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.     

Discrimination of functionally appropriate and inappropriate throwing tools by captive tufted capuchins (<Emphasis Type="Italic">Cebus apella</Emphasis>)

A tool-throwing task was used to test whether capuchin monkeys understand the difference between functionally appropriate and functionally inappropriate tools. A group of monkeys was trained to obtain a sticky treat from a container outside their enclosure using a projectile attached to one end of an anchored line. Subsequently, these monkeys were given choice tests between functional and nonfunctional versions of tools used in training. A different feature of the tool was varied between alternatives in each choice test. The monkeys chose to use functional tools significantly more often than nonfunctional tools in early exposures to each choice test. A second experiment tested whether these subjects, as well as a second group of minimally trained participants, could distinguish between functional and nonfunctional tools that appeared different from those used in training. A new set of design features was varied between tools in these choice tests. All participants continued to choose functional tools significantly more often than nonfunctional tools, regardless of their tool-throwing experience or the novel appearance of the tools. These results suggest that capuchin monkeys, like chimpanzees studied in similar experiments, are sensitive to a variety of functionally relevant tool features.     

Tufted capuchins (<Emphasis Type="Italic">Cebus apella</Emphasis>) attribute value to foods and tools during voluntary exchanges with humans

This research examined exchange and value attribution in tufted capuchin monkeys (Cebus apella). We presented subjects with opportunities to obtain various foods and a tool from an experimenter in exchange for the foods or tool in the subjects' possession. The times elapsed before the first chow biscuits were expelled and/or an exchange took place were recorded as the dependent measures. Laboratory chow biscuits, grapes, apples, and a metal bolt (a tool used to probe for syrup) were used as experimental stimuli. The subjects demonstrated the ability to recognize that exchanges could occur when an experimenter was present with a desirable food. Results indicate that subjects exhibited significant variation in their willingness to barter based upon the types of foods that were both in their possession and presented by the experimenter. Subjects more readily traded chow biscuits for fruit, and more readily traded apples for grapes than grapes for apples. During the exchange of tools and food, the subjects preferred the following in descending order when the probing apparatus was baited with sweet syrup: grapes, metal bolts, and chow biscuits. However when the apparatus was not baited, the values changed to the following in descending order: grapes, chow, and metal bolts. These results indicate that tufted capuchins recognize opportunities to exchange and engage in a simple barter system whereby low-valued foods are readily traded for more highly valued food. Furthermore, these capuchins demonstrate that their value for a tool changes depending upon its utility.     

Quantity judgments of sequentially presented food items by capuchin monkeys (Cebus apella)

Recent assessments have shown that capuchin monkeys, like chimpanzees and other Old World primate species, are sensitive to quantitative differences between sets of visible stimuli. In the present study, we examined capuchins’ performance in a more sophisticated quantity judgment task that required the ability to form representations of food quantities while viewing the quantities only one piece at a time. In three experiments, we presented monkeys with the choice between two sets of discrete homogeneous food items and allowed the monkeys to consume the set of their choice. In Experiments 1 and 2, monkeys compared an entirely visible food set to a second set, presented item-by-item into an opaque container. All monkeys exhibited high accuracy in choosing the larger set, even when the entirely visible set was presented last, preventing the use of one-to-one item correspondence to compare quantities. In Experiment 3, monkeys compared two sets that were each presented item-by-item into opaque containers, but at different rates to control for temporal cues. Some monkeys performed well in this experiment, though others exhibited near-chance performance, suggesting that this species’ ability to form representations of food quantities may be limited compared to previously tested species such as chimpanzees. Overall, these findings support the analog magnitude model of quantity representation as an explanation for capuchin monkeys’ quantification of sequentially presented food items.

Concurrent disjoint and reciprocal classification by Cebus apella in seriation tasks: evidence for hierarchical organization

We report the results of a 4-year-long study of capuchin monkeys (Cebus apella ) on concurrent three-way classification and linear size seriation tasks using explicit ordering procedures, requiring subjects to select icons displayed on touch screens rather than manipulate and sort actual objects into groups. The results indicate that C. apella is competent to classify nine items concurrently, first into three disjoint classes where class exemplars are identical to one another, then into three reciprocal classes which share common exemplar (size) features. In the final phase we compare the relative efficiency of executive control under conditions where both hierarchical and/or linear organization can be utilized. Whilst this shows a superiority of categorical based size seriation for a nine item test set suggesting an adaptive advantage for hierarchical over linear organization, Cebus nevertheless achieved high levels of principled linear size seriation with sequence lengths not normally achieved by children below the age of six years.     

Understanding of the relationship between seeing and knowing by tufted capuchin monkeys (Cebus apella)

The ability of four tufted capuchin monkeys (Cebus apella) to recognize the causal connection between seeing and knowing was investigated. The subjects were trained to follow a suggestion about the location of hidden food provided by a trainer who knew where the food was (the knower) in preference to a trainer who did not (the guesser). The experimenter baited one of three opaque containers behind a cardboard screen so that the subjects could not see which of the containers hid the reward. In experiment 1, the knower appeared first in front of the apparatus and looked into each container; next, the guesser appeared but did not look into any containers. Then the knower touched the correct cup while the guesser touched one of the three randomly. The capuchin monkeys gradually learned to reach toward the cup that the knower suggested. In experiment 2, the subjects adapted to a novel variant of the task, in which the guesser touched but did not look into any of the containers. In experiment 3, the monkeys adapted again when the knower and the guesser appeared in a random order. These results suggest that capuchin monkeys can learn to recognize the relationship between seeing and knowing. Accepted after revision: 10 September 2001 Electronic Publication     

How do tufted capuchin monkeys (Cebus apella) understand causality involved in tool use?

Four tufted capuchin monkeys (Cebus apella) were trained to choose from 2 hook-like tools, 1 of which successfully led to collecting food, whereas the other did not because of inappropriate spatial arrangement of the tool and the food. In Experiment 1, all of the monkeys successfully learned the basic task. The monkeys performed successfully with tools of novel colors and shapes in Experiments 2-5. These results demonstrate that the monkeys used the spatial arrangement of the tool and the food as a cue. However, they failed when there were obstacles (Experiment 6) or traps (Experiment 7) on the path along which the monkeys dragged tools. These results may suggest that capuchin monkeys understand the spatial relationship between 2 items, namely, food and the tool, but do not understand the spatial relationship among 3 items, namely, food, tool, and the environmental condition. The possible role of stimulus generalization is also considered.     

Observational learning from tool using models by human-reared and mother-reared capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

Studies of wild capuchins suggest an important role for social learning, but experiments with captive subjects have generally not supported this. Here we report social learning in two quite different populations of capuchin monkeys (Cebus apella). In experiment 1, human-raised monkeys observed a familiar human model open a foraging box using a tool in one of two alternative ways: levering versus poking. In experiment 2, mother-raised monkeys viewed similar techniques demonstrated by monkey models. A control group in each population saw no model. In both experiments, independent coders detected which technique experimental subjects had seen, thus confirming social learning. Further analyses examined fidelity of copying at three levels of resolution. The human-raised monkeys exhibited fidelity at the highest level, the specific tool use technique witnessed. The lever technique was seen only in monkeys exposed to a levering model, by contrast with controls and those witnessing poke. Mother-reared monkeys instead typically ignored the tool and exhibited fidelity at a lower level, tending only to re-create whichever result the model had achieved by either levering or poking. Nevertheless this level of social learning was associated with significantly greater levels of success in monkeys witnessing a model than in controls, an effect absent in the human-reared population. Results in both populations are consistent with a process of canalization of the repertoire in the direction of the approach witnessed, producing a narrower, socially shaped behavioural profile than among controls who saw no model. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Self-control and tool use in tufted capuchin monkeys (Cebus apella)

Self-control is defined as forgoing immediate gratification to obtain a greater reward. Tool use may relate to self-control because both behaviors may require foresight and deliberate control over one's actions. The authors assessed 20 capuchin monkeys (Cebus apella) for the ability to delay gratification in a tool task. Subjects were given rod-shaped food items that could either be consumed immediately or be carried to an apparatus and used to extract a more preferred food. The authors found that some monkeys were able to exhibit self-control. Monkeys with relatively more tool use experience demonstrated the greatest levels of self-control. These results indicate that capuchins are capable of delaying gratification when a higher quality reinforcer is present and that tool experience can influence levels of self-control in this task.     

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.     

Experimental evidence for route integration and strategic planning in wild capuchin monkeys

Both in captivity and the wild, primates are found to travel mostly to the nearest available resource, but they may skip over the closest resource and travel to more distant resources, which are often found to be more productive. This study examines the tradeoff between distance and reward in the foraging choices of one group of wild capuchin monkeys (Cebus apella nigritus) using feeding platforms in large-scale foraging experiments conducted over four years. Three feeding sites were arrayed in an oblique triangle, such that once the monkey group had chosen one site to feed, they had a choice between two remaining sites, a close one with less food and the other up to 2.3 times as far away but with more food. Sites were provisioned once per day. The capuchins generally chose the closer feeding site, even when the more distant site offered up to 12 times as much food. The distances to, rewards of, or various profitability measures applied to each alternative site individually did not explain the group’s choices in ways consistent with foraging theory or principles of operant psychology. The group’s site choices were predicted only by comparing efficiency measures of entire foraging pathways: (1) direct travel to the more rewarding distant site, versus (2) the longer ‘detour’ through the closer site on the way to the more distant one. The group chose the detour more often when the reward was larger and the added detour distance shorter. They appeared to be more sensitive to the absolute increase in detour distance than to the relative increase compared to the straight route. The qualitative and quantitative results agree with a simple rule: do not use the detour unless the energy gain from extra food outweighs the energy cost of extra travel. These results suggest that members of this group integrate information on spatial location, reward, and perhaps potential food competition in their choice of multi-site foraging routes, with important implications for social foraging. This contribution is part of the special issue “ A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007b).     

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.     

Redundant food searches by capuchin monkeys (Cebus apella): a failure of metacognition?

This study investigated capuchin monkeys' understanding of their own visual search behavior as a means to gather information. Five monkeys were presented with three tubes that could be visually searched to determine the location of a bait. The bait's visibility was experimentally manipulated, and the monkeys' spontaneous visual searches before tube selection were analyzed. In Experiment 1, three monkeys selected the baited tube significantly above chance; however, the monkeys also searched transparent tubes. In Experiment 2, a bent tube in which food was never visible was introduced. When the bent tube was baited, the monkeys failed to deduce the bait location and responded randomly. They also continued to look into the bent tube despite not gaining any pertinent information from it. The capuchin monkeys' behavior contrasts with the efficient employment of visual search behavior reported in humans, apes and macaques. This difference is consistent with species-related variations in metacognitive abilities, although other explanations are also possible.     

Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) discriminate between knowing and not knowing and collect information as needed before acting

Humans use memory awareness to determine whether relevant knowledge is available before acting, as when we determine whether we know a phone number before dialing. Such metacognition, or thinking about thinking, can improve selection of appropriate behavior. We investigated whether rhesus monkeys (Macaca mulatta) are capable of a simple form of metacognitive access to the contents of short-term memory. Monkeys chose among four opaque tubes, one of which concealed food. The tube containing the reward varied randomly from trial to trial. On half the trials the monkeys observed the experimenter baiting the tube, whereas on the remaining trials their view of the baiting was blocked. On each trial, monkeys were allowed a single chance to select the tube containing the reward. During the choice period the monkeys had the opportunity to look down the length of each tube, to determine if it contained food. When they knew the location of the reward, most monkeys chose without looking. In contrast, when ignorant, monkeys often made the effort required to look, thereby learning the location of the reward before choosing. Looking improved accuracy on trials on which monkeys had not observed the baiting. The difference in looking behavior between trials on which the monkeys knew, and trials on which they were ignorant, suggests that rhesus monkeys discriminate between knowing and not knowing. This result extends similar observations made of children and apes to a species of Old World monkey, suggesting that the underlying cognitive capacities may be widely distributed among primates.     

Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus)

Helping others at no cost to oneself is a simple way to demonstrate other-regarding preferences. Yet, primates exhibit mixed results for other-regarding preferences: chimpanzees and tamarins do not show these effects, whereas capuchin monkeys and marmosets preferentially give food to others. One factor of relevance to this no-cost food donation is the payoff to the donor. Though donors always receive the same payoffs regardless of their choice, previous work varies in whether they receive either a food reward or no food reward. Here, I tested cotton-top tamarins in a preferential giving task. Subjects could choose from two tools, one of which delivered food to a partner in an adjacent cage and the other of which delivered food to an empty cage. Thus, subjects could preferentially give or withhold food from a partner. I varied whether subjects received food payoffs, whether a partner was present or absent, and whether the partner was a non-cagemate or the subject’s mate. Results showed that the subjects’ overall motivation to pull either tool declined when they did not receive any food. Additionally, they did not preferentially donate or withhold food, regardless of their own payoff or their relationship with the partner. Thus, cotton-top tamarins do not take advantage of cost-free food giving, either when they might gain in the future (mates) or when they have no opportunity for future interactions (non-cagemates).     

Capuchin monkeys (Cebus apella) let lesser rewards pass them by to get better rewards

Self-control is defined as foregoing an immediate reward to gain a larger delayed reward. Methods used to test self-control comparatively include inter-temporal choice tasks, delay of gratification tasks, and accumulation tasks. To date, capuchin monkeys have shown different levels of self-control across tasks. This study introduced a new task that could be used comparatively to measure self-control in an intuitive context that involved responses that required no explicit training. Capuchin monkeys (Cebus apella) were given a choice between two food items that were presented on a mechanized, revolving tray that moved those foods sequentially toward the monkeys. A monkey could grab the first item or wait for the second, but was only allowed one item. Most monkeys in the study waited for a more highly preferred food item or a larger amount of the same food item when those came later, and they inhibited the prepotent response to grab food by not reaching out to take less-preferred foods or smaller amounts of food that passed directly in front of them first. These data confirm that the mechanisms necessary for self-control are present in capuchin monkeys and indicate that the methodology can be useful for broader comparative assessments of self-control.     

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.     

Tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) show understanding of human attentional states when requesting food held by a human

Researchers have investigated to what extent non-human primates understand others’ attentional states, as this ability is considered an important prerequisite for theory of mind. However, previous studies using food requesting tasks have failed to show that non-human primates attribute perception to others as a function of their attentional states. One possible reason is that food requesting tasks may require subjects not only to take into account an experimenter’s attentional state but also to direct it toward the food. The present study tested tufted capuchin monkeys’ (Cebus apella) understanding of others’ attentional states in a food requesting task. In the first situation, monkeys were required only to attract an experimenter’s attention. In the second situation, the monkeys were required to both attract the experimenter’s attention and direct it toward food on a table. The results revealed that capuchin monkeys showed evidence of understanding the experimenter’s attentional variations only in the former condition. This suggests that previous tasks, requiring referential gestures, lacking in most non-human primates, failed to reveal sensitivity to human attentional states because the subjects might not have understood the requesting situation. In conclusion, capuchin monkeys can understand variations in others’ attentional states, although this ability appears limited compared to what is seen in humans.     

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.     

Spider monkey ranging patterns in Mexican subtropical forest: do travel routes reflect planning?

Although it is well known that frugivorous spider monkeys (Ateles geoffroyi yucatanensis) occupy large home ranges, travelling long distances to reach highly productive resources, little is known of how they move between feeding sites. A 11 month study of spider monkey ranging patterns was carried out at the Otochma’ax Yetel Kooh reserve, Yucatán, Mexico. We followed single individuals for as long as possible each day and recorded the routes travelled with the help of a GPS (Global Positioning System) device; the 11 independently moving individuals of a group were targeted as focal subjects. Travel paths were composed of highly linear segments, each typically ending at a place where some resource was exploited. Linearity of segments did not differ between individuals, and most of the highly linear paths that led to food resources were much longer than the estimate visibility in the woodland canopy. Monkeys do not generally continue in the same ranging direction after exploiting a resource: travel paths are likely to deviate at the site of resource exploitation rather than between such sites. However, during the harshest months of the year consecutive route segments were more likely to retain the same direction of overall movement. Together, these findings suggest that while moving between feeding sites, spider monkeys use spatial memory to guide travel, and even plan more than one resource site in advance. This contribution is part of the special issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007).