Social Attention in the Two Species of Pan: Bonobos Make More Eye Contact than Chimpanzees

RESEARCH ARTICLE Social Attention in the Two Species of Pan: Bonobos Make More Eye Contact than Chimpanzees Fumihiro Kano2,3,4¤*, Satoshi Hirata1, Josep Call3,5 1 Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, Kumamoto, Uki, Japan, 2 Primate Research Institute, Kyoto University, Inuyama, Japan, 3 Department of Developmental and Comparative Psychology, Max-Planck Institute for Evolutionary Anthropology, Leipzig, Germany, 4 Japan Society for Promotion of Science, Tokyo, Japan, 5 School of Psychology and Neuroscience, University of St Andrews, St Andrews, United Kingdom ¤ Current address: Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, Kumamoto, Uki, Otao 990, Japan * OPEN ACCESS Citation: Kano F, Hirata S, Call J (2015) Social Attention in the Two Species of Pan: Bonobos Make More Eye Contact than Chimpanzees. PLoS ONE 10 (6): e0129684. doi:10.1371/journal.pone.0129684 Academic Editor: Roscoe Stanyon, University of Florence, ITALY Received: January 11, 2015 Accepted: May 12, 2015 Published: June 15, 2015 Copyright: © 2015 Kano et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This study was conducted in part under FK’s post-doc program; the Japan Society for Promotion of Science (JSPS) for study abroad. FK and SH respectively received JSPS KAKENHI Grant Number 26885040 and 26245069 URL:http://www. jsps.go.jp/english/. This study was in part funded by JSPS KAKENHI Grant Number 26885040 and 26245069, MEXT KAKENHI Grant Number 24000001, JSPS-LGP-U04, JSPS core-to-core type A CCSN, and MEXT-PRI-Human Evolution. The funders had no role in study design, data collection Abstract Humans’ two closest primate living relatives, bonobos and chimpanzees, differ behaviorally, cognitively, and emotionally in several ways despite their general similarities. While bonobos show more affiliative behaviors towards conspecifics, chimpanzees display more overt and severe aggression against conspecifics. From a cognitive standpoint, bonobos perform better in social coordination, gaze-following and food-related cooperation, while chimpanzees excel in tasks requiring extractive foraging skills. We hypothesized that attention and motivation play an important role in shaping the species differences in behavior, cognition, and emotion. Thus, we predicted that bonobos would pay more attention to the other individuals’ face and eyes, as those are related to social affiliation and social coordination, while chimpanzees would pay more attention to the action target objects, as they are related to foraging. Using eye-tracking we examined the bonobos’ and chimpanzees’ spontaneous scanning of pictures that included eyes, mouth, face, genitals, and action target objects of conspecifics. Although bonobos and chimpanzees viewed those elements overall similarly, bonobos viewed the face and eyes longer than chimpanzees, whereas chimpanzees viewed the other elements, the mouth, action target objects and genitals, longer than bonobos. In a discriminant analysis, the individual variation in viewing patterns robustly predicted the species of individuals, thus clearly demonstrating species-specific viewing patterns. We suggest that such attentional and motivational differences between bonobos and chimpanzees could have partly contributed to shaping the species-specific behaviors, cognition, and emotion of these species, even in a relatively short period of evolutionary time. PLOS ONE | DOI:10.1371/journal.pone.0129684 June 15, 2015 1 / 14 Eye Contact in Bonobos and Chimpanzees and analysis, decision to publish, or preparation of the manuscript Competing Interests: The authors have declared that no competing interests exist. Introduction Despite their general similarities and close phylogenetic relationship, bonobos and chimpanzees show some important differences, particularly in their patterns of aggression and affiliation. While chimpanzees often engage in aggressive displays and severe aggression which occasionally involves the killing of conspecifics, bonobos rarely exhibit such overt aggressive behaviors [1–3]. Moreover, bonobos exhibit a larger repertoire of affiliative behaviors towards conspecifics compared to chimpanzees including non-conceptive sexual behaviors, frequent play among adults, and non-aggressive encounters with strangers [1, 4–6]. It has been hypothesized that bonobo behavior has evolved in part as a response to the relaxation of intra-group competition and selection against male aggression [1, 3]. In humans, eye contact is related to the level of affiliation among individuals, and thus it reflects an individual’s temperament and the interpersonal relationships [7, 8]. People facing each other tend to reach an equilibrium in both physical distance and eye contact that depends on their affiliative motivation and the approach-avoidance conflict; people with a more relaxed relationship with their partners and with a higher need for affiliation show a closer physical distance and an increased level of eye contact. The level of eye contact is also modulated by social parameters such as cultural background and clinical condition [8–10]. If eye contact is modulated by the same principles in bonobos and chimpanzees as in humans, it is predicted that bonobos, the species with an increased affiliative motivation, would make more eye contact than chimpanzees. Non-human primates have much in common with humans in terms of the pattern and function of eye contact [11]. From an early age, humans and chimpanzees preferentially orient to faces looking at vs. looking away from observers [12, 13]. Visual search experiments have shown that humans and chimpanzees are able to detect such direct gaze faster than averted gaze [14, 15]. Eye-tracking experiments have shown that humans and several species of nonhuman primates predominantly fixate eyes among facial features [16–21]. Observational studies have found that, although prolonged eye contact is not commonly observed among adults in nonhuman primates as it serves as a threat to the conspecifics [11], eye contact plays an important role in affiliative contexts. Mothers and infants in macaques and chimpanzees exchange frequent eye contact and facial expressions [22, 23]. When chimpanzees and gorillas make an attempt to reconcile with conspecifics after fighting, they first establish eye contact before approaching their counterparts [24, 25]. Only few studies examined the individual and species variation of eye contact in nonhuman primates. One study examined the eye-contact frequency of six monkey species in response to an experimenter approaching the subjects [26]. Rhesus macaques exhibited the lowest frequencies of e (...truncated)