A Capuchin monkey (<Emphasis Type="Italic">Cebus apella</Emphasis>) recognizes when people do and do not know the location of food

In a previous study, Kuroshima and colleagues demonstrated that capuchin monkeys (Cebus apella) learned to discriminate between a "knower" who inspected a box for food, and a "guesser" who did not. The aim of the present study was to specify whether the subjects learned a simple conditional discrimination or a causal relationship that seeing leads to knowing. In experiment 1, we introduced five types of novel containers to two subjects. Each container was of different shape and color. The subjects gradually learned to reach toward the container the knower suggested. In experiment 2, we diversified the behavior of the knower and the guesser. In experiment 3, in order to eliminate the possibility of discrimination based on differences in the magnitude and the complexity of two trainers, we equated their behaviors. One subject adapted to the novel behaviors of the knower and the guesser, successfully discriminating the two trainers. Thus this monkey clearly learned to use the inspecting action of the knower and the non-inspecting action of the guesser as a discriminative cue to recognize the baited container. This result suggests that one capuchin monkey learned to recognize the relationship between seeing and knowing.     

Do rhesus monkeys (Macaca mulatta) attribute knowledge and ignorance to others?

The ability of 4 rhesus monkeys (Macaca mulatta) to understand the causal connection between seeing and knowing was investigated. The subjects were tested to determine if they could discriminate between information provided by experimenters who randomly alternated between roles of guesser and knower. In a series of tests, the knower either hid food under 1 of 3 cups or watched as someone else hid the food. The guesser waited outside the room or covered her or his head until the food was hidden. The subjects watched this procedure occur but could not see which cup the food was hidden under. The knower pointed to the correct cup while the guesser pointed to an incorrect one. None of the macaques provided any evidence that they realized the different states of knowledge possessed by the guesser and knower. The results are consistent with the hypothesis that rhesus macaques are incapable of making inferences about the mental states of others.     

Inferences about guessing and knowing by chimpanzees (Pan troglodytes)

The visual perspective-taking ability of 4 chimpanzees (Pan troglodytes) was investigated. The subjects chose between information about the location of hidden food provided by 2 experimenters who randomly alternated between two roles (the guesser and the knower). The knower baited 1 of 4 obscured cups so that the subjects could watch the process but could not see which of the cups contained the reward. The guesser waited outside the room until the food was hidden. Finally, the knower pointed to the correct cup while the guesser pointed to an incorrect one. The chimpanzees quickly learned to respond to the knower. They also showed transfer to a novel variation of the task, in which the guesser remained inside the room and covered his head while the knower stood next to him and watched a third experimenter bait the cups. The results are consistent with the hypothesis that chimpanzees are capable of modeling the visual perspectives of others.     

Training squirrel monkeys (Saimiri sciureus) to deceive: acquisition and analysis of behavior toward cooperative and competitive trainers

Three squirrel monkeys (Saimiri sciureus) learned to reach toward a container that covered food if a cooperative trainer rewarded such reaches by giving the food. A competitive trainer kept any food found, but wrong selections by this trainer were also rewarded. The monkeys initially reached toward the baited container indiscriminately, but gradually and with the aid of color-cued containers, all 3 reliably reached "honestly" and "deceptively" in the presence of the cooperative and competitive trainers, respectively. The monkeys did not appear to take the trainers' knowledge about the location of the food into account, and deception did not occur if food was placed under the normally unbaited container. With additional containers present, monkeys misled the competitive trainer into selecting the unbaited container farthest from the baited one. Although not indicative of mental attribution, the monkeys' behavior suggests awareness of the acquired communicative function of the reaching response.     

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.     

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.     

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.     

Insightful problem solving and emulation in brown capuchin monkeys

We investigated problem solving abilities of capuchin monkeys via the “floating object problem,” a task in which the subject must use creative problem solving to retrieve a favored food item from the bottom of a clear tube. Some great apes have solved this problem by adding water to raise the object to a level at which it can be easily grabbed. We presented seven capuchins with the task over eight trials (four “dry” and four “wet”). None of the subjects solved the task, indicating that no capuchin demonstrated insightful problem solving under these experimental conditions. We then investigated whether capuchins would emulate a solution to the task. Seven subjects observed a human model solve the problem by pouring water from a cup into the tube, which brought the object to the top of the tube, allowing the subject to retrieve it. Subjects were then allowed to interact freely with an unfilled tube containing the object in the presence of water and objects that could be used to solve the task. While most subjects were unable to solve the task after viewing a demonstrator solve it, one subject did so, but in a unique way. Our results are consistent with some previous results in great ape species and indicate that capuchins do not spontaneously solve the floating object problem via insight.     

Analogical reasoning in a capuchin monkey (Cebus apella)

Previous evidence has suggested that analogical reasoning (recognizing similarities among object relations when the objects themselves are dissimilar) is limited to humans and apes. This study investigated whether capuchin monkeys (Cebus apella) can use analogical reasoning to solve a 3-dimensional search task. The task involved hiding a food item under 1 of 2 or 3 plastic cups of different sizes and then allowing subjects to search for food hidden under the cup of analogous size in their own set of cups. Four monkeys were exposed to a series of relational matching tasks. If subjects reached criterion on these tasks, they were exposed to relational transfer tasks involving novel stimuli. Three of the monkeys failed to reach criterion on the basic relational matching tasks and therefore were not tested further. One monkey, however, revealed above-chance performance on a series of transfer tasks with 3 novel stimuli. This evidence suggests that contrary to previous arguments, a member of a New World monkey species can solve an analogical problem.     

I acknowledge your help: capuchin monkeys’ sensitivity to others’ labor

Our society is sustained by wide-ranging cooperation. If individuals are sensitive to others’ gains and losses as well as the amount of labor, they can ensure future beneficial cooperative interaction. However, it is still an open question whether nonhuman primates are sensitive to others’ labor. We asked this question in tufted capuchin monkeys in an experimental food-sharing situation by comparing conditions with labor by two participants equalized (Equal labor condition) or unequalized (Unequal labor condition). The operator monkey pulled the drawer of one of the two food containers placed between two monkeys, each containing a food for him/herself and another for the recipient monkey. The recipient 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. In Unequal labor condition, the operator first had to pull the handle of the board to which the containers were glued and then pull the drawer of one of the containers, while the recipient received food with no labor. In Equal labor condition, the recipient had to pull the handle of the board so that the operator could operate a container. Results showed that operators chose the high-value food container for recipients more often than when the recipient was absent only in Equal labor condition. This suggests that capuchin monkeys are sensitive to others’ labor and actively give food to a partner who has helped them to complete a task.     

Cues that chimpanzees do and do not use to find hidden objects

Chimpanzees follow conspecific and human gaze direction reliably in some situations, but very few chimpanzees reliably use gaze direction or other communicative signals to locate hidden food in the object-choice task. Three studies aimed at exploring factors that affect chimpanzee performance in this task are reported. In the first study, vocalizations and other noises facilitated the performance of some chimpanzees (only a minority). In the second study, various behavioral cues were given in which a human experimenter either touched, approached, or actually lifted and looked under the container where the food was hidden. Each of these cues led to enhanced performance for only a very few individuals. In the third study – a replication with some methodological improvements of a previous experiment – chimpanzees were confronted with two experimenters giving conflicting cues about the location of the hidden food, with one of them (the knower) having witnessed the hiding process and the other (the guesser) not. In the crucial test in which a third experimenter did the hiding, no chimpanzee found the food at above chance levels. Overall, in all three studies, by far the best performers were two individuals who had been raised in infancy by humans. It thus seems that while chimpanzees are very good at “behavior reading” of various sorts, including gaze following, they do not understand the communicative intentions (informative intentions) behind the looking and gesturing of others – with the possible exception of enculturated chimpanzees, who still do not understand the differential significance of looking and gesturing done by people who have different knowledge about states of affairs in the world. Received: 8 November 1999 / Accepted after revision: 24 January 2000     

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.     

I know you are not looking at me: capuchin monkeys’ (<Emphasis Type="Italic">Cebus apella</Emphasis>) sensitivity to human attentional states

The present study asked whether capuchin monkeys recognize human attentional states. The monkeys requested food from the experimenter by extending an arm (pointing) toward the baited one of two transparent cups. On regular trials the experimenter gave the food immediately to the monkeys upon pointing but on randomly inserted test trials she ignored the pointing for 5 s during which she displayed different attentional states. The monkeys looked at the experimenter's face longer when she looked at the monkeys than when she looked at the ceiling in Experiment 1, and longer when she oriented her head midway between the two cups with eyes open than when she did so with eyes closed in Experiment 2. However, the monkeys showed no differential pointing in these conditions. These results suggest that capuchins are sensitive to eye direction but this sensitivity does not lead to differential pointing trained in laboratory experiments. Furthermore, to our knowledge, this is the first firm behavioral evidence that non-human primates attend to the subtle states of eyes in a food requesting task.     

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.     

Capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) use conspecifics’ emotional expressions to evaluate emotional valence of objects

Emotional expressions provide important clues to other individuals’ emotional states, as well as the environmental situations leading to such states. Although monkeys often modify their behavior in response to others’ expressions, it is unclear whether this reflects understanding of emotional meanings of expressions, or simpler, non-cognitive processes. The present study investigated whether a New World monkey species, tufted capuchin monkeys, recognize objects as elicitors of others’ expressions. Observer monkeys witnessed another individual (demonstrator) reacting either positively or negatively to the contents of one of two containers and were then allowed to choose one of the containers. The observer preferred the container that evoked positive expressions in the demonstrator and avoided the container that evoked negative expressions. Thus, the monkeys appropriately associated the emotional valence of others’ expressions with the container. This finding supports the view that the ability to represent others’ emotions is not limited to humans and apes.     

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.

Ontogenetic dissociation between habit learning and recognition memory in capuchin monkeys (Cebus apella)

The performance of young and adult capuchin monkeys (Cebus apella) on a Concurrent Discrimination Learning (CDL) test and a Delayed Non-Matching to Sample (DNMS) task were investigated. Results indicate that all subjects were able to learn the CDL test with 20-pairs simultaneously and retain this stimulus/reward association within 24-h interval. In contrast, young subjects did not perform the DNMS task with the same proficiency as adults. While adults' scores were above chance across all memory test delays, the young capuchin monkeys performed the test by chance level. These results support the hypothesis that these two tasks require different cognitive processes mediated by two independent neural systems with a differentiated ontogenetic development. Moreover, they provide evidence that this dissociation occurs not only in humans and Old World monkeys but also in the New World capuchin monkeys indicating that this species can be a valuable alternative model for investigations of the neurobiological basis of memory.     

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.     

Do tufted capuchin monkeys (Cebus apella) spontaneously deceive opponents? A preliminary analysis of an experimental food-competition contest between monkeys

A new laboratory procedure which allows the study of deceptive behavior in nonhuman primates is described. Pairs of tufted capuchin monkeys faced each other in a food-competition contest. Two feeder boxes were placed between the monkeys. A piece of food was placed in one of the boxes. The subordinate individual was able to see the food and to open the box to obtain the bait. A dominant male was unable to see the food or to open the box but was able to take the food once the box was opened by the subordinate. In experiment 1, two of four subordinate monkeys spontaneously started to open the unbaited box first with increasing frequency. Experiment 2 confirmed that this "deceptive" act was not due to a drop in the rate of reinforcement caused by the usurping dominant male, under the situation in which food sometimes automatically dropped from the opened box. In experiment 3, two subordinate monkeys were rerun in the same situation as experiment 1. One of them showed some recovery of the "deceptive" act but the other did not; instead the latter tended to position himself on the side where there was no food before he started to open the box. Although the results do not clearly indicate spontaneous deception, we suggest that operationally defined spontaneous deceptive behaviors in monkeys can be analyzed with experimental procedures such as those used here. Accepted after revision: 13 June 2001 Electronic Publication     

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.