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.     

Tool choice on the basis of rigidity in capuchin monkeys

Wild capuchin monkeys select stone tools to crack open nuts on the basis of their weight and friability, two non-visual functional properties. Here, we investigated whether they would select new stick-like tools on the basis of their rigidity. In Experiment 1, subjects faced an out-of-reach reward and a choice of three unfamiliar tools differing in color, diameter, material, and rigidity. In order to retrieve the reward, capuchins needed to select the rigid tool exemplar. Capuchins gathered information regarding tools’ pliability either by (1) manipulating the tools themselves (manipulation condition), (2) observing a human demonstrator repeatedly bending the tools (observation condition), or (3) seeing the tools placed on a platform without any manipulation taking place (visual static condition). Subjects selected the rigid tool above chance levels in both the manipulation and observation conditions, but not in the visual static condition. In Experiment 2, subjects needed to select and use a flexible tool to access a liquid reward (as opposed to the rigid tool, as in previous experiment). Again, capuchins selected above chance levels the appropriate tool (i.e., flexible), thus demonstrating a good appreciation of the relation between the tool properties and the task requirements.     

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.     

Global/local processing of hierarchical visual stimuli in a conflict–choice task by capuchin monkeys (<Emphasis Type="Italic">Sapajus</Emphasis> spp.)

In the last two decades, comparative research has addressed the issue of how the global and local levels of structure of visual stimuli are processed by different species, using Navon-type hierarchical figures, i.e. smaller local elements that form larger global configurations. Determining whether or not the variety of procedures adopted to test different species with hierarchical figures are equivalent is of crucial importance to ensure comparability of results. Among non-human species, global/local processing has been extensively studied in tufted capuchin monkeys using matching-to-sample tasks with hierarchical patterns. Local dominance has emerged consistently in these New World primates. In the present study, we assessed capuchins’ processing of hierarchical stimuli with a method frequently adopted in studies of global/local processing in non-primate species: the conflict–choice task. Different from the matching-to-sample procedure, this task involved processing local and global information retained in long-term memory. Capuchins were trained to discriminate between consistent hierarchical stimuli (similar global and local shape) and then tested with inconsistent hierarchical stimuli (different global and local shapes). We found that capuchins preferred the hierarchical stimuli featuring the correct local elements rather than those with the correct global configuration. This finding confirms that capuchins’ local dominance, typically observed using matching-to-sample procedures, is also expressed as a local preference in the conflict–choice task. Our study adds to the growing body of comparative studies on visual grouping functions by demonstrating that the methods most frequently used in the literature on global/local processing produce analogous results irrespective of extent of the involvement of memory processes.     

Attention to combined attention in new world monkeys (Cebus apella, Saimiri sciureus)

Co-orientation by capuchin (Cebus apella) and squirrel (Saimiri sciureus) monkeys in response to familiar humans abruptly switching the direction of their visual attention was recorded. Co-orientation occurred more frequently overall in capuchins than squirrel monkeys. Capuchins showed a tendency to habituate within trials involving consecutive attention switches performed by 2 different people, whereas squirrel monkeys co-oriented more when the 2nd attention switch was by a 2nd actor. These results suggest variable attention-processing abilities in New World monkeys, including differences in summation of attention by others.     

Intuitive probabilistic inference in capuchin monkeys

The ability to reason about probabilities has ecological relevance for many species. Recent research has shown that both preverbal infants and non-human great apes can make predictions about single-item samples randomly drawn from populations by reasoning about proportions. To further explore the evolutionary origins of this ability, we conducted the first investigation of probabilistic inference in a monkey species (capuchins; Sapajus spp.). Across four experiments, capuchins (N = 19) were presented with two populations of food items that differed in their relative distribution of preferred and non-preferred items, such that one population was more likely to yield a preferred item. In each trial, capuchins had to select between hidden single-item samples randomly drawn from each population. In Experiment 1 each population was homogeneous so reasoning about proportions was not required; Experiments 2–3 replicated previous probabilistic reasoning research with infants and apes; and Experiment 4 was a novel condition untested in other species, providing an important extension to previous work. Results revealed that at least some capuchins were able to make probabilistic inferences via reasoning about proportions as opposed to simpler quantity heuristics. Performance was relatively poor in Experiment 4, so the possibility remains that capuchins may use quantity-based heuristics in some situations, though further work is required to confirm this. Interestingly, performance was not at ceiling in Experiment 1, which did not involve reasoning about proportions, but did involve sampling. This suggests that the sampling task posed demands in addition to reasoning about proportions, possibly related to inhibitory control, working memory, and/or knowledge of object permanence.     

Socially learned preferences for differentially rewarded tokens in the brown capuchin monkey (Cebus apella)

Social learning is assumed to underlie traditions, yet evidence indicating social learning in capuchin monkeys (Cebus apella), which exhibit traditions, is sparse. The authors tested capuchins for their ability to learn the value of novel tokens using a previously familiar token-exchange economy. Capuchins change their preferences in favor of a token worth a high-value food reward after watching a conspecific model exchange 2 differentially rewarded tokens, yet they fail to develop a similar preference after watching tokens paired with foods in the absence of a conspecific model. They also fail to learn that the value of familiar tokens has changed. Information about token value is available in all situations, but capuchins seem to pay more attention in a social situation involving novel tokens.     

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.     

Evaluation of third-party reciprocity by squirrel monkeys (<Emphasis Type="Italic">Saimiri sciureus</Emphasis>) and the question of mechanisms

Social evaluation during third-party interactions emerges early in human ontogeny, and it has been shown in adult capuchin monkeys who witness violations of reciprocity in object exchanges: Monkeys were less inclined to accept food from humans who refused to reciprocate with another human. A recent study reporting similar evidence in marmoset monkeys raised the possibility that such evaluations might be based on species’ inherent cooperativeness. We tested a species not renowned for cooperativeness—squirrel monkeys—using the procedure used with marmosets and found a similar result. This finding rules out any crucial role for cooperative tendencies in monkeys’ responses to unfair exchanges. We then tested squirrel monkeys using procedures more similar to those used in the original study with capuchins. Squirrel monkeys again accepted food less frequently from non-reciprocators, but unlike capuchins, they also strongly preferred reciprocators. We conclude that neither squirrel monkeys nor marmoset monkeys engaged in emotional bookkeeping of the type that probably underlies social evaluation in capuchin monkeys; instead, they employed one or more simple behavioral rules. Further comparative studies are required to clarify the mechanisms underlying social evaluation processes across species.     

Capuchin monkeys (Cebus apella) are sensitive to others’ reward: an experimental analysis of food-choice for conspecifics

The issue whether non-human primates have other-regarding preference and/or inequity aversion has been under debate. We investigated whether tufted capuchin monkeys are sensitive to others’ reward in various experimental food sharing settings. Two monkeys faced each other. The operator monkey chose one of two food containers placed between the participants, each containing a food item for him/herself and another for the recipient. The recipient passively received either high- or low-value food depending on the operator’s choice, whereas the operator obtained the same food regardless of his/her choice. The recipients were either the highest- or lowest-ranking member of the group, and the operators were middle-ranking. In Experiment 1, the operators chose the high-value food for the subordinate recipient more frequently than when there was no recipient, whereas they were indifferent in their choice for the dominant. This differentiated behavior could have been because the dominant recipient frequently ate the low-value food. In Experiment 2, we increased the difference in the value of the two food items so that both recipients would reject the low-value food. The results were the same as in Experiment 1. In Experiment 3, we placed an opaque screen in front of the recipient to examine effects of visual contact between the participants. The operators’ food choice generally shifted toward providing the low-value food for the recipient. These results suggest that capuchins are clearly sensitive to others’ reward and that they show other-regarding preference or a form of inequity aversion depending upon the recipients and the presence of visual contact.     

Identity concept learning in matching-to-sample tasks by tufted capuchin monkeys (Cebus apella)

The abstract concept of equivalence is considered one of the bases of higher-order cognition, and it has been the subject of considerable research in comparative cognition. This study examined the conditions under which tufted capuchin monkeys (Cebus apella) are able to acquire an identity concept. Six capuchin monkeys were trained to solve a visual matching-to-sample (MTS) task on the basis of perceptual identity. The acquisition of the identity rule was inferred from the subject’s ability to solve transfer tests with novel stimuli. We evaluated the ability of the capuchin monkeys to match the shape of novel stimuli after training with both several small stimulus sets (Experiment 1) and a large stimulus set (Experiment 2). Moreover, we examined the ability of capuchins to transfer the concept to novel visual dimensions, such as colour and size and to transfer to novel spatial arrangements of the stimuli (Experiment 2). We demonstrated that the ability of capuchins to match novel stimuli was improved by increasing the number of stimuli used during training (Experiments 1 and 2) and that after a widely applicable identity concept based on the stimulus shape was acquired, the capuchins were able to match stimuli according to an identity rule based on both the colour and size of the stimuli and when the spatial arrangement of the stimuli was varied (Experiment 2). This study is the first to demonstrate that the size of the training set affects the acquisition of an abstract identity concept in an MTS task in non-human primates.     

The sources of skill in seriating cups in children,monkeys and apes

Is a concept of either reversibility or of hierarchical forms of combination necessary for skilled seriation? We examined this question by presenting seriating cups to adult capuchin monkeys and chimpanzees and to 11‐, 16‐ and 21‐month‐old children. Capuchins and chimpanzees consistently created seriated sets with five cups, and placed a sixth cup into a previously seriated set. Children of all three ages created seriated five‐cup sets less consistently than the capuchins and chimpanzees, and were rarely able to place a sixth cup into a seriated set. Twenty‐one‐month‐olds produced more structures containing three or more cups than did the younger age groups, and these children also achieved seriated sets more frequently. Within all participant groups, success at seriating five cups was associated with the frequency of combining three or more cups, regardless of form. The ability to integrate multiple elements in persistent combinatorial activity is sufficient for the emergence of seriation in young children, monkeys and apes. Reliance on particular methods of combination and a concept of reversibility are later refinements that can enhance skilled seriation.     

Categorization of above and below spatial relations by tufted capuchin monkeys (Cebus apella)

Using a matching-to-sample procedure, the researchers investigated tufted capuchins' (Cebus apella) ability to form categorical representations of above and below spatial relations. In Experiment 1, 5 capuchins correctly matched bar-dot stimuli on the basis of the relative above and below location of their constituent elements. The monkeys showed a positive transfer of performance both when the bar-dot distance in the two comparison stimuli differed from that of the sample and when the actual location of the matching stimulus and the nonmatching stimulus on the apparatus was modified. In Experiment 2, the researchers systematically changed the shapes of the located object (the dot) or the reference object (the horizontal bar). These manipulations did not affect the monkeys' performance. Overall, the data suggest that capuchins can form abstract, conceptual-like representations for above and below spatial relations.     

Does own experience affect perception of others’ actions in capuchin monkeys (Cebus apella)?

Anticipating another’s actions is an important ability in social animals. Recent research suggests that in human adults and infants one’s own action experience facilitates understanding and anticipation of others’ actions. We investigated the link between first-person experience and perception of another’s action in adult tufted capuchin monkeys (Sapajus apella spp., formerly Cebus apella spp.). In Experiment 1, the monkeys observed a familiar human (actor) trying to open a container using either a familiar or an unfamiliar action. They looked for longer when the actor tried to open the container using a familiar action. In Experiment 2, the actor performed two novel actions on a new container. The monkeys looked equally at the two actions. In Experiment 3, the monkeys were trained to open the container using one of the novel actions in Experiment 2. After training, we repeated the same procedure as in Experiment 2. The monkeys looked for longer when the actor manipulated the container using the action they had practiced than when she used the unfamiliar action. These results show that knowledge derived from one’s own experience impacts perception of another’s action in these New World monkeys.     

Aspects of spatial cognition in capuchins (Cebus apella): frames of reference and scale of space

Frames of reference (i.e. sets of loci defining spatial locations) determine animals’ performances in object search tasks. Reference frames are used at different scales. Although much behavioural research has been conducted on search strategies in many animal species, relatively little has been done on nonhuman primates. The two experiments reported here focused on the relative strength and the level of functioning of different reference frames at the small-scale level in four capuchins (Cebus apella). Two identical boxes and a landmark were placed on a round platform that could be rotated. A reward was hidden in subject’s view under one box, and then a sash-screen was lowered to hide the rotation of the platform; the sash-screen was then lifted and the subject allowed to search for the reward. In experiment 1 the rewarded box was always the closer to the landmark, in experiment 2 it could be either the box closer to or the box farther from the landmark. Capuchins were successful after invisible rotations in experiment 1, but they failed after invisible rotations in experiment 2. Two possible explanations are proposed: (1) capuchins relied heavily on the left-right body-axis as a frame, and they could only substitute it with a simple association between the rewarded position and the landmark; or (2) capuchins failed because they chose external cues in the room, therefore on a inappropriate scale. The latter explanation allows two further inferences: (a) the capuchins’ choice was indirectly related to their body-axes; and (b) the capuchins revealed a cognitive asymmetry between small-scale and large-scale spaces, thus differing from humans. Received: 10 October 1999 / Accepted after revision: 4 May 2000     

An assessment of memory awareness in tufted capuchin monkeys (Cebus apella)

Humans, apes, and rhesus monkeys demonstrate memory awareness by collecting information when ignorant and acting immediately when informed. In this study, five capuchin monkeys searched for food after either watching the experimenter bait one of four opaque tubes (seen trials), or not watching (unseen trials). Monkeys with memory awareness should look into the tubes before making a selection only on unseen trials because on seen trials they already know the location of the food. In Experiment 1, one of the five capuchins looked significantly more often on unseen trials. In Experiment 2, we ensured that the monkeys attended to the baiting by interleaving training and test sessions. Three of the five monkeys looked more often on unseen trials. Because monkeys looked more often than not on both trial types, potentially creating a ceiling effect, we increased the effort required to look in Experiment 3, and predicted a larger difference in the probability of looking between seen and unseen trials. None of the five monkeys looked more often on unseen trials. These findings provide equivocal evidence for memory awareness in capuchin monkeys using tests that have yielded clear evidence in humans, apes, and rhesus monkeys.     

Inferences about the location of food in capuchin monkeys (Cebus apella) in two sensory modalities

The authors tested the ability of capuchin monkeys (Cebus apella) to make inferences about hidden food. In Experiment 1, we showed the content of 2 boxes, 1 of which was baited (visual condition, VC) or we shook both boxes producing noise from the baited box (auditory condition, AC). Seven subjects (out of 8) were above chance in the VC, whereas only 1 was above chance in AC. During treatment, by manipulating empty and filled objects subjects experienced the relation between noise and content. When tested again, 7 capuchins were above chance in the VC and 3 in AC. In Experiment 2, we gave visual or auditory information only about the empty box and, consequently, successful choice implied inferential reasoning. All subjects (out of 4) were above chance in the VC, and 2 in the AC. Control tests ruled out the possibility that success resulted from simply avoiding the shaken noiseless box, or from the use of arbitrary auditory information. Similar to apes (Call, 2004), capuchins were capable of inferential reasoning.     

Capuchins’ (Cebus apella) sensitivity to others’ goal-directed actions in a helping context

As humans, our ability to help others effectively is at least in part dependent upon our capacity to infer others’ goals in a variety of different contexts. Several species of nonhuman primate have demonstrated that they will also help others in some relatively simple situations, but it is not always clear whether this helping is based on an understanding of another agent’s goals. Although the results of a number of different studies support the hypothesis that chimpanzees represent others’ goals in various helping contexts and are sensitive to these goals when actually helping others, less work has addressed whether more distantly related species actively represent goals when helping. To explore the cognitive mechanisms underlying helping behaviors in species less closely related to humans, we tested whether a species of New World monkey—the brown capuchin (Cebus apella)—would provide an experimenter with a desired out-of-reach object more often than an alternative object when the experimenter attempted to obtain the former object only. We found that capuchins reliably helped by providing the experimenter’s goal object (Experiment 1) and that explanations based on the use of several less sophisticated strategies did not account for the overall pattern of data (Experiments 2–4). Results are thus consistent with the hypothesis that capuchins help others based on an understanding of their goals although more work is needed to address the possibility that capuchins may be responding to gestural and postural factors alone.     

Ordinal representation of numeric quantities by brown capuchin monkeys (Cebus apella)

Using techniques established by E. M. Brannon and H. S. Terrace (2000) with rhesus macaques (Macaca mulatta), the authors tested the ability of brown capuchins (Cebus apella) to order arrays of items ranging in quantity from 1 to 9. Three monkeys were trained on a touch screen to select the quantities 1-4 in ascending order. The monkeys exhibited successful transfer of this ability to novel representations of the quantities 1-4 and to pairs of the novel quantities 5-9. Patterns of responding with respect to numeric distance and magnitude were similar to those seen in human subjects, suggesting the use of similar psychological processes. The capuchins demonstrated an ordinal representation of quantity equivalent to that shown in Old World monkeys.     

Stock optimizing in choice when a token deposit is the operant.

Each of 2 monkeys typically earned their daily food ration by depositing tokens in one of two slots. Tokens deposited in one slot dropped into a bin where they were kept (token kept). Deposits to a second slot dropped into a bin where they could be obtained again (token returned). In Experiment 1, a fixed-ratio (FR) 5 schedule that provided two food pellets was associated with each slot. Both monkeys preferred the token-returned slot. In Experiment 2, both subjects chose between unequal FR schedules with the token-returned slot always associated with the leaner schedule. When the FRs were 2 versus 3 and 2 versus 6, preferences were maintained for the token-returned slot; however, when the ratios were 2 versus 12, preference shifted to the token-kept slot. In Experiment 3, both monkeys chose between equal-valued concurrent variable-interval variable-interval schedules. Both monkeys preferred the slot that returned tokens. In Experiment 4, both monkeys chose between FRs that typically differed in size by a factor of 10. Both monkeys preferred the FR schedule that provided more food per trial. These data show that monkeys will choose so as to increase the number of reinforcers earned (stock optimizing) even when this preference reduces the rate of reinforcement (all reinforcers divided by session time).