How to crack nuts: acquisition process in captive chimpanzees (Pan troglodytes) observing a model

Stone tool use for nut cracking consists of placing a hard-shelled nut onto a stone anvil and then cracking the shell open by pounding it with a stone hammer to get to the kernel. We investigated the acquisition of tool use for nut cracking in a group of captive chimpanzees to clarify what kind of understanding of the tools and actions will lead to the acquisition of this type of tool use in the presence of a skilled model. A human experimenter trained a male chimpanzee until he mastered the use of a hammer and anvil stone to crack open macadamia nuts. He was then put in a nut-cracking situation together with his group mates, who were naïve to this tool use; we did not have a control group without a model. The results showed that the process of acquisition could be broken down into several steps, including recognition of applying pressure to the nut, emergence of the use of a combination of three objects, emergence of the hitting action, using a tool for hitting, and hitting the nut. The chimpanzees recognized these different components separately and practiced them one after another. They gradually united these factors in their behavior leading to their first success. Their behavior did not clearly improve immediately after observing successful nut cracking by a peer, but observation of a skilled group member seemed to have a gradual, long-term influence on the acquisition of nut cracking by naïve chimpanzees.     

Ontogeny of manipulative behavior and nut‐cracking in young tufted capuchin monkeys (Cebus apella): a Perception–action perspective

How do capuchin monkeys learn to use stones to crack open nuts? Perception–action theory posits that individuals explore producing varying spatial and force relations among objects and surfaces, thereby learning about affordances of such relations and how to produce them. Such learning supports the discovery of tool use. We present longitudinal developmental data from semifree‐ranging tufted capuchin monkeys (Cebus apella) to evaluate predictions arising from Perception–action theory linking manipulative development and the onset of tool‐using. Percussive actions bringing an object into contact with a surface appeared within the first year of life. Most infants readily struck nuts and other objects against stones or other surfaces from 6 months of age, but percussive actions alone were not sufficient to produce nut‐cracking sequences. Placing the nut on the anvil surface and then releasing it, so that it could be struck with a stone, was the last element necessary for nut‐cracking to appear in capuchins. Young chimpanzees may face a different challenge in learning to crack nuts: they readily place objects on surfaces and release them, but rarely vigorously strike objects against surfaces or other objects. Thus the challenges facing the two species in developing the same behavior (nut‐cracking using a stone hammer and an anvil) may be quite different. Capuchins must inhibit a strong bias to hold nuts so that they can release them; chimpanzees must generate a percussive action rather than a gentle placing action. Generating the right actions may be as challenging as achieving the right sequence of actions in both species. Our analysis suggests a new direction for studies of social influence on young primates learning sequences of actions involving manipulation of objects in relation to surfaces.     

Wild bearded capuchin (Sapajus libidinosus) select hammer tools on the basis of both stone mass and distance from the anvil

Contemporary optimization models suggest that animals optimize benefits of foraging and minimize its costs. For wild bearded capuchins (Sapajus libidinosus), nut-cracking entails cost related to lifting the heavy stone and striking the nut and additional cost to transport the stone if it is not already on the anvil. To assess the role of stone mass and transport distance in capuchins’ tool selection, we carried out three field experiments. In Experiment 1, we investigated whether transport distance affected choice of a tool by positioning two stones of the same mass close and far from the anvil. Capuchins consistently selected the closer stone, effectively reducing transport costs. In Experiment 2, we examined the trade-off between the cost of transport and the effectiveness in cracking by positioning two stones of different mass close and far from the anvil. Most subjects significantly preferred the closer stone, regardless of mass, whereas others preferred the heavier stone regardless of transport distance. In Experiment 3, we changed transport distance of both stones while maintaining the same distance ratios as in Experiment 2. Capuchins maintained the preferences expressed in Experiment 2, with the exception of one subject. Overall, our findings indicate that (1) individuals vary in their sensitivity to distance of transport, (2) a few meters are perceived as a substantive cost by some monkeys, and (3) monkeys’ body mass affects their decisions. We also developed a non-dimensional Preference index (P) defined as a function of the stone mass and the transport distance to describe monkey’s choice.     

Transport of tools to food sites in tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Tool use and transport represent cognitively important aspects of early hominid evolution, and nonhuman primates are often used as models to examine the cognitive, ecological, morphological and social correlates of these behaviors in order to gain insights into the behavior of our early human ancestors. In 2001, Jalles-Filho et al. found that free-ranging capuchin monkeys failed to transport tools (stones) to food sites (nuts), but transported the foods to the tool sites. This result cast doubt on the usefulness of Cebus to model early human tool-using behavior. In this study, we examined the performance of six captive tufted capuchin monkeys (Cebus apella) in a tool transport task. Subjects were provided with the opportunity to transport two different tools to fixed food reward sites when the food reward was visible from the tool site and when the food reward was not visible from the tool site. We found that the subjects quickly and readily transported probing tools to an apparatus baited with syrup, but rarely transported stones to a nut-cracking apparatus. We suggest that the performance of the capuchins here reflects an efficient foraging strategy, in terms of energy return, among wild Cebus monkeys.     

Manipulation of walnuts to facilitate opening by the great spotted woodpecker (Picoides major): is it tool use?

True tool use has been documented in some bird species, but to our knowledge, it has not been shown in woodpeckers. Here, we investigated the ability of Picoides major to open nuts of Juglans mandshurica by consistently inserting walnuts between tree branches in a specific position that facilitated nut opening. As seen in these birds, we showed that woodpeckers removed 96 % of the nuts of J. mandshurica from experimental seed trays and inserted each nut in a precise position that specifically allowed nut cracking. When we inserted nuts in an alternative position, woodpeckers manipulated and repositioned nuts to allow nut opening. In contrast, when we inserted the nuts in positions preferred for nut opening, woodpeckers did not alter their position and instead opened the nuts. We suggest that the origin of this behavior, as in other forms of tool use, likely requires a higher cognitive ability in these birds.     

Severity of agonism of free-ranging patas monkeys differs according to the composition of dyads

Differences in the severity of behavior used in dyadic agonistic interactions of adult female and immature free-ranging patas monkeys (Erythrocebus patas) were assessed. The behaviors exhibited were rank-ordered according to severity. Analysis of data from 1,353 agonistic interactions indicated a significant difference in the severity of agonistic behaviors, based on the composition of the dyad. Interactions between two adult females contained the least severe agonism, whereas interactions between two immature monkeys contained the most severe agonistic behaviors. When adult females and immatures interacted agonistically, the severity of the behaviors emitted and received were related to the age of the immature monkey; the older the immature, the less severe were the agonistic behaviors. These results support the ideas that social stability mediates the severity of agonism, and that agonism serves a socializing function. © 1994 Wiley-Liss, Inc.     

Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments

Chimpanzees (Pan troglodytes) are the most proficient and versatile users of tools in the wild. How such skills become integrated into the behavioural repertoire of wild chimpanzee communities is investigated here by drawing together evidence from three complementary approaches in a group of oil-palm nut- (Elaeis guineensis) cracking chimpanzees at Bossou, Guinea. First, extensive surveys of communities adjacent to Bossou have shown that population-specific details of tool use, such as the selection of species of nuts as targets for cracking, cannot be explained purely on the basis of ecological differences. Second, a 16-year longitudinal record tracing the development of nut-cracking in individual chimpanzees has highlighted the importance of a critical period for learning (3–5 years of age), while the similar learning contexts experienced by siblings have been found to result in near-perfect (13 out of 14 dyads) inter-sibling correspondence in laterality. Third, novel data from field experiments involving the introduction of unfamiliar species of nuts to the Bossou group illuminates key aspects of both cultural innovation and transmission. We show that responses of individuals toward the novel items differ markedly with age, with juveniles being the most likely to explore. Furthermore, subjects are highly specific in their selection of conspecifics as models for observation, attending to the nut-cracking activities of individuals in the same age group or older, but not younger than themselves. Together with the phenomenon of inter-community migration, these results demonstrate a mechanism for the emergence of culture in wild chimpanzees.     

Social learning of nut-cracking behavior in East African sanctuary-living chimpanzees (Pan troglodytes schweinfurthii)

Nut cracking is restricted to communities of wild chimpanzees living in West Africa, suggesting it is an example of a socially transmitted tradition. Detailed study of the acquisition of nut cracking in wild chimpanzees is consistent with this conclusion. However, only 2, small-scale experiments have been carried out in captivity to explore the role of social transmission in the acquisition of this behavior. The study presented here does this with a comparatively larger, statistically viable sample of 11 sanctuary-living chimpanzees (Pan troglodytes schweinfurthii), permitting both between- and within-subjects experimental manipulations. Results confirmed that nut cracking can be acquired in a matter of days by social learning, but only in chimpanzees 3 to 4 years old and older. Direct comparisons are made with a study carried out in the wild, revealing striking similarities in developmental profiles.     

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.     

Tool-composite reuse in wild chimpanzees (Pan troglodytes): archaeologically invisible steps in the technological evolution of early hominins?

Recent etho-archaeological studies of stone-tool use by wild chimpanzees have contributed valuable data towards elucidating the variables that influenced the emergence and development of the first lithic industries among Plio-Pleistocene hominins. Such data help to identify potential behaviours entailed in the first percussive technologies that are invisible in archaeological records. The long-term research site of Bossou in Guinea features a unique chimpanzee community whose members systematically use portable stones as hammers and anvils to crack open nuts in natural as well as in field experimental settings. Here we present the first analysis of repeated reuse of the same tool-composites in wild chimpanzees. Data collected over 5 years of experimental nut-cracking sessions at an “outdoor laboratory” site were assessed for the existence of systematic patterns in the selection of tool-composites, at group and at individual levels. Chimpanzees combined certain stones as hammer and anvil more often than expected by chance, even when taking into account preferences for individual stones by themselves. This may reflect an ability to recognise the nut-cracker as a single tool (composed of two elements, but functional only as a whole), as well as discrimination of tool quality-effectiveness. Through repeatedly combining the same pairs of stones—whether due to preferences for particular composites or for the two elements independently—tool-users may amplify use-wear traces and increase the likelihood of fracturing the stones, and thus of detaching pieces by battering.     

Stone-Tool Use in Wild Monkeys: Implications for the Study of the Body-Plus-Tool System

Handheld tools transform the actor's body into a body-plus-tool system such that the fit of the actor's body, the tool, and the task demand channel movement in action. In this study, we performed a biomechanical analysis of percussive actions in wild bearded capuchin monkeys, Sapajus libidinosus at Fazenda Boa Vista, Brazil, as they cracked open tucum nuts with anvil-and-hammer tools from the frame of reference of the body-plus-tool system. The ratio of hammer mass to body mass—the “body-scaled hammer mass”—influenced the monkeys' actions with a hammer and their performance in cracking nuts. Both body mass and hammer mass did not independently influence the monkeys' actions with a hammer and their performance in cracking nuts. These findings support the hypothesis that the properties of the body-plus-tool system are not simply the sum of the properties of the body and the tool.     

Maternal gestational stress alters adaptive and social behavior in adolescent rhesus monkey offspring

Data from rodent studies have indicated that stress experienced by pregnant mothers may result in behavioral and biological abnormalities in their offspring. However, few studies have examined the effects of prenatal stress on the offspring beyond the childhood period. In this study, 7 prenatally stressed (PNS) monkeys and 7 monkeys from undisturbed pregnancies were tested under mildly challenging conditions at 4 years of age. Following separation from cagemates and group formation, PNS monkeys showed more locomotion, abnormal and disturbance behavior than controls. Controls showed approximately six times more play than PNS animals. The PNS males showed the most clinging to others and the largest increase in contact with other animals over the period. Group differences were also found when the monkeys were observed as groups or alone in a playroom. Controls showed more explanatory behavior in the playroom, whereas PNS monkeys showed more inactivity. Control animals showed a decrease in distress vocalizations over time in the playroom, whereas PNS animals showed the opposite pattern. Control animals spent more time in proximity to and contact with cagemates than PNS animals. These results indicate that prenatal stress can have effects on adaptive and social behavior that persist into adolescence.     

Field dependent eating and perception as a function of weight and sex

It was hypothesized that the greater influence of external cues on obese than on normal individuals' eating behavior is a manifestation of a generalized sensitivity to external cues. Responsivity of nut consumption to the external cue of shells on the nuts and responsivity of judgment of verticality to the external cue of a tilted visual field were assessed for male and female, obese and normal-weight subjects. As predicted, both obese subjects' nut consumption and their judgments of verticality were more influenced by external cues than were those of normals. Females' judgments of verticality were more influenced by external cues than males' were, but the sex differences in eating behavior were not statistically significant. A significant correlation between the field dependence of subjects' eating behavior and their judgments of verticality suggests that a single cause may generate sensitivity to external cues in these two diverse situations.     

Cognitions and behavior in asymmetric social dilemmas: a comparison of two cultures

This study investigated whether cognitions and behavior in an asymmetric social dilemma can be predicted by national culture. Results indicated that, as predicted, groups of decision makers from Japan--a collectivist, hierarchical culture-were more cooperative, expected others to be more cooperative, and were more likely to adopt an equal allocation distribution rule to resolve the dilemma than were groups of decision makers from the United States-an individualist, egalitarian culture. An opportunity for communication had a greater impact on expectations of others' behavior in groups of U.S. decision makers than in groups of Japanese decision makers.     

Effect of an observer's presence on facial behavior during dyadic communication

In everyday life, people communicate not only with another person but also in front of other people. How do people behave during communication when observed by others? Effects of an observer (presence vs absence) and interpersonal relationship (friends vs strangers vs alone) on facial behavior were examined. Participants viewed film clips that elicited positive affect (film presentation) and discussed their impressions about the clips (conversation). Participants rated their subjective emotions and social motives. Durations of smiles, gazes, and utterances of each participant were coded. The presence of an observer did not affect facial behavior during the film presentation, but did affect gazes during conversation. Whereas the presence of an observer seemed to facilitate affiliation in pairs of strangers, communication between friends was exclusive and not affected by an observer.     

Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) show robust evidence for memory awareness across multiple generalization tests

The possibility that memory awareness occurs in nonhuman animals has been evaluated by providing opportunity to decline memory tests. Current evidence suggests that rhesus monkeys (Macaca mulatta) selectively decline tests when memory is weak (Hampton in Proc Natl Acad Sci USA 98:5359–5362, 2001; Smith et al. in Behav Brain Sci 26:317–374, 2003). However, much of the existing research in nonhuman metacognition is subject to the criticism that, after considerable training on one test type, subjects learn to decline difficult trials based on associative learning of external test-specific contingencies rather than by evaluating the private status of memory or other cognitive states. We evaluated whether such test-specific associations could account for performance by presenting monkeys with a series of generalization tests across which no single association with external stimuli was likely to adaptively control use of the decline response. Six monkeys performed a four alternative delayed matching to location task and were significantly more accurate on trials with a decline option available than on trials without it, indicating that subjects selectively declined tests when memory was weak. Monkeys transferred appropriate use of the decline response under three conditions that assessed generalization: two tests that weakened memory and one test that enhanced memory in a novel way. Bidirectional generalization indicates that use of the decline response by monkeys is not controlled by specific external stimuli but is rather a flexible behavior based on a private assessment of memory.     

Horse sense: social status of horses (<Emphasis Type="Italic">Equus caballus</Emphasis>) affects their likelihood of copying other horses’ behavior

Animals that live in stable social groups need to gather information on their own relative position in the group's social hierarchy, by either directly threatening or by challenging others, or indirectly and in a less perilous manner , by observing interactions among others. Indirect inference of dominance relationships has previously been reported from primates, rats, birds, and fish. Here, we show that domestic horses, Equus caballus, are similarly capable of social cognition. Taking advantage of a specific "following behavior" that horses show towards humans in a riding arena, we investigated whether bystander horses adjust their response to an experimenter according to the observed interaction and their own dominance relationship with the horse whose reaction to the experimenter they had observed before. Horses copied the "following behavior" towards an experimenter after watching a dominant horse following but did not follow after observing a subordinate horse or a horse from another social group doing so. The "following behavior," which horses show towards an experimenter, therefore appears to be affected by the demonstrator's behavior and social status relative to the observer.     

Implicit self-theories of shyness

Three studies examined implicit self-theories in relation to shy people's goals, responses, and consequences within social situations. Shy incremental theorists were more likely than shy entity theorists to view social situations as a learning opportunity and to approach social settings (Study 1). Shy incremental theorists were less likely to use strategies aimed at avoiding social interaction (Studies 2 and 3) and suffered fewer negative consequences of their shyness (Study 3). These findings generalized across both hypothetical and actual social situations as well as both self-reports and observer reports and could not be attributed to individual differences in level of shyness. Together, these studies indicate that implicit self-theories of shyness are important for understanding individual differences among shy people and suggest new avenues for implicit self-theories research.     

Social processes in communication and cognition in callitrichid monkeys: a review

Studies of vocal development in nonhuman primates have found little evidence for plasticity in vocal production, somewhat more for usage of calls, with the greatest plasticity arising in response to calls of others. Generally, similar results were obtained with callitrichid monkeys, the marmosets and tamarins, but with several interesting exceptions. Infant pygmy marmosets show babbling behavior with improvement in adult call structure related to the amount and diversity of babbling. Adult marmosets alter call structure in response to changes in social partners, and wild marmosets have vocal dialects and modify call structure according to how far they are from other group members, suggesting the potential to modify call structure in different social and environmental contexts, though direct learning of novel vocalizations has not been observed. Infant cotton-top tamarins do not produce adult-like calls in appropriate contexts, at least in the first few months of life, but through food sharing from adults infants learn about appropriate foods and the appropriate contexts for food vocalizations. Tamarins modify call structure and usage with changes in social status. Tamarins, unlike other monkeys tested, can learn to avoid noxious foods through observation of other group members, and can learn about novel food locations. Recent studies provide evidence of contextual imitation in marmosets. The plasticity in vocal communication and evidence of social learning in marmosets and tamarins relative to other monkeys may be related to the cooperative breeding system of marmosets and tamarins. With a high degree of behavioral coordination among group members, there is a priority on monitoring signals and behavior of others and adjusting one's own signals and behavior. This creates the context for vocal plasticity and social learning. Accepted after revision: 23 May 2001 Electronic Publication