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de Waal, F. B. M., & Ferrari, P. F. (2010). Towards a bottom-up perspective on animal and human cognition. Trends Cognit. Sci., 14(5), 201–207.
Abstract: Over the last few decades, comparative cognitive research has focused on the pinnacles of mental evolution, asking all-or-nothing questions such as which animals (if any) possess a theory of mind, culture, linguistic abilities, future planning, and so on. Research programs adopting this top-down perspective have often pitted one taxon against another, resulting in sharp dividing lines. Insight into the underlying mechanisms has lagged behind. A dramatic change in focus now seems to be under way, however, with increased appreciation that the basic building blocks of cognition might be shared across a wide range of species. We argue that this bottom-up perspective, which focuses on the constituent capacities underlying larger cognitive phenomena, is more in line with both neuroscience and evolutionary biology.
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de Waal, F. B. M., & Luttrell, L. M. (1988). Mechanisms of social reciprocity in three primate species: Symmetrical relationship characteristics or cognition? Ethology and Sociobiology, 9(2–4), 101–118.
Abstract: Agonistic intervention behavior was observed in captive groups of chimpanzees (Pan troglodytes), rhesus monkeys (Macaca mulatta), and stumptail monkeys (M. arctoides). Reciprocity correlations of interventions were determined while removing from the data the effects of several symmetrical relationship characteristics, that is, matrillineal kinship, proximity relations, and same-sex combination. It was considered likely that if significant reciprocity persisted after controlling for these characteristics, the reciprocity was based on cognitive mechanisms. Statistical significance was tested by means of recently developed matrix permutation procedures. All three species exhibited significant reciprocity with regard to beneficial interventions, even after controlling for symmetrical traits. Harmful interventions were, however, reciprocal among chimpanzees only. This species showed a “revenge system”, that is, if A often intervened against B, B did the same to A. In contrast, both macaque species showed significantly inversed reciprocity in their harmful interventions: if A often intervened against B, B rarely intervened against A. Further analysis indicates that the strict hierarchy of macaques prevents them from achieving complete reciprocity. Compared to chimpanzees, macaques rarely intervene against higher ranking group members. The observed contrast can be partially explained on the basis of differences in available space, as indicated by a comparison of indoor and outdoor living conditions for the chimpanzee colony. Yet, even when such spatial factors are taken into account, substantial behavior differences between chimpanzees and macaques remain.
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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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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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de Waal, F. B. M. (2004). Peace lessons from an unlikely source. PLoS. Biol., 2(4), E101.
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Bonnie, K. E., Horner, V., Whiten, A., & de Waal, F. B. M. (2007). Spread of arbitrary conventions among chimpanzees: a controlled experiment. Proc Biol Sci, 274(1608), 367–372.
Abstract: Wild chimpanzees (Pan troglodytes) have a rich cultural repertoire--traditions common in some communities are not present in others. The majority of reports describe functional, material traditions, such as tool use. Arbitrary conventions have received far less attention. In the same way that observations of material culture in wild apes led to experiments to confirm social transmission and identify underlying learning mechanisms, experiments investigating how arbitrary habits or conventions arise and spread within a group are also required. The few relevant experimental studies reported thus far have relied on cross-species (i.e. human-ape) interaction offering limited ecological validity, and no study has successfully generated a tradition not involving tool use in an established group. We seeded one of two rewarded alternative endpoints to a complex sequence of behaviour in each of two chimpanzee groups. Each sequence spread in the group in which it was seeded, with many individuals unambiguously adopting the sequence demonstrated by a group member. In one group, the alternative sequence was discovered by a low ranking female, but was not learned by others. Since the action-sequences lacked meaning before the experiment and had no logical connection with reward, chimpanzees must have extracted both the form and benefits of these sequences through observation of others.
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Flack, J. C., de Waal, F. B. M., & Krakauer, D. C. (2005). Social structure, robustness, and policing cost in a cognitively sophisticated species. Am Nat, 165(5), E126–139.
Abstract: Conflict management is one of the primary requirements for social complexity. Of the many forms of conflict management, one of the rarest and most interesting is third-party policing, or intervening impartially to control conflict. Third-party policing should be hard to evolve because policers personally pay a cost for intervening, while the benefits are diffused over the whole group. In this study we investigate the incidence and costs of policing in a primate society. We report quantitative evidence of non-kin policing in the nonhuman primate, the pigtailed macaque. We find that policing is effective at reducing the intensity of or terminating conflict when performed by the most powerful individuals. We define a measure, social power consensus, that predicts effective low-cost interventions by powerful individuals and ineffective, relatively costly interventions by low-power individuals. Finally, we develop a simple probabilistic model to explore whether the degree to which policing can effectively reduce the societal cost of conflict is dependent on variance in the distribution of power. Our data and simple model suggest that third-party policing effectiveness and cost are dependent on power structure and might emerge only in societies with high variance in power.
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Plotnik, J. M., de Waal, F. B. M., & Reiss, D. (2006). Self-recognition in an Asian elephant. Proc. Natl. Acad. Sci. U.S.A., 103(45), 17053–17057.
Abstract: Considered an indicator of self-awareness, mirror self-recognition (MSR) has long seemed limited to humans and apes. In both phylogeny and human ontogeny, MSR is thought to correlate with higher forms of empathy and altruistic behavior. Apart from humans and apes, dolphins and elephants are also known for such capacities. After the recent discovery of MSR in dolphins (Tursiops truncatus), elephants thus were the next logical candidate species. We exposed three Asian elephants (Elephas maximus) to a large mirror to investigate their responses. Animals that possess MSR typically progress through four stages of behavior when facing a mirror: (i) social responses, (ii) physical inspection (e.g., looking behind the mirror), (iii) repetitive mirror-testing behavior, and (iv) realization of seeing themselves. Visible marks and invisible sham-marks were applied to the elephants' heads to test whether they would pass the litmus “mark test” for MSR in which an individual spontaneously uses a mirror to touch an otherwise imperceptible mark on its own body. Here, we report a successful MSR elephant study and report striking parallels in the progression of responses to mirrors among apes, dolphins, and elephants. These parallels suggest convergent cognitive evolution most likely related to complex sociality and cooperation.
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Flack, J. C., Girvan, M., de Waal, F. B. M., & Krakauer, D. C. (2006). Policing stabilizes construction of social niches in primates. Nature, 439(7075), 426–429.
Abstract: 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.
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Preston, S. D., & de Waal, F. B. M. (2002). Empathy: Its ultimate and proximate bases. Behav Brain Sci, 25(1), 1–20; discussion 20–71.
Abstract: 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 object's state activates the subject's 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.
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