Characterization of Pan social systems reveals in-group/out-group distinction and out-group tolerance in bonobos.

Human between-group interactions are highly variable, ranging from violent to tolerant and affiliative. Tolerance between groups is linked to our unique capacity for large-scale cooperation and cumulative culture, but its evolutionary origins are understudied. In chimpanzees, one of our closest living relatives, predominantly hostile between-group interactions impede cooperation and information flow across groups. In contrast, in our other closest living relative, the bonobo, tolerant between-group associations are observed. However, as these associations can be frequent and prolonged and involve social interactions that mirror those within groups, it is unclear whether these bonobos really do belong to separate groups. Alternatively, the bonobo grouping patterns may be homologous to observations from the large Ngogo chimpanzee community, where individuals form within-group neighborhoods despite sharing the same membership in the larger group. To characterize bonobo grouping patterns, we compare the social structure of the Kokolopori bonobos with the chimpanzee group of Ngogo. Using cluster analysis, we find temporally stable clusters only in bonobos. Despite the large spatial overlap and frequent interactions between the bonobo clusters, we identified significant association preference within but not between clusters and a unique space use of each cluster. Although bonobo associations are flexible (i.e., fission-fusion dynamics), cluster membership predicted the bonobo fission compositions and the spatial cohesion of individuals during encounters. These findings suggest the presence of a social system that combines clear in-group/out-group distinction and out-group tolerance in bonobos, offering a unique referential model for the evolution of tolerant between-group interactions in humans.

Selective and prolonged attention to emotional scenes in humans and bonobos.

Perceiving emotions in others is at the foundation of higher-order social cognition. The importance of emotions is evidenced by the fact that they receive prioritized attention at early stages of processing the environment in humans and some other primates. Nevertheless, we do not fully understand how emotion modulates attention over longer durations in primates, particularly in great apes. Bonobos, one of our closest relatives, stand out in emotion processing and regulation among great apes. This makes them an interesting comparison species and a valuable model for studying the evolution of emotion perception in hominids. We investigated how bonobos and humans spontaneously attend to emotionally valent scenes in a preferential looking task using eye-tracking. With Bayesian mixed modelling, we found that bonobos and humans generally looked longer at emotional scenes, mainly of conspecifics. Moreover, while bonobos did not have a bias toward emotional human scenes, humans sustained their attention toward bonobos playing, grooming and having sex. Furthermore, when exploring an immediate bias for emotions, humans showed a bias toward affiliative human scenes, and bonobos showed a bias away from bonobos-in-distress scenes. These findings suggest that emotions modulate attention at early and later attentional stages in bonobos, similar to humans.

The problem with two-event sequence learning by pigeons.

Bonobos appear to show little evidence of learning to make one response (R1) to an AB sequence and a different response (R2) to sequences BB, AA, and BA (Lind et al. PLoS ONE 18(9):e0290546, 2023), yet under different conditions, pigeons can learn this (Weisman et al. Exp Psychol Anim Behav Process 6(4):312, 1980). Aspects of the bonobo procedure may have contributed to this failure. Most important, no response was required in the presence of the stimuli to encourage attention to them. Furthermore, learning to make one response to the target sequence and another to the other sequences involves a bias that allows for better than chance responding. With the two-alternative forced-choice procedure used with the bonobos, the R1 response is correct for one sequence, whereas the R2 response is correct for three sequences. To correct for this, there are three times as many AB trials as each of the other sequences. However, this correction allows a bias to develop in which reinforcement often can be obtained by using only the last stimulus seen as the basis of choice (e.g., when the last stimulus is B respond R1 when the last stimulus is A respond R2). This solution yields reinforcement on five out of six, or 83%, of the trials. In the present experiment with pigeons, using this two-alternative forced choice procedure, most subjects tended to base their choice on the last-seen stimulus. This design allowed subjects to use a suboptimal but relatively effective choice strategy.

Understanding Language Evolution: Beyond Pan-Centrism.

Language does not fossilize but this does not mean that the language's evolutionary timeline is lost forever. Great apes provide a window back in time on our last prelinguistic ancestor's communication and cognition. Phylogeny and cladistics implicitly conjure Pan (chimpanzees, bonobos) as a superior (often the only) model for language evolution compared with earlier diverging lineages, Gorilla and Pongo (orangutans). Here, in reviewing the literature, it is shown that Pan do not surpass other great apes along genetic, cognitive, ecologic, or vocal traits that are putatively paramount for language onset and evolution. Instead, revived herein is the idea that only by abandoning single-species models and learning about the variation among great apes, there might be a chance to retrieve lost fragments of the evolutionary timeline of language.

Manipulative repertoire of bonobos (Pan paniscus) in spontaneous feeding situation.

Comparative behavioral studies of hand use amongst primate species, including humans, have been central in research on evolutionary mechanisms. In particular, the manipulative abilities of our closest relatives, the chimpanzee (Pan troglodytes), have been widely described in various contexts, showing a high level of dexterity both in zoo and in natural conditions. In contrast, the study of bonobos' manipulative abilities has almost exclusively been carried out in experimental contexts related to tool use. The objective of the present study is to describe the richness of the manipulative repertoire of zoo-housed bonobos, in a spontaneous feeding context including various physical substrates to gain a larger insight into our evolutionary past. Our study describes a great variety of grasping postures and grip associations in bonobos, close to the range of manipulative repertoire in chimpanzees, confirming that the two species are not markedly different in terms of cognitive and morphological constraints associated with food manipulation. We also observed differences in manipulative behaviors between juveniles and adults, indicating a greater diversity in grip associations and grasping postures used in isolation with age, and a sex-biased use of tools with females using tools more often than males. These results are consistent with the previous results in the Pan genus and reinforce the hypothesis that the evolutionary mechanisms underlying the flexibility of manipulative behaviors are shared by both species and that these ecological strategies would have already evolved in their common ancestor.

Lethal aggression in Pan is better explained by adaptive strategies than human impacts.

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.

Wild bonobo and chimpanzee females exhibit broadly similar patterns of behavioral maturation but some evidence for divergence.

OBJECTIVES: Primates exhibit variation in rates of growth and development. Variation in female growth and development across ape species appears to be explained by the Ecological Risk Aversion Hypothesis (ERAH). Indeed, existing data on variation in somatic growth and reproductive maturation between humans' closest living ape relatives, bonobos and chimpanzees, appear to be consistent with this hypothesis. However, existing data on behavioral maturation between the two species appear to contradict this hypothesis. We present novel behavioral data on infant and juvenile females from wild populations of both species in order to further evaluate predictions of the ERAH as it relates to the speed of behavioral maturation. MATERIALS AND METHODS: We analyzed 3 years of behavioral data on 17 female bonobos (<8 years of age) from LuiKotale, Democratic Republic of the Congo and 40 years of behavioral data on 30 age-matched female chimpanzees from Gombe, Tanzania. We compared the timing of (a) the attainment of independence from mothers and (b) the development of social skills using the following proxies: proximity between females and their mothers and the time that females spent engaged in eating, suckling, social play, social grooming, and riding on their mothers. RESULTS: We did not find species differences in the proportion of time that females spent in contact with their mothers or engaged in eating, suckling, social play, or social grooming. Female bonobos spent more time riding on their mothers than did female chimpanzees. Female bonobos spent more time at distances greater than 5 m from their mothers during the ages of 3-8 years, but females did not differ during the ages of 0-3 years. DISCUSSION: Behavioral maturation is largely similar between females of the two species based on the ages and proxies considered herein. We propose alternative explanations for the differences that we found in proximity and riding that do not invoke differences in underlying rates of maturation.

Investigating the Function of Mutual Grooming in Captive Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes).

Social grooming is often exchanged between individuals in many primate species. Rates of bidirectional (or simultaneous mutual) grooming vary across primate species, and its function is not yet fully understood. For example, mutual grooming is frequent in chimpanzees but rare in most primate species including wild bonobos. There are, however, no quantitative data available in captive bonobos. Therefore, through the direct comparison between captive bonobos and chimpanzees, this study aimed to (i) compare the frequency of mutual grooming between Pan species, (ii) explore and compare the function of mutual grooming, and (iii) discuss the rarity of this behavior in wild bonobo populations. We tested three hypotheses following the previous literature in wild chimpanzees. The social bonding hypothesis states that mutual grooming facilitates the maintenance of strong dyadic bonds. The immediate investment hypothesis states that it serves to signal willingness to invest in the interaction. The switching hypothesis states that mutual grooming serves no function but only occurs as an overlap to change the direction of unidirectional grooming. Our findings strongly supported the immediate investment hypothesis, but not the others. Grooming bouts that included mutual grooming were longer and more equitable than bouts without, illustrating that captive Pan species use mutual grooming to maximize their short-term benefits and increase the social value of their interaction. Captive bonobos performed mutual grooming in similar proportions and for similar functions as captive and wild chimpanzees do. This contrasts with wild bonobos who engage in this behavior only rarely. We suggest that the differences in patterns of mutual grooming between captive and wild bonobos might be explained by different degrees of kinship or by a potential intraspecies variation.

Visually attending to a video together facilitates great ape social closeness.

Humans create social closeness with one another through a variety of shared social activities in which they align their emotions or mental states towards an external stimulus such as dancing to music together, playing board games together or even engaging in minimal shared experiences such as watching a movie together. Although these specific behaviours would seem to be uniquely human, it is unclear whether the underlying psychology is unique to the species, or if other species might possess some form of this psychological mechanism as well. Here we show that great apes who have visually attended to a video together with a human (study 1) and a conspecific (study 2) subsequently approach that individual faster (study 1) or spend more time in their proximity (study 2) than when they had attended to something different. Our results suggest that one of the most basic mechanisms of human social bonding-feeling closer to those with whom we act or attend together-is present in both humans and great apes, and thus has deeper evolutionary roots than previously suspected.

Inter-group aggressive interaction patterns indicate male mate defense and female cooperation across bonobo groups at Wamba, Democratic Republic of the Congo.

OBJECTIVES: Although conflicts between groups over valuable resources are common in the animal kingdom, an individual's strategy toward out-group individuals may differ according to the benefits and costs received from inter-group interactions. Groups of bonobos encounter each other frequently and may mingle and range together from a few hours to a few days. During these inter-group associations, individuals across groups exhibit both aggressive and affiliative interactions. This study aimed to examine the strategies that bonobos employ with other groups, by comparing the patterns of within- and inter-group aggression. MATERIALS AND METHODS: We observed the aggressive interactions within a group of wild bonobos and between the group and three neighboring groups in Wamba, Luo Scientific Reserve, DR Congo. RESULTS: Bonobos increased the level of cooperation to attack out-group individuals more than they do to attack within-group individuals. Additionally, they reduced the aggression between within-group members during inter-group associations, compared to that when not associated with other groups. Males selectively and cooperatively attacked out-group males. Inter-group aggression among females was rare. Furthermore, females sometimes formed coalitions with out-group individuals to attack a common target. DISCUSSION: Our results support the hypothesis that inter-group competition occurs in bonobos, with males across groups competing over mates. Females across groups were tolerant and even cooperative with each other. Regardless of the ideal male strategy, female tolerant and cooperative relationships across groups and female within-group superiority over males could preserve tolerant inter-group relationships in bonobos.

Differences in novel food response between Pongo and Pan.

The diversity of great ape diets requires behavioral flexibility. Consequently, the exploration of potentially novel food sources is supposedly beneficial, but simultaneously, apes show high neophobia to prevent harmful and poisonous food intake. Social information, such as presence of group members or observations of non-naïve, experienced individuals have been demonstrated to affect the acceptance of novel food items in primates. Sociality may have evolutionary effects on the response of apes to novel foods. Here we assess the social information hypothesis, which predicts that selection favors higher neophobia in species where social information is abundant. We report the results from 134 great apes housed in multiple facilities from four closely related species that naturally differ in their degree of sociality: Pongo pygmaeus, Pongo abelii, Pan troglodytes and Pan paniscus. We examined individuals' reactions to novel foods when alone, which enabled us to detect any inherent differences and revealed significant distinctions between species. Chimpanzees and bonobos, that are naturally exposed to higher amounts of social information, were less likely to consume novel foods alone (showed higher neophobia) than the two more solitary orangutan species. Chimpanzees were especially cautious and showed higher explorative behaviors before tasting novel food than other species. Age influenced neophobia as younger individuals of all species took longer to taste novel foods than adults did.

Bonobos (Pan paniscus) show an attentional bias toward conspecifics' emotions.

In social animals, the fast detection of group members' emotional expressions promotes swift and adequate responses, which is crucial for the maintenance of social bonds and ultimately for group survival. The dot-probe task is a well-established paradigm in psychology, measuring emotional attention through reaction times. Humans tend to be biased toward emotional images, especially when the emotion is of a threatening nature. Bonobos have rich, social emotional lives and are known for their soft and friendly character. In the present study, we investigated (i) whether bonobos, similar to humans, have an attentional bias toward emotional scenes compared with conspecifics showing a neutral expression, and (ii) which emotional behaviors attract their attention the most. As predicted, results consistently showed that bonobos' attention was biased toward the location of the emotional versus neutral scene. Interestingly, their attention was grabbed most by images showing conspecifics such as sexual behavior, yawning, or grooming, and not as much-as is often observed in humans-by signs of distress or aggression. The results suggest that protective and affiliative behaviors are pivotal in bonobo society and therefore attract immediate attention in this species.

Bonobos voluntarily hand food to others but not toys or tools.

A key feature of human prosociality is direct transfers, the most active form of sharing in which donors voluntarily hand over resources in their possession Direct transfers buffer hunter-gatherers against foraging shortfalls. The emergence and elaboration of this behaviour thus likely played a key role in human evolution by promoting cooperative interdependence and ensuring that humans' growing energetic needs (e.g. for increasing brain size) were more reliably met. According to the strong prosociality hypothesis, among great apes only humans exhibit sufficiently strong prosocial motivations to directly transfer food. The versatile prosociality hypothesis suggests instead that while other apes may make transfers in constrained settings, only humans share flexibly across food and non-food contexts. In controlled experiments, chimpanzees typically transfer objects but not food, supporting both hypotheses. In this paper, we show in two experiments that bonobos directly transfer food but not non-food items. These findings show that, in some contexts, bonobos exhibit a human-like motivation for direct food transfer. However, humans share across a far wider range of contexts, lending support to the versatile prosociality hypothesis. Our species' unusual prosocial flexibility is likely built on a prosocial foundation we share through common descent with the other apes.

Is Overimitation a Uniquely Human Phenomenon? Insights From Human Children as Compared to Bonobos.

Imitation is a key mechanism of human culture and underlies many of the intricacies of human social life, including rituals and social norms. Compared to other animals, humans appear to be special in their readiness to copy novel actions as well as those that are visibly causally irrelevant. This study directly compared the imitative behavior of human children to that of bonobos, our understudied great ape relatives. During an action-copying task involving visibly causally irrelevant actions, only 3- to 5-year-old children (N = 77) readily copied, whereas no bonobo from a large sample did (N = 46). These results highlight the distinctive nature of the human cultural capacity and contribute important insights into the development and evolution of human cultural behaviors.

Prevalence and characteristics of hair plucking in captive bonobos (Pan paniscus) in North American zoos.

When primates exhibit hair loss and are observed to engage in self or social hair plucking (a rapid jerking away of the hair shaft and follicle by the hand or mouth, often accompanied by inspection, and consumption) the altered appearance, and behavior patterns are thought to reflect individual physiological, and psychological well-being. Hair loss and hair plucking occur in many captive primate species, including all of the great apes. We present the first survey of this behavior among captive bonobos (N = 88; 50 females and 38 males) in seven zoos in the United States. We found that 43% of the population engaged in this behavior pattern and discounting youngsters (who are not observed to hair pluck until the age of five), 58% of individuals hair plucked. Of the individuals who hair plucked, 97% engaged in social plucking, whereas 46% engaged in self-directed plucking. We regressed the occurrence of hair plucking with multiple predictor variables using binary logistic regression and multimodel inference to determine which predictors best explained the prevalence of self-directed and social plucking. We also analyzed publicly available data on hair plucking in captive chimpanzees. We found that the occurrence of another abnormal behavior, age, origin, and pelage condition best explained self-directed plucking in bonobos. Social plucking was explained by age, origin, pelage, and sex. Our analysis of chimpanzee hair plucking revealed that plucking is strongly influenced by rearing and sex. This study demonstrates that hair plucking is more prevalent in captive bonobos compared to captive chimpanzees and gorillas, however, the covariates associated with hair plucking for each species are different. Our data suggest a potential link between self-directed plucking and well-being. However, the higher prevalence and etiology of social hair plucking is more difficult to explain.

Laterality of Grooming and Tool Use in a Group of Captive Bonobos (Pan paniscus).

Humans exhibit population level handedness for the right hand; however, the evolution of this behavioral phenotype is poorly understood. Here, we compared the laterality of a simple task (grooming) and a complex task (tool use) to investigate whether increasing task difficulty elicited individual hand preference among a group of captive bonobos (Pan paniscus). Subjects were 17 bonobos housed at the Columbus Zoo and Aquarium. Laterality of grooming was recorded using group scans; tool use was recorded using all-occurrence sampling. Grooming was characterized as unimanual or bimanual, and both tasks were scored as right-handed or left-handed. Most individuals did not exhibit significant hand preference for unimanual or bimanual (asymmetrical hand use) grooming, although 1 individual was lateralized for each. For the 8 subjects who engaged in termite fishing enough for statistical testing, 7 individuals exhibited significant laterality and strong individual hand preference. Four subjects preferred their left hand, 3 preferred their right, and 1 had no preference. Grooming, a simple behavior, was not lateralized in this group, yet a more complex behavior revealed a strong individual hand preference, and these results are congruent with other recent findings that demonstrate complex tasks elicit hand preference in bonobos.

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.

Hair plucking, stress, and urinary cortisol among captive bonobos (Pan paniscus).

Hair plucking has been observed in many captive primate species, including the great apes; however, the etiology of this behavioral pattern is poorly understood. While this behavior has not been reported in wild apes, an ethologically identical behavior in humans, known as trichotillomania, is linked to chronic psychosocial stress and is a predominantly female disorder. This study examines hair plucking (defined here as a rapid jerking away of the hair shaft and follicle by the hand or mouth, often accompanied by inspection and consumption of the hair shaft and follicle) in a captive group of bonobos (N = 13) at the Columbus Zoo and Aquarium in Columbus, Ohio. Plucking data were collected using behavior and all-occurrence sampling; 1,450 social and self-directed grooming bouts were recorded during 128 hr of observation. Twenty-one percent of all grooming bouts involved at least one instance of plucking. Urine samples (N = 55) were collected and analyzed for the stress hormone cortisol. Analyses of urinary cortisol levels showed a significant positive correlation between mean cortisol and self-directed plucking for females (r = 0.88, P < 0.05) but not for males (r = -0.73, P = 0.09). These results demonstrate an association between relative self-directed hair plucking and cortisol among female bonobos. This is the first study to investigate the relationship between hair plucking and cortisol among apes. Overall, these data add to our knowledge of a contemporary issue in captive ape management. Zoo Biol. 35:415-422, 2016. © Wiley Periodicals, Inc.

Personality in Bonobos.

To better understand human and chimpanzee personality evolution, we obtained trait ratings of personality for 154 captive bonobos (~80% of the U.S. and European population). We found factors that we labeled Assertiveness, Conscientiousness, Openness, Agreeableness, Attentiveness, and Extraversion. The interrater reliabilities and test-retest reliabilities for these factors were comparable to those found in humans and other species. Using orthogonal targeted Procrustes rotations, we compared the bonobo dimensions with those of three samples of captive chimpanzees. Overall congruence coefficients indicated a fair degree of similarity; at the factor level, there was good evidence for Assertiveness, Conscientiousness, Openness, and Agreeableness in the chimpanzee samples; evidence for Attentiveness and Extraversion was poor. These findings suggest that, as expected given their close phylogenetic relationship, bonobo personality structure resembles chimpanzee personality structure in some respects. However, divergent evolution, perhaps as a result of socioecological differences between bonobos and chimpanzees, also appears to have shaped personality structure in these species.