Frans B. M. de Waal

Empathy: Its ultimate and proximate bases

There is disagreement in the literature about the exact nature of the phenomenon of empathy. There are emotional, cognitive, and conditioning views, applying in varying degrees across species. An adequate description of the ultimate and proximate mechanism can integrate these views. Proximately, the perception of an objects state activates the subjects corresponding representations, which in turn activate somatic and autonomic responses. This mechanism supports basic behaviors (e.g., alarm, social facilitation, vicariousness of emotions, mother-infant responsiveness, and the modeling of competitors and predators) that are crucial for the reproductive success of animals living in groups. The Perception-Action Model (PAM), together with an understanding of how representations change with experience, can explain the major empirical effects in the literature (similarity, familiarity, past experience, explicit teaching, and salience). It can also predict a variety of empathy disorders. The interaction between the PAM and prefrontal functioning can also explain different levels of empathy across species and age groups. This view can advance our evolutionary understanding of empathy beyond inclusive fitness and reciprocal altruism and can explain different levels of empathy across individuals, species, stages of development, and situations.

Monkeys reject unequal pay

During the evolution of cooperation it may have become critical for individuals to compare their own efforts and pay-offs with those of others. Negative reactions may occur when expectations are violated. One theory proposes that aversion to inequity can explain human cooperation within the bounds of the rational choice model, and may in fact be more inclusive than previous explanations. Although there exists substantial cultural variation in its particulars, this ‘sense of fairness’ is probably a human universal that has been shown to prevail in a wide variety of circumstances. However, we are not the only cooperative animals, hence inequity aversion may not be uniquely human. Many highly cooperative nonhuman species seem guided by a set of expectations about the outcome of cooperation and the division of resources. Here we demonstrate that a nonhuman primate, the brown capuchin monkey (Cebus apella), responds negatively to unequal reward distribution in exchanges with a human experimenter. Monkeys refused to participate if they witnessed a conspecific obtain a more attractive reward for equal effort, an effect amplified if the partner received such a reward without any effort at all. These reactions support an early evolutionary origin of inequity aversion.

Reconciliation and consolation among chimpanzees

Summary1.After agonistic interactions among chimpanzees, former opponents often come into non-violent body contact. The present paper gives a quantitative description of such contacts among the chimpanzees of a large semi-free-living colony at the Arnhem Zoo, in order to establish whether these post-conflict contacts are of a specific nature.2.Our data indicate that former opponents preferentially make body contact with each other rather than with third partners. They tend to contact each other shortly after the conflict and show special behaviour patterns during these first contacts. Data on contacts of the aggressed party with third animals indicate that such contacts are characterized by the same special behaviour patterns as first interopponent contacts. These patterns are: ‘kiss’, ‘embrace’, ‘hold-out-hand’, ‘submissive vocalization’ and ‘touch’.3.Such interactions apparently serve an important socially homeostatic function and we termed them ‘reconciliation’ (i.e. contact between former opponents) and ‘consolation’ (i.e. contact of the aggressed party with a third animal). According to our data, ‘kissing’ is characteristic of reconciliation and ‘embracing’ of consolation.

Conformity to cultural norms of tool use in chimpanzees.

Rich circumstantial evidence suggests that the extensive behavioural diversity recorded in wild great apes reflects a complexity of cultural variation unmatched by species other than our own. However, the capacity for cultural transmission assumed by this interpretation has remained difficult to test rigorously in the field, where the scope for controlled experimentation is limited. Here we show that experimentally introduced technologies will spread within different ape communities. Unobserved by group mates, we first trained a high-ranking female from each of two groups of captive chimpanzees to adopt one of two different tool-use techniques for obtaining food from the same ‘Pan-pipe’ apparatus, then re-introduced each female to her respective group. All but two of 32 chimpanzees mastered the new technique under the influence of their local expert, whereas none did so in a third population lacking an expert. Most chimpanzees adopted the method seeded in their group, and these traditions continued to diverge over time. A subset of chimpanzees that discovered the alternative method nevertheless went on to match the predominant approach of their companions, showing a conformity bias that is regarded as a hallmark of human culture.

Policing stabilizes construction of social niches in primates.

All organisms interact with their environment, and in doing so shape it, modifying resource availability. Termed niche construction, this process has been studied primarily at the ecological level with an emphasis on the consequences of construction across generations. We focus on the behavioural process of construction within a single generation, identifying the role a robustness mechanism—conflict management—has in promoting interactions that build social resource networks or social niches. Using ‘knockout’ experiments on a large, captive group of pigtailed macaques (Macaca nemestrina), we show that a policing function, performed infrequently by a small subset of individuals, significantly contributes to maintaining stable resource networks in the face of chronic perturbations that arise through conflict. When policing is absent, social niches destabilize, with group members building smaller, less diverse, and less integrated grooming, play, proximity and contact-sitting networks. Instability is quantified in terms of reduced mean degree, increased clustering, reduced reach, and increased assortativity. Policing not only controls conflict, we find it significantly influences the structure of networks that constitute essential social resources in gregarious primate societies. The structure of such networks plays a critical role in infant survivorship, emergence and spread of cooperative behaviour, social learning and cultural traditions.

Reconciliation and Redirected Affection in Rhesus Monkeys

The question whether rhesus monkeys reconcile was empirically translated as: Do they seek non-agonistic contact with former adversaries? The study concerned a captive group of forty-one monkeys, Macaca mulatta. Participants in 350 aggressive incidents were followed both immediately after the incident and during matched control periods. Comparison of the two sets of data showed that: - After the incident former opponents had an increased tendency to approach and contact each other. - The attraction between them was selective, i.e., the number of inter-opponent contacts showed not only an absolute but also a relative increase. - Also former alliance partners showed attraction to each other. - Inter-opponent contacts were behaviorally distinctive. The most characteristic behavior patterns were embrace, lipsmack and redirected threat. - Conciliatory tendency increased with general bond strength between individuals, even though the first measure had a built-in correction for the second. - A higher conciliatory tendency among matrilineal relatives could be fully explained by the above mentioned influence of bond strength. - General effects of agonistic interactions included a grooming increase for violent aggressors, a grooming decrease for victim of severe aggression, and an increased receipt of grooming for mild aggressors. - Grooming of outsiders by violent aggressors depended on the intensity of the bond between aggressor and victim. Therefore, this grooming behavior was interpreted as redirected affection.

The Chimpanzee's service economy: Food for grooming

Abstract Evidence is presented that the reciprocal exchange of social services among chimpanzees ( Pan troglodytes ) rests on cognitive abilities that allow current behavior to be contingent upon a history of interaction. Food sharing within a captive colony of chimpanzees was studied by means of 200 food trials, conducted on separate daus over a 3-year period, in which 6,972 approaches occurred among the nine adults in the colony. The success rate of each adult, A, to obtain food from another adult, B, was compared with grooming interactions between A and B in the 2 hours prior to each food trial. The tendency of B to share with A was higher if A had groomed B than if A had not done so. The exchange was partner-specific, i.e., the effect of previous grooming on the behavior of food possessors was limited to the grooming partner. Grooming did not affect subsequent sharing by the groomer, only by the groomee. The effect of grooming was greatest for pairs of adults who rarely groomed. Nevertheless, the effect was general: 31 dyadic directions showed an increase in sharing following grooming, and only 11 a decrease. Food possessors actively resisted approaches by individuals who had not groomed them. After food trials there was a significant reduction of grooming by previous possessors towards those individuals with whom they had shared.

Food sharing and reciprocal obligations among chimpanzees

Food sharing has been proposed as the propeller of hominid evolution, particularly of the development of systems of mutual social obligation. Yet, food sharing in our closest relative has never been subjected to a rigorous analysis of reciprocity. Provisioning of branches and leaves to nineteen chimpanzees (Pan troglodytes) in an outdoor corral resulted in 4,653 interactions over food. Food trials were characterised by increased levels of aggressive as well as appeasement behavior. Food exchanges among the nine adult group members (one male, eight females) were remarkably balanced per dyad, and sharing of individual A with B correlated positively with sharing of B with A (r = 0·552). After adjustment of the data for effects of proximity and dominance relationships, a significant degree of reciprocity remained. Individual As sharing with B on a particular day, however, could not be predicted on the basis of Bs sharing with A on the previous trial day. Social grooming earlier during the same trial day did have an effect. Individual A was more likely to share with B after B had groomed A, but less likely after A had groomed B. This suggests a turn-taking rule in the exchange of social favors, which prevents one-sided accumulation of benefits. Individuals who were reluctant to share (i.e., showed a low rate of food distribution) had a higher probability of encountering aggression when they themselves approached food possessors.

Tolerance for inequity may increase with social closeness in chimpanzees

Economic decision–making depends on our social environment. Humans tend to respond differently to inequity in close relationships, yet we know little about the potential for such variation in other species. We examine responses to inequity in several groups of chimpanzees (Pan troglodytes) in a paradigm similar to that used previously in capuchin monkeys (Cebus apella). We demonstrate that, like capuchin monkeys, chimpanzees show a response to inequity of rewards that is based upon the partner receiving the reward rather than the presence of the reward alone. However, we also found a great amount of variation between groups tested, indicating that chimpanzees, like people, respond to inequity in a variable manner, which we speculate could be caused by such variables as group size, the social closeness of the group (as reflected in length of time that the group has been together) and group–specific traditions.

Ape gestures and language evolution

The natural communication of apes may hold clues about language origins, especially because apes frequently gesture with limbs and hands, a mode of communication thought to have been the starting point of human language evolution. The present study aimed to contrast brachiomanual gestures with orofacial movements and vocalizations in the natural communication of our closest primate relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We tested whether gesture is the more flexible form of communication by measuring the strength of association between signals and specific behavioral contexts, comparing groups of both the same and different ape species. Subjects were two captive bonobo groups, a total of 13 individuals, and two captive chimpanzee groups, a total of 34 individuals. The study distinguished 31 manual gestures and 18 facial/vocal signals. It was found that homologous facial/vocal displays were used very similarly by both ape species, yet the same did not apply to gestures. Both within and between species gesture usage varied enormously. Moreover, bonobos showed greater flexibility in this regard than chimpanzees and were also the only species in which multimodal communication (i.e., combinations of gestures and facial/vocal signals) added to behavioral impact on the recipient.