such as mass; species that do not use tools are less likely to explore objects in this way. The precision with which individuals can judge invariant properties may differ considerably, and this also should predict prevalence of tool use across 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.

Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus.

Socioecological models assume that primates adapt their social behavior to ecological conditions, and predict that food availability and distribution, predation risk and risk of infanticide by males affect patterns of social organization, social structure and mating system of primates. However, adaptability and variation of social behavior may be constrained by conservative adaptations and by phylogenetic inertia. The comparative study of closely related species can help to identify the relative contribution of ecological and of genetic determinants to primate social systems. We compared ecological features and social behavior of two species of the genus Sapajus, S. nigritus in Carlos Botelho State Park, an area of Atlantic Forest in São Paulo state, and S. libidinosus in Fazenda Boa Vista, a semi‐arid habitat in Piauí state, Brazil. S. libidinosus perceived higher predation risk and fed on clumped, high quality, and usurpable resources (fruits) all year round, whereas S. nigritus perceived lower predation risk and relied on evenly distributed, low‐quality food sources (leaves) during periods of fruit shortage. As predicted by socioecology models, S. libidinosus females were philopatric and established linear and stable dominance hierarchies, coalitions, and grooming relationships. S. nigritus females competed less often, and could transfer between groups, which might explain the lack of coalitions and grooming bonds among them. Both populations presented similar group size and composition and the same polygynous mating system. The species differed from each other in accordance with differences in the characteristics of their main food sources, as predicted by socioecological models, suggesting that phylogenetic inertia does not constrain social relationships established among female Sapajus. The similarity in mating systems indicates that this element of the social system is not affected by ecological variables and thus, is a more conservative behavioral feature of the genus Sapajus. Am. J. Primatol. 74:315–331, 2012.

Wild bearded capuchin monkeys (Cebus libidinosus) place nuts in anvils selectively

Are wild bearded capuchin monkeys selective about where they place nuts on anvils, specifically the anvil pits, during nut cracking? In the present study, we examined (1) whether capuchins’ preferences for particular pits are influenced by the effectiveness of the pit in cracking the nut and/or by the stability of the nut during striking, (2) how capuchins detect the affordances of novel pits and (3) the influence of social context on their selections. Anvil pits varied in horizontal dimension (small, medium and large) in experiment 1 and in depth (shallow, medium and deep) in experiment 2. In both experiments, three different pits were simultaneously presented, each on one anvil. We coded the capuchins’ actions with the nut in each pit, and recorded the outcome of each strike. In both experiments, capuchins preferred the most effective pit, but not the most stabilizing pit, based on the number of first strikes, total strikes and nuts cracked. Their choice also reflected where the preceding individual had last struck. The capuchins explored the pits indirectly, placing nuts in them and striking nuts with a stone. The preference for pits was weaker than the preference for nuts and stones shown previously with the same monkeys. Our findings suggest that detecting affordances of pits through indirect action is less precise than through direct action, and that social context may also influence selection. We show that field experiments can demonstrate embodied cognition in species-typical activities in natural environments.

Socioecology of wild bearded capuchin monkeys (Sapajus libidinosus): an analysis of social relationships among female primates that use tools in feeding

Socioecology considers that the features of food sources affect female social relationships in group-living species. Among primates, the tests of socioecological models are largely focused on Old World species and do not evaluate if the use of feeding tools affects the competitive regime over food and females’ relations in wild populations. We studied female social relationships among a wild population of bearded capuchins monkeys (Sapajus libidinosus) that use percussive tools (stones) to crack encased foods, in a semi-arid habitat in Brazil. Females fed mainly on clumped, high quality resources, indicating that the habitat provides a high quality diet year-round. Females experienced contest competition within and between-groups. As predicted by socioecological models, females’ social relationships were characterized by philopatry, linear dominance hierarchies, coalitions, and tolerance in feeding bouts. Females spent a small proportion of their feeding time using tools. Nevertheless, tool sites generated high rates of contest competition and lower indices of tolerance among females. Although the social structure of our study population did not differ significantly from the pattern observed in wild populations of Sapajus that do not use tools, tool use increased within-group contest competition and apparently contributed to the linearity of the dominance hierarchies established among females. We predict that when tool use results in usurpable food resources, it will increase contest competition within group-living species.