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.     

Chimpanzees (Pan troglodytes) can wait,when they choose to: a study with the hybrid delay task

Self-control has been studied in nonhuman animals using a variety of tasks. The inter-temporal choice (ITC) task presents choices between smaller–sooner (SS) and larger–later (LL) options. Using food amounts as rewards, this presents two problems: (a) choices of the LL option could either reflect self-control or instead result from animals’ difficulty with pointing to smaller amounts of food; (b) there is no way to verify whether the subjects would not revert their choice for the LL option, if given the opportunity to do so during the ensuing delay. To address these problems, we have recently introduced a new protocol, the hybrid delay task, which combines an initial ITC with a subsequent accumulation phase in which selection of the SS option leads to its immediate delivery, but choice of the LL option then leads to one-by-one presentation of those items that continues only as long as the subject does not eat any of the accumulated items. The choice of the LL option therefore only reflects self-control when the number of items obtained from LL choices during the accumulation phase is higher than what could be received in the SS option. Previous research with capuchin monkeys demonstrated that their apparent self-control responses in the ITC task may have overestimated their general self-control abilities, given their poor performance in the hybrid delay task. Here, chimpanzees instead demonstrated that their choices for the LL option in the ITC phase of the hybrid delay task were confirmed by their ability to sustain long delays during accumulation of LL rewards.     

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.     

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.     

Delay of gratification and delay maintenance by rhesus macaques (Macaca mulatta)

The authors tested the self-control of rhesus macaques by assessing if they could refrain from reaching into a food container to maximize the accumulation of sequentially delivered food items (a delay-maintenance task). Three different versions of the task varied the quantity and quality of available food items. In the first 2 versions, food items accumulated across the length of the trial until a monkey consumed the items. In the 3rd task, a single less-preferred food item preceded a single more-preferred food item. Some monkeys delayed gratification even with relatively long delays between deliveries of items. However, the data suggested that self-control, in the majority of tested individuals, was not significantly different across different task versions and that self-control by macaques was not as prevalent in these tasks as it is in chimpanzees and human children.     

Time preferences in long-tailed macaques (Macaca fascicularis) and humans (Homo sapiens)

Rosati et al. (Curr Biol 17(19):1663–1668, 2007) found in a self-control test in which choice was between a smaller, immediately delivered food and a larger, delayed food, that chimpanzees preferred the larger reward (self-control); humans, however, preferred the smaller reward (impulsivity). They attributed their results to a species difference in self-control. In Experiment 1, monkeys (long-tailed macaques) were exposed to a self-control task in two conditions: where the food was hidden under differently colored bowls and where it was visible. When these two conditions were compared, choice shifted from greater preference for the impulsive alternative in the hidden condition to greater preference for the self-control alternative in the visible condition. Additionally, in both conditions, preference shifted from self-control to impulsivity over sessions. These results were explained in terms of the reversed-contingency effect (a propensity to reach for more over less when rewards are visible) and not to a capacity for self-control. In Experiment 2, humans that demonstrated preference for more over less in choice preferred the impulsive alternative when choice to either alternative was followed by the same intertrial interval—a preference that accelerates trial rates relative to preference of the self-control alternative. When trial rates were equated so that neither choice accelerated session’s end, humans demonstrated self-control. These results suggest that Rosati et al.’s demonstration of impulsivity in humans was due to participants’ desire to minimize session time.     

Waiting by mistake: Symbolic representation of rewards modulates intertemporal choice in capuchin monkeys,preschool children and adult humans

In the Delay choice task subjects choose between a smaller immediate option and a larger delayed option. This paradigm, also known as intertemporal choice task, is frequently used to assess delay tolerance, interpreting a preference for the larger delayed option as willingness to wait. However, in the Delay choice task subjects face a dilemma between two preferred responses: “go for more” (i.e., selecting the larger, but delayed, option) vs. “go for sooner” (i.e., selecting the immediate, but smaller, option). When the options consist of visible food amounts, at least some of the choices of the larger delayed option might be due to a failure to inhibit a prepotent response towards the larger option rather than to a sustained delay tolerance. To disentangle this issue, we tested 10 capuchin monkeys, 101 preschool children, and 88 adult humans in a Delay choice task with food, low-symbolic tokens (objects that can be exchanged with food and have a one-to-one correspondence with food items), and high-symbolic tokens (objects that can be exchanged with food and have a one-to-many correspondence with food items). This allows evaluating how different methods of representing rewards modulate the relative contribution of the “go for more” and “go for sooner” responses. Consistently with the idea that choices for the delayed option are sometimes due to a failure at inhibiting the prepotent response for the larger quantity, we expected high-symbolic tokens to decrease the salience of the larger option, thus reducing “go for more” responses. In fact, previous findings have shown that inhibiting prepotent responses for quantity is easier when the problem is framed in a symbolic context. Overall, opting for the larger delayed option in the visible-food version of the Delay choice task seems to partially result from an impulsive preference for quantity, rather than from a sustained delay tolerance. In capuchins and children high-symbolic stimuli decreased the individual’s preference for the larger reward by distancing from its appetitive features. Conversely, the sophisticated symbolic skills of adult humans prevented the distancing effect of high-symbolic stimuli in this population, although this result may be due to methodological differences between adult humans and the other two populations under study. Our data extend the knowledge concerning the influence of symbols on both human and non-human primate behavior and add a new element to the interpretation of the Delay choice task. Since high-symbolic stimuli decrease the individual’s preference for the larger reward by eliminating those choices due to prepotent responses towards the larger quantity, they allow to better discriminate responses based on genuine delay aversion. Thus, these findings invite greater caution in interpreting the results obtained with the visible-food version of the Delay choice task, which may overestimate delay tolerance.     

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.     

Copying without rewards: socially influenced foraging decisions among brown capuchin monkeys

An individual’s foraging activity can be influenced by the choices made by nearby conspecifics. The interest shown in the location and characteristics of a feeding patch may depend on the feeding success of a conspecific there, a process that needs to be distinguished from choices guided by rewards to the observer itself. We investigated how rewards for both self and others influence the foraging choices of captive capuchin monkeys (Cebus apella). Thirteen adult capuchins observed familiar female conspecific models explore one of three opaque boxes under three conditions. In the first, there were no rewards available to either monkey; in the second, rewards were available to the model only; and in the third, both monkeys could retrieve a reward. Under all conditions, subjects more often explored the same box as the model than was expected by chance. Thus, without ever receiving a reward themselves or without seeing another receive rewards, subjects’ searches were directed at the box explored by another monkey. The tendency to match the model’s choice increased if the subject was rewarded. We compared these results to control conditions in which the model was either absent, or present but not allowed to demonstrate. Subjects’ located the reward less often in control conditions, than in the experimental conditions. We conclude that extrinsic rewards, while helpful, are not required for partners to influence the foraging choices of capuchins, and that the unrewarded copying of foraging choices demonstrated here may provide the basis for additional social influences on learning. This contribution is part of the Special Issue “A Socioecological Perspective on Primate Cognition” (Cunningham and Janson 2007)     

Preference reversals with food and water reinforcers in rats

Rats were given a choice between a smaller, immediately available reward and a larger reward available after a delay. In one phase, the reward was food and in another phase, the reward was water. Constant delays were added between the choice presentation and the delivery of the reward alternatives. As the time between choice and reward delivery increased from 0 to 25 s, all rats (except one in the water phase) reversed their preference from the smaller, sooner alternative to the larger, later alternative. These findings extend the generality of the preference-reversal animal model to qualitatively different reinforcers. Furthermore, the presence of both impulsive and self-control choices within the same animal is consistent with the view that self-control may be understood as choice behavior, and that species differences in self-control may be differences in degree, not kind.     

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.     

Making choices in anticipation of similar future choices can increase self-control

Two experiments tested the efficacy of linking a current choice with similar future choices as a means of increasing self-control. Participants were offered choices between smaller and sooner vs. larger and later amounts of money (Experiment 1, n = 60) or food (Experiment 2, n = 34). After a small-large pair for which the participant preferred the smaller reward was found, a choice between the same pair was offered as the 1st of 5 such choices to be offered over a period of weeks. The majority of participants in both experiments who chose between all 5 smaller and all 5 larger rewards chose the larger rewards. One third of participants in Experiment 1 who could choose independently on each pair in the series reversed their previous preference and chose the larger reward in the context of the series. These results suggest that self-control can be enhanced by viewing one's current choice as predictive of future choices.     

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.     

Chimpanzees (Pan troglodytes) transfer tokens repeatedly with a partner to accumulate rewards in a self-control task

There has been extensive research investigating self-control in humans and nonhuman animals, yet we know surprisingly little about how one’s social environment influences self-control. The present study examined the self-control of chimpanzees in a task that required active engagement with conspecifics. The task consisted of transferring a token back and forth with a partner animal in order to accumulate food rewards, one item per token transfer. Self-control was required because at any point in the trial, either chimpanzee could obtain their accumulated rewards, but doing so discontinued the food accumulation and ended the trial for both individuals. Chimpanzees readily engaged the task and accumulated the majority of available rewards before ending each trial, and they did so across a number of conditions that varied the identity of the partner, the presence/absence of the experimenter, and the means by which they could obtain rewards. A second experiment examined chimpanzees’ self-control when given the choice between immediately available food items and a potentially larger amount of rewards that could be obtained by engaging the token transfer task with a partner. Chimpanzees were flexible in their decision-making in this test, typically choosing the option representing the largest amount of food, even if it involved delayed accumulation of the rewards via the token transfer task. These results demonstrate that chimpanzees can exhibit self-control in situations involving social interactions, and they encourage further research into this important aspect of the self-control scenario.     

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     

Experimental field study of hand preference in wild black-horned (<Emphasis Type="Italic">Cebus nigritus</Emphasis>) and white-faced (<Emphasis Type="Italic">Cebus capucinus</Emphasis>) capuchins: evidence for individual and species differences

In this experimental field investigation, we compare the degree to which wild capuchins in Brazil (Cebus nigritus) and Costa Rica (Cebus capucinus) exhibit individual- and population-level handedness during three visually-guided tasks. These tasks required reaching to remove a large leaf covering a hidden food reward, seizing the food reward, and manipulating a tool (pulling a wooden dowel) in order to obtain access to an embedded food reward. Studies in some populations of captive capuchins indicate evidence for both individual hand preferences and population-level handedness. In this study, six of eight wild C. capucinus and six of seven wild C. nigritus exhibited a significant hand preference during individual tasks, but no individual exhibited a consistent preference across all three tasks. Task-specialization, or the tendency for most individuals in the same group or population to use the same hand to accomplish a particular task, also was evaluated. Cebus nigritus showed a significant bias toward the use of the right hand in removing the leaf. Although the number of individual capuchins in both species that manipulated the dowels was limited (N = 7), each individual that manipulated the dowels in eight or more instances had a positive handedness index, suggesting a greater use of the right hand to accomplish this task. Overall, our results provide preliminary support for individual- and population-level handedness in wild capuchin monkeys.     

Multi-stage mental process for economic choice in capuchins

We studied economic choice behavior in capuchin monkeys by offering them to choose between two different foods available in variable amounts. When monkeys selected between familiar foods, their choice patterns were well-described in terms of relative value of the two foods. A leading view in economics and biology is that such behavior results from stimulus-response associations acquired through experience. According to this view, values are not psychologically real; they can only be defined a posteriori. One prediction of this associative model is that animals faced for the first time with a new pair of foods learn to choose between them gradually. We tested this prediction. Surprisingly, we find that monkeys choose as effectively between new pairs of foods as they choose between familiar pairs of foods. We therefore, propose a cognitive model in which economic choice results from a two-stage mental process of value-assignment and decision-making. In a follow-up experiment, we find that the relative value assigned to three foods in sessions in which we tested them against each other combine according to transitivity.     

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.     

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).     

Can squirrel monkeys (Saimiri sciureus) learn self-control? A study using food array selection tests and reverse-reward contingency

Eight squirrel monkeys (Saimiri sciureus) were presented with 2 stimulus arrays, namely 1 and 4 pieces of food, but they received only the array other than the one they reached for. In this reverse-reward condition, all monkeys initially showed a strong preference for the larger array. One monkey learned to reach toward the smaller array when a large-or-none reward contingency was applied (i.e., no reward followed a reach toward the larger array, but this array was given for a reach toward the smaller array). When correction trials and time-out were added to the large-or-none procedure, all remaining monkeys except 1 learned this form of self-control. Performance was maintained when correction trials were discontinued, the original reverse-reward condition was rerun, and novel array-size pairs were presented. This study demonstrates one form of self-control in a New World primate and shows the reverse-reward procedure to be a potentially valuable method for assessing species and individual differences in self-control and numerosity-related abilities.