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.     

When and where to practice: social influences on the development of nut-cracking in bearded capuchins (<Emphasis Type="Italic">Sapajus libidinosus</Emphasis>)

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.     

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.     

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.     

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.     

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.     

‘Unwilling’ versus ‘unable’: capuchin monkeys’ (Cebus apella) understanding of human intentional action

A sensitivity to the intentions behind human action is a crucial developmental achievement in infants. Is this intention reading ability a unique and relatively recent product of human evolution and culture, or does this capacity instead have roots in our non‐human primate ancestors? Recent work by Call and colleagues (2004) lends credence to the latter hypothesis, providing evidence that chimpanzees are also sensitive to human intentions. Specifically, chimpanzees remained in a testing area longer and exhibited fewer frustration behaviors when an experimenter behaved as if he intended to give food but was unable to do so, than when the experimenter behaved as if he had no intention of giving food. The present research builds on and extends this paradigm, providing some of the first evidence of intention reading in a more distant primate relative, the capuchin monkey (Cebus apella). Like chimpanzees, capuchin monkeys distinguish between different goal‐directed acts, vacating an enclosure sooner when an experimenter acts unwilling to give food than when she acts unable to give food. Additionally, we found that this pattern is specific to animate action, and does not obtain when the same actions are performed by inanimate rods instead of human hands (for a similar logic, see Woodward, 1998 ). Taken together with the previous evidence, the present research suggests that our own intention reading is not a wholly unique aspect of the human species, but rather is shared broadly across the primate order.     

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.     

Parallels Between Action‐Object Mapping and Word‐Object Mapping in Young Children

Across a series of four experiments with 3‐ to 4‐year‐olds we demonstrate how cognitive mechanisms supporting noun learning extend to the mapping of actions to objects. In Experiment 1 (n = 61) the demonstration of a novel action led children to select a novel, rather than a familiar object. In Experiment 2 (n = 78) children exhibited long‐term retention of novel action‐object mappings and extended these actions to other category members. In Experiment 3 (n = 60) we showed that children formed an accurate sensorimotor record of the novel action. In Experiment 4 (n = 54) we demonstrate limits on the types of actions mapped to novel objects. Overall these data suggest that certain aspects of noun mapping share common processing with action mapping and support a domain‐general account of word learning.     

Navigating two-dimensional mazes: chimpanzees (Pan troglodytes) and capuchins (Cebus apella sp.) profit from experience differently

We examined whether navigation is impacted by experience in two species of nonhuman primates. Five chimpanzees (Pan troglodytes) and seven capuchin monkeys (Cebus apella) navigated a cursor, using a joystick, through two-dimensional mazes presented on a computer monitor. Subjects completed 192 mazes, each one time. Each maze contained one to five choices, and in up to three of these choices, the correct path required moving the cursor away from the Euclidean direction toward the goal. Some subjects completed these mazes in a random order (Random group); others in a fixed order by ascending number of choices and ascending number of turns away from goal (Ordered group). Chimpanzees in both groups performed equivalently, demonstrated fewer errors and a higher rate of self-correcting errors with increasing experience at solving the mazes, and made significantly fewer errors than capuchin monkeys. Capuchins were more sensitive to the mode of presentation than chimpanzees; monkeys in the Ordered group made fewer errors than monkeys in the Random group. However, capuchins’ performance across testing changed little, and they remained particularly susceptible to making errors when the correct path required moving away from the goal. Thus, these two species responded differently to the same spatial challenges and same learning contexts. The findings indicate that chimpanzees have a strong advantage in this task compared to capuchins, no matter how the task is presented. We suggest that differences between the species in the dynamic organization of attention and motor processes contribute to their differences in performance on this task, and predict similar differences in other tasks requiring, as this one does, sustained attention to a dynamic visual display and self-produced movements variably towards and away from a goal.     

What limits tool use in nonhuman primates? Insights from tufted capuchin monkeys (Sapajus spp.) and chimpanzees (Pan troglodytes) aligning three-dimensional objects to a surface

Perceptuomotor functions that support using hand tools can be examined in other manipulation tasks, such as alignment of objects to surfaces. We examined tufted capuchin monkeys’ and chimpanzees’ performance at aligning objects to surfaces while managing one or two spatial relations to do so. We presented six subjects of each species with a single stick to place into a groove, two sticks of equal length to place into two grooves, or two sticks joined as a T to place into a T-shaped groove. Tufted capuchins and chimpanzees performed equivalently on these tasks, aligning the straight stick to within 22.5° of parallel to the groove in approximately half of their attempts to place it, and taking more attempts to place the T stick than two straight sticks. The findings provide strong evidence that tufted capuchins and chimpanzees do not reliably align even one prominent axial feature of an object to a surface, and that managing two concurrent allocentric spatial relations in an alignment problem is significantly more challenging to them than managing two sequential relations. In contrast, humans from 2 years of age display very different perceptuomotor abilities in a similar task: they align sticks to a groove reliably on each attempt, and they readily manage two allocentric spatial relations concurrently. Limitations in aligning objects and in managing two or more relations at a time significantly constrain how nonhuman primates can use hand tools.     

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.     

Concept learning set‐size functions for Clark's nutcrackers

Same/Different abstract‐concept learning by Clark's nutcrackers (Nucifraga columbiana) was tested with novel stimuli following learning of training set expansion (8, 16, 32, 64, 128, 256, 512, and 1024 picture items). The resulting set‐size function was compared to those from rhesus monkeys (Macaca mulatta), capuchin monkeys (Cebus apella), and pigeons (Columba livia). Nutcrackers showed partial concept learning following initial eight‐item set learning, unlike the other species (Magnotti, Katz, Wright, & Kelly, 2015). The mean function for the nutcrackers' novel‐stimulus transfer increased linearly as a function of the logarithm of training set size, which intersected its baseline function at the 128‐item set size. Thus, nutcrackers on average achieved full concept learning (i.e., transfer statistically equivalent to baseline performance) somewhere between set sizes of 64 to 128 items, similar to full concept learning by monkeys. Pigeons required a somewhat larger training set (256 items) for full concept learning, but results from other experiments (initial training and transfer with 32‐ and 64‐item set sizes) suggested carryover effects with smaller set sizes may have artificially prolonged the pigeon's full concept learning. We find it remarkable that these diverse species with very different neural architectures can fully learn this same/different abstract concept, and (at least under some conditions) do so with roughly similar sets sizes (64‐128 items) and numbers of training exemplars, despite initial concept learning advantages (nutcrackers), learning disadvantages (pigeons), or increasing baselines (monkeys).     

Testing for social learning in the "artificial fruit" processing of wildborn orangutans (Pongo pygmaeus), Tanjung Puting, Indonesia

Social learning about actions, objects and sequencing was investigated in a group of 14 wildborn orangutans (four adult females and ten 3- to 5-year-old juveniles). Human models showed alternative methods and sequences for dismantling an artificial fruit to groups of participants matched by gender and age. Each participant received three to six 2-min trials in which they were given access to the artificial fruit for manipulation. Independent coders, who were unaware of which method each participant had seen, gave confidence ratings and collected action frequencies from watching video recordings of the experimental trials. No significant differences were found between groups in terms of the coders' confidence ratings, the action frequencies or the sequence of manipulations. These negative results may at least partly reflect the immaturity of a large proportion of the participants. A positive correlation was found between age and the degree of matching to the method shown. Although none of the juveniles succeeded in opening the "fruit", two out of the four adults did so and they also seemed to match more closely the sequence of elements touched over successive trials. The results are compared with similar data previously collected from human children, chimpanzees, gorillas, capuchin monkeys and common marmosets. Accepted after revision: 30 July 2001 Electronic Publication     

Delaying gratification for food and tokens in capuchin monkeys (Cebus apella) and chimpanzees (Pan troglodytes): when quantity is salient, symbolic stimuli do not improve performance

Capuchin monkeys have been tested for the capacity to delay gratification for accumulating rewards in recent studies and have exhibited variable results. Meanwhile, chimpanzees have consistently excelled at this task. However, neither species have ever been tested at accumulating symbolic tokens instead of food items, even though previous reports indicate that tokens sometimes facilitate performance in other self-control tasks. Thus, in the present study, we tested capuchin monkeys and chimpanzees for their capacity to delay gratification in a delay maintenance task, in which an experimenter presented items, one at a time, to within reach of an animal for as long as the animal refrained from taking them. In Experiment 1, we assessed how long capuchin monkeys could accumulate items in the delay maintenance task when items were food rewards or tokens exchangeable for food rewards. Monkeys accumulated more food rewards than they did tokens. In Experiment 2, we tested capuchin monkeys and chimpanzees in a similar accumulation test. Whereas capuchins again accumulated more food than tokens, all chimpanzees but one showed no difference in performance in the two conditions. These findings provide additional evidence that chimpanzees exhibit greater self-control capacity in this task than do capuchin monkeys and indicate that symbolic stimuli fail to facilitate delay maintenance when they do not abstract away from the quantitative dimension of the task. This is consistent with previous findings on the effects of symbols on self-control and illuminates what makes accumulation a particularly challenging task.     

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.     

Token mediated tool exchange between tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Three experiments were conducted to test whether a pair of tufted capuchin monkeys (Cebus apella) could generalize their ability to exchange tokens and tool objects with a human experimenter to similar exchanges with a conspecific partner. Monkeys were tested in side-by-side enclosures, one enclosure containing a tool-use apparatus and one or more token(s), and the other enclosure containing one or more tool object(s). The monkeys willingly transferred tokens and tools to a conspecific with little practice. Following a small amount of training, we also found that the monkeys would select situation-appropriate tokens to exchange for specific tools, but did not select appropriate tool objects in response to another monkey’s token transfers. Implications regarding role reversal are discussed.     

Learning from others’ mistakes in capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

We investigated whether tufted capuchin monkeys (Cebus apella) learn from others' mistakes. We prepared three kinds of transparent containers having the same appearance: one that could be opened by the lid, one that could be opened from the bottom, and one that could be opened either way. Using each of the first two one-way-open type containers, the monkeys were trained to copy the human demonstrator's action to open the container and obtain a piece of sweet potato contained therein. After this training, the demonstrator showed the monkeys an action that would open or fail to open the third, two-way-open type container. None of the monkeys reliably opened the container by spontaneously compensating for the demonstrator's failure (Experiment 1). In Experiment 2, the same subjects were trained to correct their own mistakes immediately after failure, before we introduced the same test as in Experiment 1. This experience did not result in subjects using the demonstrator's failure to produce a successful action. In Experiment 3, we placed two monkeys face to face. In this situation, the second monkey was presented with the container after the first monkey failed to open it. As a result, two capuchin monkeys capitalized on the partner's failure to correctly guide his/her behavior. Thus, the monkeys monitored not only the outcome of the others' action, but also that action per se. This result suggests that not only humans and apes, but also monkeys may understand the meaning of others' actions in social learning.     

Is the inversion effect in rhesus monkeys face-specific?

This study investigated the face inversion effect in rhesus monkeys (Macaca mulatta). Face stimuli consisted of ten black-and-white examples of unfamiliar rhesus monkey faces, brown capuchin faces, and human faces. Two non-face categories included ten examples of automobiles and abstract shapes. All stimuli were presented in a sequential matching-to-sample format using an automated joystick-testing paradigm. Subjects performed significantly better on upright than on inverted presentations of automobiles, rhesus monkey and capuchin faces, but not human faces or abstract shapes. These results are inconsistent with data from humans and chimpanzees that show the inversion effect only for categories of stimuli for which subjects have developed expertise. The inversion effect in rhesus monkeys does not appear to be face-specific, and should therefore not be used as a marker of specialized face processing in this species. Received: 18 November 1998 / Accepted after revision: 9 May 1999