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Brosnan, S. F., & de Waal, F. B. M. (2005). Responses to a simple barter task in chimpanzees, Pan troglodytes. Primates, 46(3), 173–182.
Abstract: Chimpanzees (Pan troglodytes) frequently participate in social exchange involving multiple goods and services of variable value, yet they have not been tested in a formalized situation to see whether they can barter using multiple tokens and rewards. We set up a simple barter economy with two tokens and two associated rewards and tested chimpanzees on their ability to obtain rewards by returning the matching token in situations in which their access to tokens was unlimited or limited. Chimpanzees easily learned to associate value with the tokens, as expected, and did barter, but followed a simple strategy of favoring the higher-value token, regardless of the reward proffered, instead of a more complex but more effective strategy of returning the token that matched the reward. This response is similar to that shown by capuchin monkeys in our previous study. We speculate that this response, while not ideal, may be sufficient to allow for stability of the social exchange system in these primates, and that the importance of social barter to both species may have led to this convergence of strategies.
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Bonnie, K. E., & de Waal, F. B. M. (2006). Affiliation promotes the transmission of a social custom: handclasp grooming among captive chimpanzees. Primates, 47(1), 27–34.
Abstract: Handclasp grooming is a unique social custom, known to occur regularly among some, but not all populations of chimpanzees (Pan troglodytes). As with other cultural behaviors, it is assumed that this distinctive grooming posture is learned socially by one individual from another. However, statistical comparisons among factors thought to influence how a behavior spreads within a group have never, to our knowledge, been conducted. In the present study, the origination and spread of handclasp grooming in a group of captive chimpanzees was followed throughout more than 1,500 h of observation over a period of 12 years. We report on the frequency, bout duration, and number and demography of performers throughout the study period, and compare these findings to those reported for wild populations. We predicted that dyads with strong affiliative ties, measured by time spent in proximity to and grooming one another, were likely to develop a handclasp grooming partnership during the study period. A quadratic assignment procedure was used to compare correlations among observed frequencies of grooming and proximity with handclasp grooming in all possible dyads within the group. As predicted, the formation of new handclasp grooming dyads was positively correlated with the rate of overall grooming and proximity within a dyad. In addition, in nearly all dyads formed, at least one individual had been previously observed to handclasp groom. We concluded that affiliation and individual experience determines the transmission of handclasp grooming among captive chimpanzees.
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Parr, L. A., Matheson, M. D., Bernstein, I. S., & De Waal, F. B. M. (1997). Grooming down the hierarchy: allogrooming in captive brown capuchin monkeys, Cebus apella. Anim. Behav., 54(2), 361–367.
Abstract: Observations of captive female brown capuchin monkeys in five groups revealed that grooming is primarily the occupation of dominant females at both the individual and dyadic levels. When categorized according to rank class, alpha females were the only class to perform significantly more grooming than they received. These results are inconsistent with reports on vervets, baboons and macaques, and suggest that grooming in capuchin monkeys may have different functions from those reported for cercopithecine primates. A dyadic analysis revealed, however, that grooming occurred more often between closely ranked females, similar to what is seen in several Old World monkey species. Therefore, some aspects of grooming in capuchins are similar to that seen in Old World monkeys, but the way they distribute grooming is different, which may prompt a re-evaluation of current theories regarding the social function of allogrooming in non-human primates.
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de Waal, F. B. M. (2008). Putting the Altruism Back into Altruism: The Evolution of Empathy. Annu Rev Psychol, 59(1), 279–300.
Abstract: Evolutionary theory postulates that altruistic behavior evolved for the return-benefits it bears the performer. For return-benefits to play a motivational role, however, they need to be experienced by the organism. Motivational analyses should restrict themselves, therefore, to the altruistic impulse and its knowable consequences. Empathy is an ideal candidate mechanism to underlie so-called directed altruism, i.e., altruism in response to anothers's pain, need, or distress. Evidence is accumulating that this mechanism is phylogenetically ancient, probably as old as mammals and birds. Perception of the emotional state of another automatically activates shared representations causing a matching emotional state in the observer. With increasing cognition, state-matching evolved into more complex forms, including concern for the other and perspective-taking. Empathy-induced altruism derives its strength from the emotional stake it offers the self in the other's welfare. The dynamics of the empathy mechanism agree with predictions from kin selection and reciprocal altruism theory.
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Call, J., Aureli, F., & de Waal, F. B. M. (2002). Postconflict third-party affiliation in stumptailed macaques. Anim. Behav., 63(2), 209–216.
Abstract: Stumptailed macaques, Macaca arctoides, are characterized by high levels of postconflict affiliative contacts between opponents. We investigated the occurrence of postconflict affiliative contacts between opponents and third parties that were not involved in the original conflict. We collected 10-min focal observations during postconflict and control periods in which we recorded all aggressive and affiliative behaviours between opponents and third parties. We distinguished three types of third parties depending on the relationship with the focal animal: own kin, opponent's kin and individuals unrelated to both opponents. We analysed the interactions with third parties separately, while distinguishing two classes of affiliative behaviours: (1) allogrooming and contact sitting and (2) sociosexual behaviours (e.g. genital inspection). The macaques showed differences between postconflict and control periods in their affiliative contacts with third parties. Aggressors received more postconflict grooming and contact sitting from their opponents' kin, received more sociosexual behaviour from their own kin and unrelated individuals, and directed more sociosexual behaviour to unrelated individuals. Victims received and directed less postconflict grooming from and towards their own kin. They received more postconflict sociosexual behaviour from all partners except their own kin and directed more sociosexual behaviour to all partners except the opponent's kin. This study establishes the occurrence of multiple postconflict triadic affiliation in stumptailed macaques, and is the first to show that victims receive contacts from third parties in a cercopithecine species, a behaviour previously described only in chimpanzees. It also highlights the importance of analysing the different affiliative behaviours separately in postconflict situations. Otherwise, many of the patterns we report, especially those involving victims, would have been missed.
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Brosnan, S. F., Freeman, C., & De Waal, F. B. M. (2006). Partner's behavior, not reward distribution, determines success in an unequal cooperative task in capuchin monkeys. Am. J. Primatol., 68(7), 713–724.
Abstract: It was recently demonstrated that capuchin monkeys notice and respond to distributional inequity, a trait that has been proposed to support the evolution of cooperation in the human species. However, it is unknown how capuchins react to inequitable rewards in an unrestricted cooperative paradigm in which they may freely choose both whether to participate and, within the bounds of their partner's behavior, which reward they will receive for their participation. We tested capuchin monkeys with such a design, using a cooperative barpull, which has been used with great success in the past. Contrary to our expectations, the equity of the reward distribution did not affect success or pulling behavior. However, the behavior of the partner in an unequal situation did affect overall success rates: pairs that had a tendency to alternate which individual received the higher-value food in unequal reward situations were more than twice as successful in obtaining rewards than pairs in which one individual dominated the higher-value food. This ability to equitably distribute rewards in inherently biased cooperative situations has profound implications for activities such as group hunts, in which multiple individuals work together for a single, monopolizable reward.
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Dindo, M., & De Waal, F. B. M. (2007). Partner effects on food consumption in brown capuchin monkeys. Am. J. Primatol., 69(4), 448–456.
Abstract: It has been claimed that capuchin monkeys (Cebus apella) show inequity aversion in relation to food rewards for a simple exchange task. However, other factors may affect the willingness of a monkey to consume foods of high or low value in the presence of a conspecific. In this study, pairs of monkeys were presented with unequally valued foods, but without any task-performance: they simply received the food under four experimental conditions. By looking at the rate of collection and consumption of low-valued cucumber slices we expected to see variation dependent on whether the partner either had 1) cucumber (equity), 2) grape (inequity), 3) inaccessible cucumber or 4) inaccessible grape. Testing 12 adult capuchin monkeys, our findings differed from those of other authors in that the monkeys failed to show negative reactions to inequity, but rather responded with scramble competition (i.e., fast food collection) in the presence of a conspecific without access to food. They also showed facilitated consumption in the presence of a conspecific consuming high-valued food. Possibly, (in)equity plays a different role if food serves as a reward for a task rather than if it is simply made available for consumption. Am. J. Primatol. 69:1-9, 2007. (c) 2006 Wiley-Liss, Inc.
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Brosnan, S. F., & de Waal, F. B. M. (2004). A concept of value during experimental exchange in brown capuchin monkeys, Cebus apella. Folia Primatol (Basel), 75(5), 317–330.
Abstract: We evaluated the response of brown capuchin monkeys to two differentially valued tokens in an experimental exchange situation akin to a simple barter. Monkeys were given a series of three tests to evaluate their ability to associate tokens with food, then their responses were examined in a barter situation in which tokens were either limited or unlimited. Capuchins did not perform barter in the typical sense, returning the tokens which were associated with the reward. However, females, but not males, showed a different response, preferring the higher-value token. This may indicate that they learned to prefer one token over the other rather than to associate the tokens with their specific rewards. This sex difference parallels previous findings of greater reciprocity in female brown capuchins than in males.
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de Waal, F. B. M., Dindo, M., Freeman, C. A., & Hall, M. J. (2005). The monkey in the mirror: hardly a stranger. Proc. Natl. Acad. Sci. U.S.A., 102(32), 11140–11147.
Abstract: It is widely assumed that monkeys see a stranger in the mirror, whereas apes and humans recognize themselves. In this study, we question the former assumption by using a detailed comparison of how monkeys respond to mirrors versus live individuals. Eight adult female and six adult male brown capuchin monkeys (Cebus apella) were exposed twice to three conditions: (i) a familiar same-sex partner, (ii) an unfamiliar same-sex partner, and (iii) a mirror. Females showed more eye contact and friendly behavior and fewer signs of anxiety in front of a mirror than they did when exposed to an unfamiliar partner. Males showed greater ambiguity, but they too reacted differently to mirrors and strangers. Discrimination between conditions was immediate, and blind coders were able to tell the difference between monkeys under the three conditions. Capuchins thus seem to recognize their reflection in the mirror as special, and they may not confuse it with an actual conspecific. Possibly, they reach a level of self-other distinction intermediate between seeing their mirror image as other and recognizing it as self.
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Horner, V., Whiten, A., Flynn, E., & de Waal, F. B. M. (2006). Faithful replication of foraging techniques along cultural transmission chains by chimpanzees and children. Proc. Natl. Acad. Sci. U.S.A., 103(37), 13878–13883.
Abstract: Observational studies of wild chimpanzees (Pan troglodytes) have revealed population-specific differences in behavior, thought to represent cultural variation. Field studies have also reported behaviors indicative of cultural learning, such as close observation of adult skills by infants, and the use of similar foraging techniques within a population over many generations. Although experimental studies have shown that chimpanzees are able to learn complex behaviors by observation, it is unclear how closely these studies simulate the learning environment found in the wild. In the present study we have used a diffusion chain paradigm, whereby a behavior is passed from one individual to the next in a linear sequence in an attempt to simulate intergenerational transmission of a foraging skill. Using a powerful three-group, two-action methodology, we found that alternative methods used to obtain food from a foraging device (“lift door” versus “slide door”) were accurately transmitted along two chains of six and five chimpanzees, respectively, such that the last chimpanzee in the chain used the same method as the original trained model. The fidelity of transmission within each chain is remarkable given that several individuals in the no-model control group were able to discover either method by individual exploration. A comparative study with human children revealed similar results. This study is the first to experimentally demonstrate the linear transmission of alternative foraging techniques by non-human primates. Our results show that chimpanzees have a capacity to sustain local traditions across multiple simulated generations.
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