Intersection as key locations for bearded capuchin monkeys (Sapajus libidinosus) traveling within a route network.

There is evidence that wild animals are able to recall key locations and associate them with navigational routes. Studies in primate navigation suggest most species navigate through the route network system, using intersections among routes as locations of decision-making. Recent approaches presume that points of directional change may be key locations where animals decide where to go next. Over four consecutive years, we observed how a wild group of bearded capuchin monkeys used a route network system and Change Point locations (CPs) in the Brazilian ecotone of Cerrado-Caatinga. We built 200 daily routes of one wild bearded capuchin group. We used ArcGIS, the Change Point Test, Spatial Analysis in Macroecology (SAM), and statistical models to test the hypothesis that wild bearded capuchins use CPs located along routes in a different fashion than they use the CPs located at intersections of routes. A logistic regression model was used to determine the landscape variables affecting capuchins' directional changes at intersections or along routes. CPs at intersections were important points of travel path changes, whereas CPs along routes represented a zig-zag movement along the routes following the landscape features. CPs at intersections were associated with steeper terrains and shorter distances from important resources, along with better visibility of the home range. Our results support the hypothesis that intersections among routes in the route network system are located at points where monkeys have the best visibility available to make decisions on where to visit next.

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.

Social learning strategies for nut-cracking by tufted capuchin monkeys (Sapajus spp.).

The spontaneous use of stone tools for cracking nuts by tufted capuchin monkeys, now known to be habitual among wild populations in savanna environments, was first described in a semifree group living in the Tietê Ecological Park (SP, Brazil). Nut-cracking at TEP was first observed by our team in 1995 (Ottoni and Mannu in Int J Primatol 22(3):347-358, 2001), and its ontogeny and associated social dynamics, with inexperienced observers highly interested in the activities of proficient individuals, greatly tolerant to scrounging, support hypotheses about social biases on tool-use learning. Here we further analyze the social learning biases, better characterizing: the social context of nut-cracking in which observation by conspecifics occurs, the quality of the nut-cracking behavior itself and whether scrounging may be the motivation behind this behavior. We confirm that the choice of observational targets is an active one; monkeys do not simply observe those who they are socially close to. We investigate social learning strategies, describing how young capuchins choose to observe older, more proficient and dominant individuals during nut-cracking bouts. Monkeys with higher productivity rates were also more frequently targeted by observers, who were tolerated scroungers, further supporting the scrounging hypothesis. Finally, based on changes of the demographic patterns of tool use and observation, we set to retrace data from 14 years of continuous studies. We argue that we have followed the dissemination of the behavior (Transmission Phase) almost from its beginning, when juveniles were the most frequent nutcrackers, to a more common pattern where adults are the most active tool users (Tradition Phase).

Transferability of microsatellites for studies on the social behavior of the tufted capuchin monkey (genus Sapajus).

Because of relevant results that indicated that molecular techniques can provide increased knowledge of animal social systems, they usually complement observational field studies. Despite the great utility of microsatellites, they are not available for all species. Gathering genetic information using microsatellites that were originally designed for other species is a time-saving procedure. The aim of this study was to test the transferability of microsatellites and their usefulness in studies of social behavior of black capuchin monkeys (Sapajus nigritus). We noninvasively sampled adult and subadult black capuchins of three wild groups in southeastern Brazil. Seventeen microsatellites, which were previously designed for and successfully amplified in multiple Neotropical primate species, were tested. Nine of the 17 microsatellite loci tested produced an average of 6.22 alleles (range 2-12) per locus. The allelic richness and the expected heterozygosity for all loci was 5.93 and 0.70, respectively. The combined non-exclusion probability for one candidate parent across all loci was 0.01. The nine microsatellite loci optimized in this study have a great potential for application in studies of social structure and dispersal patterns in S. nigritus populations and in other Neotropical primate species.

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 Piauí, 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.

Characteristics of hammer stones and anvils used by wild bearded capuchin monkeys (Cebus libidinosus) to crack open palm nuts.

Capuchins living in Boa Vista (Piauì, Brazil) crack open hard palm nuts on hard, level surfaces (anvils) using stones (hammers) as percussive tools. This activity leaves diagnostic physical remains: distinctive shallow depressions (pits) on the surface of the anvil, cracked shells, and stone hammers on the anvil. To initiate comparison of percussive stone tool use and interpretation of the artifacts it produces across capuchins, chimpanzees, and hominins, we describe a sample of the anvils and hammer stones used by capuchin monkeys at our site. Anvils (boulders and logs) were located predominantly in the transition zone between the flat open woodland and ridges, in locations that offered some overhead coverage, and with a tree nearby, but not necessarily near palm trees. Anvils contained shallow, hemispherical pits with smooth interiors. Hammers represent a diverse assemblage of ancient rocks that are much harder than the prevailing sedimentary rock out of which they eroded. Hard stones large enough to serve as hammers were more abundant on the anvils than in the surrounding area, indicating that capuchins transport them to the anvils. Capuchins use hammers weighing on average more than 1 kg, a weight that is equivalent to 25-40% of the average body weight for adult males and females. Our findings indicate that capuchins select stones to use as hammers and transport stones and nuts to anvil sites. Wild capuchins provide a new reference point for interpreting early percussive stone tool use in hominins, and a point of comparison with chimpanzees cracking nuts.