From the Cover: 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.Socio-emotional competence encompasses an array of skills, such as successfully forming and maintaining social relationships, behaving appropriately in social situations, being sensitive to the emotions of others, and effectively managing one’s own emotions (1). Emotion regulation (ER) is an essential part of socio-emotional competence and is defined as the process of modifying, inhibiting, evaluating, and monitoring internal states and reactions to enable an individual to adaptively respond to arousing situations so as to achieve individual goals (1, 2). Throughout development, social and emotional skills are tightly interconnected and “people who are unable to modulate the intensity and duration of their internal emotional responses and emotionally driven behavior are likely to be physiologically over-aroused and to behave in ways that do not foster constructive social interactions” (3).Studies of child development show that effectively managing one’s own emotions allows for greater empathy with others, including caring responses known as sympathetic concern (4–6). Sympathetic concern interacts with other social skills that emerge across development, including perspective-taking (5–9). It is reliably predicted by ER, with low-regulating individuals more likely to become emotionally overwhelmed when exposed to another’s distress, resulting in a more self-centered personal distress (6, 8, 9). This connection develops at an early age: infants with signs of better ER show less personal distress in response to peer cries than those with poorer ER (10). Overall, socially competent behavior, which includes expressions of sympathy and prosocial behavior, as well as socially appropriate responses and popularity, reliably relates to better ER in children and adults (1–3, 7–11).This socio-emotional framework is rarely applied to other species, however. This is curious, because if it is critically important for humans one would expect it to also apply to some degree to our closest relatives, the anthropoid apes. To explore this issue, we measured purported markers of socio-emotional competence in young bonobos along with consolation behavior, which previous research has suggested to be a marker of sympathetic concern (12–14). Consolation is defined as spontaneous contact comfort aimed at distressed parties by means of touching, stroking, embracing, and kissing (15) (Fig. 1), a behavior well-known of both children and apes (4–6, 12–16). In human children, consolation behavior appears already in the first year of life (10, 17), suggesting that although the cognitive component of empathy increases across development, it is no prerequisite for expressions of concern. ER seems to be critical: infants without effective ER do not orient to others because they cannot overcome their own personal distress in the face of another’s distress (10, 18).Open in a separate windowFig. 1.One juvenile bonobo embraces a distressed companion during postconflict consolation. Photograph by Zanna Clay at the Lola ya Bonobo Sanctuary in the Democratic Republic of the Congo.Whereas few animal studies have explicitly addressed ER, experimental research has revealed relevant similarities. For example, primates and other animals show human-like skin conductance and heart rate responses to emotionally arousing or calming stimuli (19–23). Chimpanzees (Pan troglodytes) spontaneously match images of positive vs. negative facial expressions to videos depicting pleasant vs. aversive situations, suggesting awareness of the emotional connotations of their species’ facial displays (19). Studies addressing emotional control typically adopt a deferred gratification paradigm. Apes, and to a lesser extent monkeys and nonprimates (24–26), are able to control the urge to reach for a reward if holding back increases the chance of a better reward later on. Moreover, like children, apes seek to distract themselves in an apparent attempt to control the temptation of immediate gratification (26). Such research suggests the importance of ER for ape behavior.An area with significant overlap in human and nonhuman developmental research is that of social deprivation. Socially deprived children demonstrate poor emotional and social competence, including lower sympathetic concern, increased risk for psychiatric disorders, and enlarged amygdala volumes, indicative of high anxiety (27–30). Although adoptive care can mitigate these negative effects, orphaned children typically show lasting socio-emotional disruptions (30). Similar effects of early deprivation have been documented in chimpanzees, rhesus monkeys (Macaca mulatta), and other primates, including increased anxiety, an inability to develop social relationships, lack of recognition of social signals, and stereotypical behaviors (31–36). A study of socially deprived monkeys found a deficiency in species-typical reconciliation with opponents after conflict, which is an essential social skill (34, 36). Although some negative effects of social deprivation can be overcome, this mostly applies to deprivation later in development, such as after weaning, or after having received substitutive maternal care (37, 38).Bonobos at a forested African sanctuary offered an opportunity to measure many of these variables in both mother-raised and orphaned juveniles, thus allowing a test of predictions derived from the above studies. Most study subjects were wild-caught orphans rescued from the illegal bush-meat and pet trades and subsequently rehabilitated with the help of human mother substitutes. The bonobo is a species of particular interest given its close genetic similarity to our own (39) and its reputation of social tolerance, peacefulness, and reduced levels of violence compared with its congener, the chimpanzee (40). Bonobos also seem to have high empathy levels (41) and are equipped with the neural substrate to support these tendencies (42). Consistent with empathy-based predictions (43), our previous study found consolation to be typical of closely bonded individuals, both kin and nonkin. Both reconciliation between former opponents and consolation of distressed parties occurred across all age classes, highlighting successful social rehabilitation within the sanctuary environment. Nevertheless, mother-reared juveniles were significantly more likely to offer consolation to others than orphans of any age (44).A year after our first study, we observed the same bonobo juveniles in greater detail to investigate the interplay between socio-emotional competence at baseline while experiencing self-distress (i.e., as a victim of a fight), and in response to the distress of others (i.e., as a bystander to conflict). Our main dependent variable was spontaneously offered consolation after naturally occurring aggressive and/or stressful episodes. We predicted that juvenile bonobos scoring higher on measures of overall sociality and socio-emotional competence, including ER, would be more likely to console distressed parties. We evaluated these effects using a generalized linear mixed model (GLMM), which helps determine independent contributions, controlled for age, sex, and other factors.