Transport of Functionally Appropriate Tools by Capuchin Monkeys (Cebus apella)

Capuchin monkeys are notable among New World monkeys for their widespread use of tools. They use both hammer tools and insertion tools in the wild to acquire food that would be unobtainable otherwise. Evidence indicates that capuchins transport stones to anvil sites and use the most functionally efficient stones to crack nuts. We investigated capuchins’ assessment of functionality by testing their ability to select a tool that was appropriate for two different tool-use tasks: A stone for a hammer task and a stick for an insertion task. To select the appropriate tools, the monkeys investigated a baited tool-use apparatus (insertion or hammer), traveled to a location in their enclosure where they could no longer see the apparatus, made a selection between two tools (stick or stone), and then could transport the tool back to the apparatus to obtain a walnut. Four capuchins were first trained to select and use the appropriate tool for each apparatus. After training, they were then tested by allowing them to view a baited apparatus and then travel to a location 8 m distant where they could select a tool while out of view of the apparatus. All four monkeys chose the correct tool significantly more than expected and transported the tools back to the apparatus. Results confirm capuchins’ propensity for transporting tools, demonstrate their capacity to select the functionally appropriate tool for two different tool-use tasks, and indicate that they can retain the memory of the correct choice during a travel time of several seconds.

Audience Effects in COgnitive Task Performance in Capuchin Monkeys (Cebus apella)

Primates as a taxonomic Order have the largest brains corrected for body size in the animal kingdom. These large brains have allowed primates to evolve the capacity to demonstrate advanced cognitive processes across a wide array of abilities. Nonhuman primates are particularly adept at social learning, defined as the modification of behavior by observing the actions of others. Additionally, primates often exploit resources differently depending on their social context. In this study, capuchin monkeys (Cebus apella) were tested on a cognitive task in three social contexts to determine if social context influenced their performance on the task. The three social contexts included: alone, having a dominant individual in an adjacent compartment, and having a subordinate individual in the adjacent compartment. The benefits to this design were thatthe social context was the only variable influencing performance, whereas in previous studies investigating audience effects other animals could physically and directly influence a subject's performance in an open testing situation. Based on past studies, Ipredicted that the presence of a dominant individual would reduce cognitive task performance compared to the other conditions. The cognitive test used was a match-tosample discrimination task in which animals matched combinations of eight geometric shapes. Animals were trained on this task in an isolated context until they reached a baseline level of proficiency and were then tested in the three social contexts in a random order multiple times. Two subjects (Mt and Dv) have successfully completed trials under all conditions. Results indicated that there were no significant difference in taskperformance across the three conditions (Dv x^2 (1) = 0.42, p=0.58; Mt x^2 (1) = 0.02, p=0.88). In all conditions, subjects performed significantly above chance (i.e., 39/60 trials determined by a binomial distribution). Results are contrary to previous studies thatreport low status monkeys 'play dumb' when testing in a mixed social context, possibly because other studies did not account for aggressive interference by dominants while testing. Results of this study suggest that the mere presence of a dominant individualdoes not necessarily affect performance on a cognitive task, but rather the imminence of physical aggression is the most important factor influencing testing in a social context.

IMPULSE CONTROL AND COOPERATION IN CAPUCHIN MONKEYS (Cebus apella)

The benefits animals derive from living in social groups have produced the evolution of many forms of cooperative behavior. To cooperate, two or more individuals coordinate their actions to accomplish a common goal. One cognitive process that has the potential to influence cooperation is self control. Individuals delaying their impulsive choice for an immediate reward may potentially receive a larger reward later by cooperating with others. In this study, I measured whether brown capuchin monkeys (Cebus apella) were capable of impulse control and whether impulse control was related to cooperation. Impulse control and cooperation were measured using a lazy susan-like apparatus, on which animals could turn a wheel to receive food rewards. The capuchins went through two training phases that taught them how to turn the wheel efficiently to obtain rewards and how to turn the wheel to obtain the larger of two rewards. After training, I tested impulse control by giving the capuchins a choice between a smaller and a larger reward placed at shorter or more distant locations on the wheel. The capuchins demonstrated impulse control in that they tended to inhibit the impulse to select the smaller reward when it was closer and easier to reach and instead selected the larger reward when it was farther away. Cooperation was tested in all possible dyads of seven individuals, a total of 21 dyads, by allowing each dyad 10 trials to work together with effort on the lazy-susan so that each would obtain a reward. Seventeen out of 21 dyads cooperated by simultaneously moving the wheel in the same direction. The correlation between how often a particular dyad cooperated and their average impulse control score was not statistically significant, r(21) = -.125, p = .591. Capuchins demonstrated impulse control and cooperation using this novel apparatus but the two abilities were not related. Other factors such as the unique social relationship between two individuals may play a more prominent role in the motivation to cooperate rather than the cognitive capacity to inhibit behavior.

Use Of Conspecific Gestural Cues To Solve An Object-Choice Task In Tufted Capuchin Monkeys (Cebus Apella)

Capuchin monkeys, Cebus sp., utilize a wide array of gestural displays in the wild, including facial displays such as lip-smacking and bare-teeth displays. In captivity, they have been shown to respond to the head orientation of humans, show sensitivity to human attentional states, as well as follow human gazes behind barriers. In this study, I investigated whether tufted capuchin monkeys (Cebus apella) would attend to and utilize the gestural cues of a conspecific to obtain a hidden reward. Two capuchins faced each other in separate compartments of an apparatus with an open field in between. The open field contained two cups with holes on one side such that only one monkey, a so-called cuing monkey, could see the reward inside one of the cups. I then moved the cups toward the other signal-receiving monkey and assessed whether it would utilize untrained cues provided by the cuing monkey to select the cup containing the reward. Two of four female capuchin monkeys learned to select the cup containing the reward significantly more often than chance. Neither of these two monkeys performed over chance spontaneously, however, and the other two monkeys never performed above chance despite many blocks of trials. Successful choices by two monkeys to obtain hidden rewards provided experimental evidence that capuchin monkeys attend to and utilize the gestural cues of conspecifics.

The Expression Of Motor Planning In Squirrel Monkeys (Saimiri sciureus) And Brown Capuchins (Cebus apella)

Multiple recent studies provide evidence that both human and nonhuman primates possess motor planning abilities. I tested for the demonstration of motor planning in two previously untested primate species through two experiments. In the first experiment, I compared the extent to which squirrel monkeys (Saimiri sciureus) and brown capuchins (Cebus apella) plan their movements in a grasping task. Individuals were presented with an inverted cup that required being turned and held upright in order to extract a food reward from the inside of the cup. This task was most efficiently solved by using an initially awkward inverted grasp that affords a comfortable hand and arm orientation at the end of the movement (known as end-state comfort). While certain individuals from both species exhibited end-state comfort, many of the capuchins never demonstrated this type of motor planning. Furthermore, the squirrel monkeys used the efficient grasp significantly more than the capuchins. In the second experiment, I presented the capuchins with another grasping task to test if they would express motor planning abilities in a different context. Here, the capuchins were offered a dowel that was baited on either the left or right end. A radial grasp with the thumb pointing towards the baited end was considered to be the most efficient grasp because it afforded a comfortable final position. The capuchins switched hands and used an overhand radial grasp on the dowel significantly more often than not, thus demonstrating motor planning in this task. The grasps typically utilized by these two closely related species differ considerably in that capuchins are capable of exercising precision grips, whereas squirrel monkeys are limited to whole-handed power grips. Moreover, unlike capuchins, squirrel monkeys are not particularly dexterous nor are they capable of precise manipulative actions. It is therefore more beneficial for squirrel monkeys to plan their movements efficiently because they are less capable of compensating for inappropriate initial grasps. Due to the appreciable variability in the expression of motor planning skills across species, I proposed that morphological constraints might explain the observed discrepancies in movement planning among different primate species.

Brown Capuchins (Cebus apella) Exhibit Self-Control on a Delay of Gratification Food Exchange Task When Food Options Differ Qualitatively

Self-control allows an individual to obtain a more preferred outcome by forgoing an immediate interest. Self-control is an advanced cognitive process because it involves the ability to weigh the costs and benefits of impulsive versus restrained behavior, determine the consequences of such behavior, and make decisions based on the most advantageous course of action. Self-control has been thoroughly explored in Old World primates, but less so in New World monkeys. There are many ways to test self-control abilities in non-human primates, including exchange tasks in which an animal must forgo an immediate, less preferred reward to receive a delayed, more preferred reward. I examined the self-control abilities of six capuchin monkeys using a task in which a monkey was given a less preferred food and was required to wait a delay interval to trade the fully intact less preferred food for a qualitatively higher, more preferred food. Partially eaten pieces of the less preferred food were not rewarded, and delay intervals increased on an individual basis based on performance. All six monkeys were successful in inhibiting impulsivity and trading a less preferred food for a more preferred food at the end of a delay interval. The maximum duration each subject postponed gratification instead of responding impulsively was considered their delay tolerance. This study was the first to show that monkeys could inhibit impulsivity in a delay of gratification food exchange task in which the immediate and delayed food options differed qualitatively and a partially eaten less preferred food was not rewarded with the more preferred food at the end of a delay interval. These results show that New World monkeys possess advanced cognitive abilities similar to those of Old World primates.

Capuchin Monkeys (Cebus apella) Fail to Be Equitable in an Ultimatum Game

The ultimatum game is a commonly used economics game testing humans' sense of fairness. In the game, a "proposer" is given a sum of money and is told they can split it however they want with another human partner. The partner can then either accept the division and both proposer and responder receive the proposed amounts, or the responder can reject the offer and neither player will get anything. Human subjects from most western cultures typically share almost half of an allotted amount, but it remains unknown whether our close primate relatives share this generosity. Recent attempts to present chimpanzees with the ultimatum game have provided inconclusive results, with some studies finding the animals share humans' disposition to behave 'fairly' and others concluding that chimpanzees act selfishly to maximize their own rewards. Capuchin monkeys are known to share many human and chimpanzee social and cooperative behaviors, and this study was the first to present capuchin monkeys with a version of the ultimatum game. Subjects were presented with two differently colored tokens representing different qualitative reward contingencies, one equitable and the other inequitable in favor of the subject proposer. Subjects could select and place one of the tokens in a transfer container. The capuchins were first tested with a "dictator game" where, after the subject monkey selected a token, the rewards (equitable or inequitable) were distributed to the subject and a nearby partner monkey that was not an active participant. The capuchins were then tested on an ultimatum game in which after the subject selected and placed a token in the container, the container was moved to the partner. The partner needed to remove the token and transfer it back to the experimenter for the rewards to be distributed. As such, the partner could reject the subject's offer by refusing to participate and neither would receive a reward. The experiment was conducted to determine if the subject monkey would select the equitable reward option rather than the selfish option in order to maintain the partner's cooperation in the task. Capuchin subjects behaved selfishly and selected the inequitable token significantly more often than the equitable token in both the dictator and ultimatum game with no significant difference in preference between the two games. Interestingly, despite the occasional occurrence of rejection by the partner monkeys (resulting in no reward for the subject), subjects never altered their strategy, continuing to prefer the selfish token. The study may indicate that capuchin monkeys have an inability to judge the effect of their behavior on a conspecific's reward outcome, or an indifference to the outcome if there is an individual cost associated with behaving prosocially.

Capuchin Monkeys Exercise Self-control by Choosing Token Exchange Over an Immediate Reward

Self-control is a prerequisite for complex cognitive processes such as cooperation and planning. As such, comparative studies of self-control may help elucidate the evolutionary origin of these capacities. A variety of methods have been developed to test for self-control in non-human primates that include some variation of foregoing an immediate reward in order to gain a more favorable reward. We used a token exchange paradigm to test for self-control in capuchin monkeys (Cebus apella). Animals were trained that particular tokens could be exchanged for food items worth different values. To test for self-control, a monkey was provided with a token that was associated with a lower-value food. When the monkey exchanged the token, the experimenter provided the monkey with a choice between the lower-value food item associated with the token or another token that was associated with a higher-value food. If the monkey chose the token, they could then exchange it for the higher-value food. Of seven monkeys trained to exchange tokens, five demonstrated that they attributed value to the tokens by differentially selecting tokens for higher-value foods over tokens for lower-value foods. When provided with a choice between a food item or a token for a higher-value food, two monkeys selected the token significantly more than expected by chance. The ability of capuchin monkeys to forego an immediate food reward and select a token that could then be traded for a more preferred food demonstrated some degree of self-control. Thus, results suggest a token exchange paradigm could be a successful technique for assessing self-control in this New World species.

The Use of Human and Conspecific Gestures By Capuchin Monkeys to Solve an Object-Choice Task

Most primates live in highly complex social systems, and therefore have evolved similarly complex methods of communicating with each other. One type of communication is the use of manual gestures, which are only found in primates. No substantial evidence exists indicating that monkeys use communicative gestures in the wild. However, monkeys may demonstrate the ability to learn and/or use gestures in certain experimental paradigms since they¿ve been shown to use other visual cues such as gaze. The purpose of this study was to investigate if ten brown capuchin monkeys (Cebus apella) were able to use gestural cues from monkeys and a pointing cue from a human to obtain a hidden reward. They were then tested to determine if they could transfer this skill from monkeys to humans and from humans to monkeys. One group of monkeys was trained and tested using a conspecific as the cue giver, and was then tested with a human cue-giver. The second group of monkeys began training and testing with a human cue giver, and was then tested with a monkey cue giver. I found that two monkeys were able to use gestural cues from conspecifics (e.g., reaching) to obtain a hidden reward and then transfer this ability to a pointing cue from a human. Four monkeys learned to use the human pointing cue first, and then transferred this ability to use the gestural cues from conspecifics to obtain a hidden reward. However, the number of trials it took for each monkey to transfer the ability varied considerably. Some subjects spontaneously transferred in the minimum number of trials needed to reach my criteria for successfully obtaining hidden rewards (N = 40 trials), while others needed a large number of trials to do so (e.g. N = 190 trials). Two subjects did not perform successfully in any of the conditions in which they were tested. One subject successfully used the human pointing cue and a human pointing plus vocalization cue, but did not learn the conspecific cue. One subject learned to use the conspecific cue but not the human pointing cue. This was the first study to test if brown capuchin monkeys could use gestural cues from conspecifics to solve an object choice task. The study was also the first to test if capuchins could transfer this skill from monkeys to humans and from humans to monkeys. Results showed that capuchin monkeys were able to flexibly use communicative gestures when they were both unintentionally given by a conspecific and intentionally given by a human to indicate a source of food.

Investigation of Rudimentary Meta-Cognition in Lion-Tailed Macaques and Tufted Capuchins

Meta-cognition, or "thinking about thinking," has been studied extensively in humans, but very little is known about the process in animals. Although great apes and rhesus macaques (Macaca mulatta) have demonstrated multiple apparently meta-cognitive abilities, other species have either been largely ignored or failed to convincingly display meta-cognitive traits. Recent work by Marsh, however, raised the possibility that some species may possess rudimentary or partial forms of meta-cognition. This thesis sought to further investigate this possibility by running multiple comparative experiments. The goal of the first study was to examine whether lion-tailed macaques, a species that may have a rudimentary form of meta-cognition, are able to use an uncertainty response adaptively, and if so, whether they could use the response flexibly when the stimuli for which the subjects should be uncertain changed. The macaques' acquisition of the initial discrimination task is ongoing, and as such there were not yet data to support a conclusion either way. In the second study, tufted capuchins were required to locate a food reward hidden beneath inverted cups that sat on a Plexiglas tray. In some conditions the capuchins were shown where the food was hidden, in others they could infer its location, and in yet others they were not given information about the location of the food. On all trials, however, capuchins could optionally seek additional information by looking up through the Plexiglas into the cups. In general, capuchins did this less often when they were shown the food reward, but not when they could infer the reward's location. These data suggest capuchins only meta-cognitively control their information seeking in some conditions, and thus, add support to the potential for a rudimentary form of meta-cognition. In convergence with other studies, these results may represent early models for rudimentary meta-cognition, although viable alternative explanations still remain.

The interface between morphology and action planning: a comparison of two species of New World monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities.

The Interface Between Morphology and Action Planning: a Comparison of Two Species of New World Monkeys

Recent research with several species of nonhuman primates suggests sophisticated motor-planning abilities observed in human adults may be ubiquitous among primates. However, there is considerable variability in the extent to which these abilities are expressed across primate species. In the present experiment, we explore whether the variability in the expression of anticipatory motor-planning abilities may be attributed to cognitive differences (such as tool use abilities) or whether they may be due to the consequences of morphological differences (such as being able to deploy a precision grasp). We compared two species of New World monkeys that differ in their tool use abilities and manual dexterity: squirrel monkeys, Saimiri sciureus (less dexterous with little evidence for tool use) and tufted capuchins, Sapajus apella (more dexterous and known tool users). The monkeys were presented with baited cups in an untrained food extraction task. Consistent with the morphological constraint hypothesis, squirrel monkeys frequently showed second-order motor planning by inverting their grasp when picking up an inverted cup, while capuchins frequently deployed canonical upright grasping postures. Findings suggest that the lack of ability for precision grasping may elicit more consistent second-order motor planning, as the squirrel monkeys (and other species that have shown a high rate of second-order planning) have fewer means of compensating for inefficient initial postures. Thus, the interface between morphology and motor planning likely represents an important factor for understanding both the ontogenetic and phylogenetic origins of sophisticated motor-planning abilities. (C) 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.