Does inequity aversion depend on a frustration effect? A test with capuchin monkeys (Cebus apella)

Brosnan and de Waal (Nature 425:297–299, 2003) reported that if a witness monkey saw a model monkey receive a high-value food, the witness was more inclined to reject a previously acceptable, but low-value food. Later work demonstrated that this alleged inequity aversion might be due to frustration induced by switching subjects from their role as models receiving a high-value food to the role of witnesses receiving a low-value food. In the present study, pairs of female capuchins exchanged a token for either a high- or a low-value food without switching their model–witness roles. Witnesses could exchange a token for a low-value food after an adjacent model had exchanged a token for the same food (Equity Condition) or for a high-value food (Inequity Condition). Failure- and latency-to-exchange measures showed that witnesses were unaffected by the food type offered to models (no inequity aversion). Moreover, models were unaffected by their history of food type offered (no frustration). These results join earlier work suggesting that alleged inequity effects depend on frustration-induction procedures. Furthermore, inequity effects sometimes fail to emerge because frustration induction in nonhuman primates is labile. This study complied with protocols approved by the Italian Health Ministry and all procedures were performed in full accordance with the European law on humane care and use of laboratory animals.     

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.     

The ecological rationality of delay tolerance: insights from capuchin monkeys

Both human and non-human animals often face decisions between options available at different times, and the capacity of delaying gratification has usually been considered one of the features distinguishing humans from other animals. However, this characteristic can widely vary across individuals, species, and types of task and it is still unclear whether it is accounted for by phylogenetic relatedness, feeding ecology, social structure, or metabolic rate. To disentangle these hypotheses, we evaluated temporal preferences in capuchin monkeys, South-American primates that, despite splitting off from human lineage approximately 35 million years ago, show striking behavioural analogies with the great apes. Then, we compared capuchins’ performance with that of the other primate species tested so far with the same procedure. Overall, capuchins showed a delay tolerance significantly higher than closely related species, such as marmosets and tamarins, and comparable to that shown by great apes. Capuchins’ tool use abilities might explain their comparatively high preference for delayed options in inter-temporal choices. Moreover, as in humans, capuchin females showed a greater delay tolerance than males, possibly because of their less opportunistic foraging style. Thus, our results shed light on the evolutionary origins of self-control supporting explanations of delay tolerance in terms of feeding ecology.     

Conformism in the food processing techniques of white-faced capuchin monkeys (Cebus capucinus)

Researchers of “culture” have long been interested in the role of social learning in establishing patterns of behavioral variation in wild animals, but very few studies examine this issue using a developmental approach. This 7-year study examines the acquisition of techniques used to process Luehea candida fruits in a wild population of white-faced capuchin monkeys, Cebus capucinus, residing in and near Lomas Barbudal Biological Reserve, Costa Rica. The two techniques for extracting seeds (pounding or scrubbing) were approximately equal in efficiency, and subjects experimented with both techniques before settling on one technique—typically the one they most frequently observed. In a sample of 106 subjects that had already settled on a preferred technique, the females adopted the maternal technique significantly more often than expected by chance, but the males did not. Using a longitudinal approach, I examined the acquisition of Luehea processing techniques during the first 5 years of life. Regression analysis revealed that the technique most frequently observed (measured as proportion of Luehea processing bouts observed that used pounding as opposed to scrubbing) significantly predicted the technique adopted by female observers, particularly in the second year of life; the amount of impact of the observed technique on the practiced technique was somewhat less significant for male observers. These results held true for (a) observations of maternal technique only, (b) observations of technique used by all individuals other than the mother, and (c) observations of maternal and non-maternal techniques combined. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Do capuchin monkeys use weight to select hammer tools?

The extent to which tool-using animals take into account the properties of the tool is little explored. The use of percussors to crack open encapsulated fruit is a complex form of tool use, the choice of an adequate tool being a critical aspect in success. Several properties (e.g., material, resistance, friability, shape and weight) affect the suitability of an object to open a hard-shelled nut, with weight being amongst the most important factors. In general, heavier tools require fewer strikes to crack open a nut.     

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

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