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Bonobos (Pan Paniscus) Show an Attentional Bias Toward Conspecifics’ Emotions

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Bonobos (Pan Paniscus) Show an Attentional Bias Toward Conspecifics’ Emotions Bonobos (Pan paniscus) show an attentional bias toward conspecifics’ emotions Mariska E. Kreta,1, Linda Jaasmab, Thomas Biondac, and Jasper G. Wijnend aInstitute of Psychology, Cognitive Psychology Unit, Leiden University, 2333 AK Leiden, The Netherlands; bLeiden Institute for Brain and Cognition, 2300 RC Leiden, The Netherlands; cApenheul Primate Park, 7313 HK Apeldoorn, The Netherlands; and dPsychology Department, University of Amsterdam, 1018 XA Amsterdam, The Netherlands Edited by Susan T. Fiske, Princeton University, Princeton, NJ, and approved February 2, 2016 (received for review November 8, 2015) In social animals, the fast detection of group members’ emotional perspective, it is most adaptive to be able to quickly attend to rel- expressions promotes swift and adequate responses, which is cru- evant stimuli, whether those are threats in the environment or an cial for the maintenance of social bonds and ultimately for group affiliative signal from an individual who could provide support and survival. The dot-probe task is a well-established paradigm in psy- care (24, 25). chology, measuring emotional attention through reaction times. Most primates spend their lives in social groups. To prevent Humans tend to be biased toward emotional images, especially conflicts, they keep close track of others’ behaviors, emotions, and when the emotion is of a threatening nature. Bonobos have rich, social debts. For example, chimpanzees remember who groomed social emotional lives and are known for their soft and friendly char- whom for long periods of time (26). In the chimpanzee, but also in acter. In the present study, we investigated (i) whether bonobos, the rarely studied bonobo, grooming is a major social activity and similar to humans, have an attentional bias toward emotional scenes a means by which animals living in proximity may bond and re- ii compared with conspecifics showing a neutral expression, and ( ) inforce social structures. It is also used as a form of reconciliation which emotional behaviors attract their attention the most. As pre- and a means of conflict resolution. Despite their general similar- ’ dicted, results consistently showed that bonobos attention was bi- ities and close phylogenetic relationship, bonobos, chimpanzees, ased toward the location of the emotional versus neutral scene. and humans show clear differences in their social behavior. Al- Interestingly, their attention was grabbed most by images showing though chimpanzee and human societies are dominated by males conspecifics such as sexual behavior, yawning, or grooming, and not and encounters between different groups frequently result in vi- as much—as is often observed in humans—by signs of distress or olence and sometimes the killing of conspecifics (27–29), bonobo aggression. The results suggest that protective and affiliative behav- society is controlled by females and aggression is usually prevented iors are pivotal in bonobo society and therefore attract immediate – attention in this species. through nonconceptive sexual behavior, grooming, and play (30 33). Compared with chimpanzees, bonobos live in more predict- bonobo | ape | affect | empathy | attention able environments with low seasonality and stable food availabil- ity, which is why they have a lower degree of fission-fusion and which, next to the peace-keeping role of the females, may also fficiently responding to others’ emotions has great survival explain the lower rates of competition (31). value, especially for social species, such as primates, who es- E Bonobos have rich personalities and share most of their traits tablish close, long-term bonds with group members (1–3). Previous with humans and chimpanzees, suggesting these were also pre- research in humans has shown that one component of this strong sent in their common ancestor (34). From early age on, bonobos sensitivity to others’ emotions is heightened attention to their af- fective states (4–6). Together with the chimpanzee, the bonobo is the closest living relative of humans. Studying components of their Significance emotional behavior, such as emotional attention, may help us not only to understand this rarely studied species better, but also Applying well-established psychological paradigms to our provide insight into (human) emotions and their evolutionary past closest relatives represents a promising approach for providing (7–9). In the present study, we investigated whether bonobos, like insight into similarities and differences between humans and humans, show increased attention to scenes depicting conspe- apes. Numerous articles have been published on the dot-probe cifics showing an emotion or are involved in emotion regulatory task, showing that humans have an attentional bias toward behaviors, compared with scenes where conspecifics are in a emotions, especially when threatening. For social species like ’ neutral state. primates, efficiently responding to others emotions has great In natural environments, attention is preferentially sustained survival value. Observational research has shown that, com- pared with humans and chimpanzees, bonobos excel in reg- by stimuli that have affective significance, in contrast to routine, ’ emotionally neutral events (6, 10). This attentional bias reflects a ulating their own and others emotions, thereby preventing conflicts from escalating. The present study is an initial effort to functional mechanism where fast and automatic attention allo- apply a psychological test to the bonobo, and demonstrates that cation to emotional information can aid humans in threatening they, like humans, have heightened attention to emotional— situations by fostering fast actions (11, 12). Experimentally, this compared with neutral—conspecifics, but are mostly drawn has, for example, been demonstrated with the dot-probe task. toward protective and affiliative emotions. Previous dot-probe studies have shown that emotional signals in- duce a bias in spatial attention, in that participants respond faster COGNITIVE SCIENCES Author contributions: M.E.K., T.B., and J.G.W. designed research; L.J. performed research; PSYCHOLOGICAL AND to a presented dot (the target, henceforth, “probe”)whenitap- M.E.K. and L.J. analyzed data; M.E.K. wrote the paper; T.B. facilitated the research in the pears at the location of a previously presented emotion compared park; and J.G.W. programmed the task. with neutral stimulus (13–17). Although in humans a bias toward The authors declare no conflict of interest. threatening compared with neutral stimuli is most commonly ob- This article is a PNAS Direct Submission. served, some studies also report increased attention toward posi- Freely available online through the PNAS open access option. tive versus neutral stimuli (18–21). Other research has shown that 1To whom correspondence should be addressed. Email: [email protected]. there are marked individual differences in biases and that these This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. are, for example, modulated by mood (22, 23). From an evolutionary 1073/pnas.1522060113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1522060113 PNAS | April 5, 2016 | vol. 113 | no. 14 | 3761–3766 Downloaded by guest on September 25, 2021 are sensitive to others’ emotions, which is demonstrated by their Results ability to provide appropriate consolatory behaviors after con- Reaction Times. Data were analyzed in a generalized mixed multi- flicts (35), a skill individuals with more effective self-regulation level model with picture category [emotional bonobo, neutral capabilities excel in particularly (35), but which is also demon- bonobo, or control animal (coded as 1, 0, and −1)] as fixed factor strated by more automatic behavior, including yawn contagion, and random intercepts for each individual and individual-by- an index of empathy (36, 37). session. The multilevel structure was defined by the different Bonobos’ personality characteristics and complex social emo- trials, nested within sessions, nested within individuals. As the tional behavior have rarely been studied experimentally, but reaction time data were skewed, a γ-probability distribution was the conclusions that can be drawn from the few studies avail- selected with a log-link function (Methods). able are in line with the conclusions from observational re- As predicted, a main effect of picture category [F(2, 1.171) = search, described above. It has for example been demonstrated 5.135, P = 0.006] showed that bonobos were faster in tapping on that great apes, bonobos included, can reliably recognize human the probe that replaced a picture of an emotional bonobo (mean emotions (38) and experiments with chimpanzees show that reaction time = 611.240, SE = 78.819) compared with a neutral they are also sensitive to the emotions of conspecifics (39–42). bonobo [mean reaction time = 645.927, SE = 83.176, t(1.171) = By using an experimental cofeeding set-up, it has been shown 2.669, P = 0.008] (Fig. 2A and Table S2) (details on all the sta- that bonobos are more tolerant than chimpanzees (43; but see tistical tests described in the main text are provided in tables in the ref. 44). In addition, an eye-tracking study demonstrated that SI Results). This pattern was visible in all subjects (Fig. 2B). bonobos make more eye contact than chimpanzees (45). Finally, Although luminance or contrast could not explain the differ- in a risky decision game, bonobos showed more risk-aversion ences in reaction times following the emotional
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