Mammalian empathy: behavioural manifestations and neural basis.

Recent research on empathy in humans and other mammals seeks to dissociate emotional and cognitive empathy. These forms, however, remain interconnected in evolution, across species and at the level of neural mechanisms. New data have facilitated the development of empathy models such as the perception-action model (PAM) and mirror-neuron theories. According to the PAM, the emotional states of others are understood through personal, embodied representations that allow empathy and accuracy to increase based on the observer's past experiences. In this Review, we discuss the latest evidence from studies carried out across a wide range of species, including studies on yawn contagion, consolation, aid-giving and contagious physiological affect, and we summarize neuroscientific data on representations related to another's state.

Fish, mirrors, and a gradualist perspective on self-awareness.

The mirror mark test has encouraged a binary view of self-awareness according to which a few species possess this capacity whereas others do not. Given how evolution works, however, we need a more gradualist model of the various ways in which animals construe a self and respond to mirrors. The recent study on cleaner wrasses (Labroides dimidiatus) by Kohda and colleagues highlights this need by presenting results that, due to ambiguous behavior and the use of physically irritating marks, fall short of mirror self-recognition. The study suggests an intermediate level of mirror understanding, closer to that of monkeys than hominids.

Ethological observations of social behavior in the operating room.

Operating rooms (ORs) are inhabited by hierarchical, mixed-gender clinical teams that are often prone to conflict. In evolutionary terms, one expects more within- than between-gender rivalries, especially since the OR is a place where all sorts of social interactions occur, not merely technical communications. To document the full range of behavior, the present study used ethological observation techniques, recording live all social behavior by the team. Using an ethogram, 6,348 spontaneous social interactions and nontechnical communications were timestamped during 200 surgical procedures. Cooperation sequences (59.0%) were more frequent than conflict sequences (2.8%), which ranged from constructive differences of opinion to discord and distraction that could jeopardize patient safety. Behavior varied by clinical role and with the gender composition in the OR. Conflict was initiated mostly down the hierarchy between individuals several ranks apart. Cooperation tended to increase with a rising proportion of females in the OR, but the most pronounced effect concerned the interaction between both genders. If the attending surgeon's gender differed from that of the majority of other personnel in the OR, cooperation was significantly more common.

Chimpanzees (Pan troglodytes) tolerate some degree of inequity while cooperating but refuse to donate effort for nothing.

In cooperative hunting, a carcass cannot be divided equally, and hunts may be unsuccessful. We studied how chimpanzees respond to these two variables, working for unequal rewards and no rewards, which have been rarely included in experimental cooperative tasks. We presented chimpanzees with a task requiring three chimpanzees to work together and varied the reward structure in two separate experiments. In Experiment 1, two individuals received more rewards than the third, making the outcome unequal. We wanted to know if cooperation would continue or break down, and what mechanisms might maintain performance. Experiment 2 used equal rewards, but this time one or more locations were left unbaited on a proportion of trials. Thus, there was a chance of individuals working to receive nothing. In Experiment 1, the chimpanzees worked at a high rate, tolerating the unequal outcomes, with rank appearing to determine who got access to the higher-value locations. However, equal outcomes (used as a control) enhanced cooperative performance, most likely through motivational processes rather than the absence of inequity aversion. In Experiment 2, performance dropped off dramatically when the chimpanzees were not rewarded on every trial. Their strategy was irrational as donating effort would have led to more rewards in the long run for each individual. Our results lead to a hierarchy of performances by condition with equity > inequity > donating effort. Chimpanzees therefore tolerate mild inequity, but cannot tolerate receiving nothing when others are rewarded.

Chimpanzees ( Pan troglodytes) Are More Averse to Social Than Nonsocial Risk.

Social risk is a domain of risk in which the costs, benefits, and uncertainty of an action depend on the behavior of another individual. Humans overvalue the costs of a socially risky decision when compared with that of purely economic risk. Here, we played a trust game with 8 female captive chimpanzees ( Pan troglodytes) to determine whether this bias exists in one of our closest living relatives. A correlation between an individual's social- and nonsocial-risk attitudes indicated stable individual variation, yet the chimpanzees were more averse to social than nonsocial risk. This indicates differences between social and economic decision making and emotional factors in social risk taking. In another experiment using the same paradigm, subjects played with several partners with whom they had varying relationships. Preexisting relationships did not impact the subjects' choices. Instead, the apes used a tit-for-tat strategy and were influenced by the outcome of early interactions with a partner.

How chimpanzees cooperate in a competitive world.

Our species is routinely depicted as unique in its ability to achieve cooperation, whereas our closest relative, the chimpanzee (Pan troglodytes), is often characterized as overly competitive. Human cooperation is assisted by the cost attached to competitive tendencies through enforcement mechanisms, such as punishment and partner choice. To examine if chimpanzees possess the same ability to mitigate competition, we set up a cooperative task in the presence of the entire group of 11 adults, which required two or three individuals to pull jointly to receive rewards. This open-group set-up provided ample opportunity for competition (e.g., freeloading, displacements) and aggression. Despite this unique set-up and initial competitiveness, cooperation prevailed in the end, being at least five times as common as competition. The chimpanzees performed 3,565 cooperative acts while using a variety of enforcement mechanisms to overcome competition and freeloading, as measured by (attempted) thefts of rewards. These mechanisms included direct protest by the target, third-party punishment in which dominant individuals intervened against freeloaders, and partner choice. There was a marked difference between freeloading and displacement; freeloading tended to elicit withdrawal and third-party interventions, whereas displacements were met with a higher rate of direct retaliation. Humans have shown similar responses in controlled experiments, suggesting shared mechanisms across the primates to mitigate competition for the sake of cooperation.

Novice chimpanzees cooperate successfully in the presence of experts, but may have limited understanding of the task.

Despite many observations of cooperation in nature, laboratory studies often fail to find careful coordination between individuals who are solving a cooperative task. Further, individuals tested are often naïve to cooperative tasks and there has been little exploration of partnerships with mixed expertise. In the current study, we examined acquisition of a cooperative pulling task in a group with both expert (N = 4) and novice (N = 11) chimpanzees (Pan troglodytes). We used five measures of competence and understanding: (1) success at the task, (2) latency to succeed, (3) efficiency, (4) uncoordinated pulling, and (5) pulling when a partner was present versus absent. We found that novices showed evidence of trial and error learning and developed competence over time, whereas the behavior of experts did not change throughout the course of the study. In addition to looking at patterns over time, we compared the performance of novices in this mixed-expertise group to an earlier study of novices in a group of all-novices. Novices in the mixed-expertise group pulled the same overall amount but for shorter periods of time, leading to higher pulling rates than individuals in the all-novice group. Taken together, these results suggest that learning in the presence of experts led to rapid and frequent success, although not necessarily careful coordination.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34-38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Chimpanzee uses manipulative gaze cues to conceal and reveal information to foraging competitor.

Tactical deception has been widely reported in primates on a functional basis, but details of behavioral mechanisms are usually unspecified. We tested a pair of chimpanzees (Pan troglodytes) in the informed forager paradigm, in which the subordinate saw the location of hidden food and the dominant did not. We employed cross-correlations to examine temporal contingencies between chimpanzees' behavior: specifically how the direction of the subordinate's gaze and movement functioned to manipulate the dominant's searching behavior through two tactics, withholding, and misleading information. In Experiment 1, not only did the informed subordinate tend to stop walking toward a single high value food, but she also refrained from gazing toward it, thus, withholding potentially revealing cues from her searching competitor. In a second experiment, in which a moderate value food was hidden in addition to the high value food, whenever the subordinate alternated her gaze between the dominant and the moderate value food, she often paused walking for 5 s; this frequently recruited the dominant to the inferior food, functioning as a "decoy." The subordinate flexibly concealed and revealed gaze toward a goal, which suggests that not only can chimpanzees use visual cues to make predictions about behavior, but also that chimpanzees may understand that other individuals can exploit their gaze direction. These results substantiate descriptive reports of how chimpanzees use gaze to manipulate others, and to our knowledge are the first quantitative data to identify behavioral mechanisms of tactical deception. RESEARCH HIGHLIGHTS: Cross correlations show a subordinate chimpanzee tactically deceived a dominant by not gazing toward a valuable food (withholding), and recruiting to a "decoy" food (misleading). Chimpanzees understand that others can exploit their gaze direction.

An Ethogram to Quantify Operating Room Behavior.

BACKGROUND: The operating room (OR) is a highly social and hierarchical setting where interprofessional team members must work interdependently under pressure. Due primarily to methodological challenges, the social and behavioral sciences have had trouble offering insight into OR dynamics. PURPOSE: We adopted a method from the field of ethology for observing and quantifying the interpersonal interactions of OR team members. METHODS: We created and refined an ethogram, a catalog of all our subjects' observable social behaviors. The ethogram was then assessed for its feasibility and interobserver reliability. RESULTS: It was feasible to use an ethogram to gather data in the OR. The high interobserver reliability (Cohen's Kappa coefficients of 81 % and higher) indicates its utility for yielding largely objective, descriptive, quantitative data on OR behavior. CONCLUSIONS: The method we propose has potential for social research conducted in healthcare settings as complex as the OR.

Chimpanzee food preferences, associative learning, and the origins of cooking.

A recent report suggested that chimpanzees demonstrate the cognitive capacities necessary to understand cooking (Warneken & Rosati, 2015). We offer alternate explanations and mechanisms that could account for the behavioral responses of those chimpanzees, without invoking the understanding of cooking as a process. We discuss broader issues surrounding the use of chimpanzees in modeling hominid behavior and understanding aspects of human evolution.

Chimpanzees, cooking, and a more comparative psychology.

A recent report suggested that chimpanzees demonstrate the cognitive capacities necessary to understand cooking (Warneken & Rosati, 2015). We offered alternative explanations and mechanisms that could account for the behavioral responses of those chimpanzees, and questioned the manner in which the data were used to examine human evolution (Beran, Hopper, de Waal, Sayers, & Brosnan, 2015). Two commentaries suggested either that we were overly critical of the original report's claims and methodology (Rosati & Warneken, 2016), or that, contrary to our statements, early biological thinkers contributed little to questions concerning the evolutionary importance of cooking (Wrangham, 2016). In addition, both commentaries took issue with our treatment of chimpanzee referential models in human evolutionary studies. Our response offers points of continued disagreement as well as points of conciliation. We view Warneken and Rosati's general conclusions as a case of affirming the consequent-a logical conundrum in which, in this case, a demonstration of a partial list of the underlying abilities required for a cognitive trait/suite (understanding of cooking) are suggested as evidence for that ability. And although we strongly concur with both Warneken and Rosati (2015) and Wrangham (2016) that chimpanzee research is invaluable and essential to understanding humanness, it can only achieve its potential via the holistic inclusion of all available evidence-including that from other animals, evolutionary theory, and the fossil and archaeological records.

Development of socio-emotional competence in bonobos.

Social and emotional skills are tightly interlinked in human development, and both are negatively impacted by disrupted social development. The same interplay between social and emotional skills, including expressions of empathy, has received scant attention in other primates however, despite the growing interest in caring, friendships, and the fitness benefits of social skills. Here we examine the development of socio-emotional competence in juvenile bonobos (Pan paniscus) at a sanctuary in the Democratic Republic of the Congo, focusing on the interplay between various skills, including empathy-related responding. Most subjects were rehabilitated orphans, but some were born at the sanctuary and mother-reared there. We observed how juveniles with different rearing backgrounds responded to stressful events, both when the stress affected themselves (e.g., a lost fight) or others (e.g., witnessing the distress of others). The main dependent variable was the consolation of distressed parties by means of calming body contact. As in children, consolation was predicted by overall social competence and effective emotion regulation, as reflected in the speed of recovery from self-distress and behavioral measures of anxiety. Juveniles more effective at self-regulation were more likely to console others in distress, and such behavior was more typical of mother-reared juveniles than orphans. These results highlight the interplay between the development of social and emotional skills in our ape relatives and the importance of the mother-offspring bond in shaping socio-emotional competence.

Chimpanzees play the ultimatum game.

Is the sense of fairness uniquely human? Human reactions to reward division are often studied by means of the ultimatum game, in which both partners need to agree on a distribution for both to receive rewards. Humans typically offer generous portions of the reward to their partner, a tendency our close primate relatives have thus far failed to show in experiments. Here we tested chimpanzees (Pan troglodytes) and human children on a modified ultimatum game. One individual chose between two tokens that, with their partner's cooperation, could be exchanged for rewards. One token offered equal rewards to both players, whereas the other token favored the chooser. Both apes and children responded like humans typically do. If their partner's cooperation was required, they split the rewards equally. However, with passive partners--a situation akin to the so-called dictator game--they preferred the selfish option. Thus, humans and chimpanzees show similar preferences regarding reward division, suggesting a long evolutionary history to the human sense of fairness.

Research chimpanzees may get a break.

A recent report by the Institute of Medicine leaves few urgent reasons standing for the continued use of chimpanzees in biomedical research. It is high time to think about their retirement, Frans de Waal argues, without neglecting prospects for non-invasive research on behavior, cognition, and genetics.

Monkeys benefit from reciprocity without the cognitive burden.

The debate about the origins of human prosociality has focused on the presence or absence of similar tendencies in other species, and, recently, attention has turned to the underlying mechanisms. We investigated whether direct reciprocity could promote prosocial behavior in brown capuchin monkeys (Cebus apella). Twelve capuchins tested in pairs could choose between two tokens, with one being "prosocial" in that it rewarded both individuals (i.e., 1/1), and the other being "selfish" in that it rewarded the chooser only (i.e., 1/0). Each monkey's choices with a familiar partner from their own group was compared with choices when paired with a partner from a different group. Capuchins were spontaneously prosocial, selecting the prosocial option at the same rate regardless of whether they were paired with an in-group or out-group partner. This indicates that interaction outside of the experimental setting played no role. When the paradigm was changed, such that both partners alternated making choices, prosocial preference significantly increased, leading to mutualistic payoffs. As no contingency could be detected between an individual's choice and their partner's previous choice, and choices occurred in rapid succession, reciprocity seemed of a relatively vague nature akin to mutualism. Having the partner receive a better reward than the chooser (i.e., 1/2) during the alternating condition increased the payoffs of mutual prosociality, and prosocial choice increased accordingly. The outcome of several controls made it hard to explain these results on the basis of reward distribution or learned preferences, and rather suggested that joint action promotes prosociality, resulting in so-called attitudinal reciprocity.

Chimpanzees empathize with group mates and humans, but not with baboons or unfamiliar chimpanzees.

Human empathy can extend to strangers and even other species, but it is unknown whether non-humans are similarly broad in their empathic responses. We explored the breadth and flexibility of empathy in chimpanzees, a close relative of humans. We used contagious yawning to measure involuntary empathy and showed chimpanzees videos of familiar humans, unfamiliar humans and gelada baboons (an unfamiliar species). We tested whether each class of stimuli elicited contagion by comparing the effect of yawn and control videos. After including previous data on the response to ingroup and outgroup chimpanzees, we found that familiar and unfamiliar humans elicited contagion equal to that of ingroup chimpanzees. Gelada baboons did not elicit contagion, and the response to them was equal to that of outgroup chimpanzees. However, the chimpanzees watched the outgroup chimpanzee videos more than any other. The combination of high interest and low contagion may stem from hostility towards unfamiliar chimpanzees, which may interfere with an empathic response. Overall, chimpanzees showed flexibility in that they formed an empathic connection with a different species, including unknown members of that species. These results imply that human empathic flexibility is shared with related species.

Gambling primates: reactions to a modified Iowa Gambling Task in humans, chimpanzees and capuchin monkeys.

Humans will, at times, act against their own economic self-interest, for example, in gambling situations. To explore the evolutionary roots of this behavior, we modified a traditional human gambling task, the Iowa Gambling Task (IGT), for use with chimpanzees, capuchin monkeys and humans. We expanded the traditional task to include two additional payoff structures to fully elucidate the ways in which these primate species respond to differing reward distributions versus overall quantities of rewards, a component often missing in the existing literature. We found that while all three species respond as typical humans do in the standard IGT payoff structure, species and individual differences emerge in our new payoff structures. Specifically, when variance avoidance and reward maximization conflicted, roughly equivalent numbers of apes maximized their rewards and avoided variance, indicating that the traditional payoff structure of the IGT is insufficient to disentangle these competing strategies. Capuchin monkeys showed little consistency in their choices. To determine whether this was a true species difference or an effect of task presentation, we replicated the experiment but increased the intertrial interval. In this case, several capuchin monkeys followed a reward maximization strategy, while chimpanzees retained the same strategy they had used previously. This suggests that individual differences in strategies for interacting with variance and reward maximization are present in apes, but not in capuchin monkeys. The primate gambling task presented here is a useful methodology for disentangling strategies of variance avoidance and reward maximization.

Using cross correlations to investigate how chimpanzees (Pan troglodytes) use conspecific gaze cues to extract and exploit information in a foraging competition.

In a dyadic informed forager task, chimpanzees (Pan troglodytes) are known to exploit the knowledge of informed subordinates; however, the behavioral mechanisms they employ are unknown. It is tempting to interpret outcome measures, such as which individual obtained the food, in a cognitively richer way than the outcomes may justify. We employed a different approach from prior research, asking how chimpanzees compete by maneuvering around each other, whether they use gaze cues to acquire information from others, and what information they use in moment-to-moment decision-making. We used cross correlations, which plot the correlation between two variables as a function of time, systematically to examine chimpanzee interactions in a series of dyadic informed forager contests. We used cross correlations as a "proof of concept" so as to determine whether the target actions were contingent on, or occurred in a time-locked pattern relative to, the referent actions. A subordinate individual was given privileged knowledge of food location. As expected, an ignorant dominant followed the informed subordinate's movement in the enclosure. The dominant also followed the subordinate's gaze direction: after she looked at the subordinate, she was more likely to gaze toward this same direction within one second. In contrast, the subordinate only occasionally followed the dominant's movement and gaze. The dominant also changed her own direction of movement to converge on the location to which the subordinate directed her gaze and movement. Cross correlation proves an effective technique for charting contingencies in social interactions, an important step in understanding the use of cognition in natural situations.