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Published in final edited form as: J Comp Psychol. 2020 Aug;134(3):318–322. doi: 10.1037/com0000247

Differences in the Mutual Eye Gaze of Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

Michele M Mulholland 1, Mary Catherine Mareno 2, Lisa A Reamer 3, Lindsay M Mahovetz 4, Steven J Schapiro 5, William D Hopkins 6
PMCID: PMC7780221  NIHMSID: NIHMS1653267  PMID: 32804530

Abstract

Eye gaze is widespread in nonhuman primate taxa and important for social cognition and communicative signaling. Bonobos and chimpanzees, two closely related primate species, differ in social organization, behavior, and cognition. Chimpanzees’ eye gaze and gaze following has been studied extensively, whereas less is known about bonobos’ eye gaze. To examine species differences using a more ecologically relevant measure than videos or pictures, the current study compared bonobo and chimpanzee mutual eye gaze with a human observer. A multivariate analysis of variance revealed significant species differences in frequency and total duration, but not bout length, of mutual eye gaze (p < .001). Specifically, bonobos engage in mutual eye gaze more frequently and for longer total duration than chimpanzees. These results are likely related to species differences in social behavior and temperament and are consistent with eye-tracking studies in which bonobos looked at the eye region of conspecifics (in pictures and videos) longer than chimpanzees. Future research should examine the relationship between mutual eye gaze and gaze following, as well as examine its genetic and neurological correlates.

Keywords: social cognition, social attention, eye gaze, chimpanzee, bonobo

Chimpanzees (Pan troglodytes) and bonobos (Pan partisans) are closely related species with distinct differences in social organization, behavior, and cognition (De Waal, 1989, 1995; Hare & Yamamoto, 2017; Herrmann, Hare, Call, & Tomasello, 2010; Rilling et al., 2012; Stanford, 1998; White & Chapman, 1994; Wobber, Wrangham, & Hare, 2010). Although both species live in fission-fusion societies, there are differences in social behavior, dominance hierarchy, mating systems and sexual behavior, hunting or foraging party size, and tool use (see reviews in Hare & Yamamoto, 2017; White & Chapman, 1994). In terms of social behavior, chimpanzees have been described as more territorial and less tolerant than bonobos. Despite these well-documented differences, we know very little about how these species differ in mutual eye gaze.

Mutual eye gaze (direct eye-to-eye contact with another individual) and gaze following (following the direction of another individual’s gaze) are important for primate social cognition and communicative signaling and are widespread in human and non-human primate taxa (see reviews in Emery, 2000; Grossmann, 2017; Shepherd, 2010). This suggests that eye gaze behaviors were highly conserved across primate evolution and potentially related to the development of complex social and cognitive functions (e.g., understanding social hierarchies, observational learning, and perspective taking; Emery, 2000; Rosati & Hare, 2009). Further studies are needed to understand phylogenetic variation in mutual eye gaze, particularly within the Pan genus. Chimpanzees and bonobos are the closest living relatives to humans, and understanding both the differences and similarities in chimpanzee and bonobo cognition, including eye gaze, is crucial for making inferences about the evolution of human cognition (Emery, 2000; Hare & Yamamoto, 2017).

Many earlier studies assumed that chimpanzees lacked mutual eye gaze, particularly during positive social interactions. However, Bard et al. (2005) revealed that chimpanzee mother-infant dyads engaged in frequent mutual eye gaze and that this behavior was inversely related to the time spent cradling. In addition, they found that mutual eye gaze differed significantly between research facilities (those from a Japanese institution engaged in more mutual eye contact with their infants than those from a U.S. institution). A more recent study found that early social experiences may influence mutual eye gaze with a human observer. Nursery-reared chimpanzees engaged in longer eye contact with humans compared with both captive mother-reared and wild-born chimpanzees (Hopkins, Mulholland, Reamer, Mareno, & Schapiro, 2020), indicating that early exposure to increased human eye gaze in the nursery setting may facilitate later adult eye gaze. In regard to gaze following, researchers found that, during food competition, captive chimpanzees use the eye gaze of conspecifics to determine which food sources can and cannot be seen by others (Bräuer, Call, & Tomasello, 2007; Hare, Call, Agnetta, & Tomasello, 2000). Despite attentional preferences for conspecific faces over human faces (Hattori, Kano, & Tomonaga, 2010), several studies show captive chimpanzees also reliably follow the gaze of humans early in life (though the exact age this begins is debated) with improvements occurring across the juvenile period (Bräuer, Call, & Tomasello, 2005; Okamoto et al., 2002; Tomasello, Call, & Hare, 1998; Tomasello, Hare, & Fogleman 2001). Chimpanzees also use human gaze, similar to conspecific gaze, to infer the target of attention in both computerized and live object search tasks (Itakura, Agnetta, Hare, & Tomasello, 1999; MacLean & Hare, 2012; Tomonaga & Imura, 2010).

Compared with chimpanzees, limited research exists on eye gaze in bonobos. Two eye-tracking studies have found that bonobos spend significantly more time examining the eye region in videos and pictures of conspecifics compared with chimpanzees (Kano, Hirata, & Call, 2015; Kano, Shepherd, Hirata, & Call, 2018). Comparing mutual eye gaze with either conspecifics or a familiar human experimenter would be a more ecologically valid way to examine the species differences revealed by eye-tracking studies using videos or pictures. No such studies have been conducted; however, researchers have compared chimpanzees and bonobos following human gaze with conflicting results. Bräuer et al. (2005) found no difference in the frequency of following an experimenter’s gaze (i.e., when looking at the ceiling) between the two species. In contrast, bonobos outperformed chimpanzees in gaze following and understanding an actor’s intentions (Herrmann et al., 2010; Hopkins, Stimpson, & Sherwood, 2018), whereas chimpanzees were more consistently able to infer the target of a human’s gaze in a perspective-taking task (i.e., knowing if an object was novel to a human experimenter; MacLean & Hare, 2012). To better understand these conflicting species differences in following humans’ gaze, it would be useful to know first how these two species differ in their engagement in mutual eye gaze with a human. No study to date has directly compared mutual eye gaze with live humans. To further examine eye gaze comparatively, we measured the frequency, duration, and bout length of mutual eye gaze with a familiar human experimenter in both chimpanzees and bonobos. Based on eye-tracking studies by Kano et al, (2015, 2018), we predicted that bonobos would engage in mutual eye gaze with a human more frequently and for longer duration than chimpanzees.

Method

Subjects

The subjects included captive juvenile and adult chimpanzees (N = 125; 80 females, 45 males) and bonobos (N = 24; 15 females, nine males). The chimpanzees were from the National Center for Chimpanzee Care at The University of Texas MD Anderson Cancer Center (n = 93) or the Yerkes National Primate Research Center (YNPRC; n = 32). The bonobos were from the Milwaukee County Zoo (n = 16) or the Jacksonville Zoo and Gardens (n = 8). Because variation in rearing environment can lead to differences in chimpanzees’ mutual eye gaze with humans (Hopkins et al., 2020; Thomsen, 1974), all subjects included in the current study were mother-reared in their conspecific family groups. At the time of testing, all apes were living in groups ranging from two to 10 individuals. The National Center for Chimpanzee Care and YNPRC housed the chimpanzees in indoor/outdoor enclosures, with 24-hr access to both areas except during cleaning. The bonobos at the Milwaukee County Zoo had indoor/outdoor access during the day and indoor-only access during the night. The Jacksonville Zoo and Gardens was undergoing construction during data collection; therefore, each social group had outdoor access on a rotating basis. All enclosures included climbing structures, bedding, and daily environmental enrichment. Care staff fed the apes a diet of commercial primate chow and fresh produce multiple times per day and provided them with several daily foraging opportunities and ad libitum access to water. Access to food was never restricted during the course of the study. All work was carried out in accordance with the care and use of animal guidelines as laid out by the National Institutes of Health in the United States and was approved by each facility’s respective Institutional Animal Care and Use Committee.

Procedure

Mutual eye gaze of each subject was assessed in four 1-min trials by familiar researchers (0.2–8 years of experience with the apes; see online supplemental materials). All subjects were tested in their social groups, and no attempt was made to separate or isolate individuals. To begin, the researcher sat or stood ~2 feet from the cage mesh (close enough to feel confident knowing when they achieved direct eye contact but not within touching distance of the subject). The researcher determined whether to sit or stand based on the position of the subject and chose the posture that would place the researcher at eye level with the subject. The 1-min trial began when the subject was sitting or standing with attention and gaze directed toward the researcher, and the researcher successfully made direct eye contact with the subject. Throughout the trial the researcher actively tried to gain or maintain eye contact with the subject by calling the subject’s name or making an attention-getting sound to regain its attention. During each trial, all scoring was done live; the researcher recorded the frequency and total duration of eye contact using a stopwatch. Though rare, we excluded any trials in which the subject left the immediate area before the end of the trial or if an event (i.e., fighting in the group, interruption by other personnel) diverted the subject’s attention. The researcher repeated this procedure four times per subject (on different days). Following all four trials, we calculated the average mutual eye gaze frequency (number of times mutual eye gaze occurred within 1 min), duration (total duration, in seconds, that mutual eye gaze was maintained), and bout length (total duration divided by frequency). Interobserver reliability was calculated for chimpanzees by coding several trials side by side (0.89–0.96; see online supplemental materials for more information about the data collection procedures and interobserver reliability). Mutual eye gaze is also consistent across trials (Hopkins et al., 2020). In the current study, frequency, duration, and bout length during the first half of testing was significantly correlated with the second half of testing, chimpanzees, r(119) = 0.538–0.546, p < .001; bonobos, r(18) = 0.601–0.824, p < .01. In addition, Bard and colleagues (2005) found that chimpanzees housed at YNPRC engaged in significantly less mutual eye gaze (between mother—infant dyads) compared with those from a Japanese facility. Our examination of facility-related differences in mutual eye gaze found no site differences for chimpanzees; however, there were differences across the bonobo sites (see online supplemental materials for details).

Results

To examine species differences in mutual eye gaze, we ran a multivariate analysis of covariance with species as the independent variable, the mutual eye gaze measures (average frequency, duration, and bout length) as dependent variables, and both sex and age as covariates. The multivariate analysis of covariance revealed no significant effects of age or sex (see online supplemental materials) but a significant main effect of species, F(3, 143) = 33.66, p < .001, η2 = 0.41. Subsequent univariate F tests revealed significant species differences in frequency, F(l, 145) = 96.68, p < .001, η2 = 0.40, and duration, F(l, 145) = 33.68, p < .001, η2 = 0.19, but no difference in bout length, F(1, 145) = 0.49, p = .48, η2 = 0.003. Bonobos engaged in mutual eye gaze more frequently and for longer total duration than chimpanzees (see Figure 1 for mean frequency, duration, and bout length for each species).

Figure 1.

Figure 1.

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The mean frequency, duration, and bout length of mutual eye gaze of bonobos and chimpanzees. Bonobos engaged in more frequent and longer total duration of eye gaze with a human compared with chimpanzees. Error bars indicate ±95% confidence interval and * indicates p < .001.

Discussion

As predicted, bonobos engaged in more frequent and longer total duration of mutual eye gaze with a human compared with chimpanzees (see Figure 1). Bonobos’ average bout duration was similar to that of chimpanzees, indicating that the difference in total duration was driven by the increase in frequency as chimpanzees and bonobos broke eye contact after approximately the same amount of time (see Figure 1). Even though the experimenter continually attempted to engage in mutual eye gaze (including calling the subject’s name to regain attention), these results are consistent with some results from eye tracking studies in which chimpanzees and bonobos looked at pictures and videos of conspecifics (Kano et al., 2015, 2018). In Kano et al.’s studies, bonobos looked at the eye region of pictures and videos for longer than chimpanzees. The eye-tracking studies, however, also report that chimpanzees looked longer at the mouth region compared with bonobos. a measure not included in the current study. In addition, the seemingly conflicting findings in studies of bonobos’ and chimpanzees’ gaze following may be explained, in part, by the current results. It is possible that bonobos outperform chimpanzees in simple gaze following tasks (Herrmann et al., 2010; Hopkins et al., 2018) as a result of increased frequency and duration of mutual eye gaze (as demonstrated in the current study, as well as eye-tracking studies; Kano et al., 2015. 2018). Similarly, it is possible that chimpanzees may be better able to infer the gaze target and determine if an object is novel to a human (MacLean & Hare, 2012) owing to their reduction in mutual eye gaze (as seen in the current study) and increased target object gaze (as demonstrated in the eye-tracking studies; Kano et al., 2015, 2018). Therefore, there is a trade-off between eye gaze and target gaze; reductions in mutual eye gaze may be beneficial, as it allows more time to focus gaze on a target object. Future research should further examine these species differences and directly test this potential relationship between mutual eye gaze and gaze following.

Further, the results reported here may reflect species differences in social behavior and temperament. Bonobos engage in more affiliative and cooperative behaviors, including greater social tolerance and closer proximity to groupmates, increased adult play, and lower intensity of aggressive behaviors than chimpanzees (see reviews in Hare & Yamamoto, 2017; White & Chapman, 1994). In addition, De Waal (1988) noted that the bonobo’s face, in contrast to the chimpanzee’s, has features that allow for more subtle and expressive facial expressions, cues that are likely monitored by conspecifics using increased eye contact and face-to-face orientation. In fact, compared with chimpanzees, bonobos show increased ventro-ventral contact and attention to faces during embraces, sociosexual behavior, and grooming (De Waal, 1988, 1995). For example, bonobos engage in ventral copulatory sex as well as frequent noncopulatory sex. Bonobos’ noncopulatory sexual behavior (genito-genital rubbing) occurs most often in female-female pairs (but also male-male and male-female) in a ventro-ventral position and involves sustained mutual eye gaze (Fruth & Hohmann, 2006; Hohmann & Fruth, 2000). When they do engage in ventro-dorsal genito-genital rubbing, the dorsal individual will often look back and make sustained eye contact with the other individual (Fruth & Hohmann, 2006; Hohmann & Fruth, 2000). Although female chimpanzees also exhibit genito-genital rubbing, they do so less frequently than bonobos. the most common position is ventro-dorsal, and they do not exhibit mutual eye gaze (Anestis, 2004). In the current study, the increase in bonobo mutual eye gaze is likely related to this increase in, and importance of. mutual eye gaze during affiliative behavior and face-to-face interaction, similar to what is reported for humans (Argyle & Dean, 1965; Kleinke, 1986). Future research could examine the relationship between mutual eye gaze and both affiliative behaviors and face-to-face interactions; it is possible that chimpanzees who engage in more of these behaviors also engage in increased eye contact.

In addition, there are genetic and physiological differences between chimpanzees and bonobos that may be related to mutual eye gaze. Increased oxytocin has been associated with increased eye contact in humans (Auyeung et al., 2015; Guastella, Mitchell, & Dadds, 2008), and interestingly, researchers have identified oxytocin receptor gene polymorphisms that are present in chimpanzees but absent in bonobos (Staes et al., 2014). Bonobos also have a greater density of serotonergic axons in the amygdala, which researchers posit may relate to species differences in sociosexual behavior, emotional reactivity, and responses to faces (Hopkins et al., 2018; Stimpson et al., 2016). Studies on the neural bases of eye gaze in human and nonhuman primates have identified regions, as well as specific neurons, that respond to faces in general or eye contact, specifically (Itier & Batty, 2009; Kamphuis, Dicke, & Their, 2009; Mosher, Zimmerman, & Cothard, 2014: Roy, Shepherd, & Platt, 2014). More recently, the bout length of mutual eye gaze in chimpanzees was associated with variation in the volume of gray matter in regions that make up the ventral pathway of the visual processing stream and the reward circuit (Hopkins et al., 2020). No studies have examined such neuroanatomical associations with mutual eye gaze in bonobos. but it is possible that bonobos would show’ a different pattern of association related to the difference in mutual eye gaze reported herein. In fact, bonobos are known to have higher gray matter volume in some of these regions (e.g., the amygdala, inferior temporal cortex, visual cortex, and nucleus accumbens; Hopkins et al. 2018; Rilling et al, 2012). Further research on the neuroanatomical and genetic correlates of mutual eye gaze in both species would tell us more about the mechanisms underlying these species differences.

Overall, the current study shows that bonobos engage in more frequent and longer durations of mutual eye gaze (with human observers) compared with chimpanzees. These findings are the first to compare mutual eye gaze between the two species directly and support previous findings from eye-tracking studies using video and picture stimuli. In addition, this study may help us to better frame previous studies of gaze following that use human observers. Continued studies of eye gaze behaviors of both bonobos and chimpanzees can advance our understanding of human evolution.

Supplementary Material

Supp Material

Acknowledgments

This research was supported by National Institutes of Health Grants U42-OD-O11197 to the National Center for Chimpanzee Care and P51OD11132 to Yerkes National Primate Research Center. Additional support was provided by National Institutes of Health Grant NS-42867 to William D. Hopkins.

Footnotes

Contributor Information

Michele M. Mulholland, Center for Behavioral Neuroscience, Georgia State University, and Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center, Bastrop, Texas

Mary Catherine Mareno, Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center.

Lisa A. Reamer, Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center

Lindsay M. Mahovetz, Department of Psychology, University of North Florida

Steven J. Schapiro, Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center, and Department of Experimental Medicine, University of Copenhagen

William D. Hopkins, Department of Comparative Medicine, The University of Texas MD Anderson Cancer Center

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