The development and flexibility of gaze alternations in bonobos and chimpanzees

Infants’ early gaze alternations are one of their first steps towards a sophisticated understanding of the social world. This ability, to gaze alternate between an object of interest and another individual also attending to that object, has been considered foundational to the development of many complex social‐cognitive abilities, such as theory of mind and language. However, to understand the evolution of these abilities, it is important to identify whether and how gaze alternations are used and develop in our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Here, we evaluated the development of gaze alternations in a large, developmental sample of bonobos (N = 17) and chimpanzees (N = 35). To assess the flexibility of ape gaze alternations, we tested whether they produced gaze alternations when requesting food from a human who was either visually attentive or visually inattentive. Similarly to human infants, both bonobos and chimpanzees produced gaze alternations, and did so more frequently when a human communicative partner was visually attentive. However, unlike humans, who gaze alternate frequently from early in development, chimpanzees did not begin to gaze alternate frequently until adulthood. Bonobos produced very few gaze alternations, regardless of age. Thus, it may be the early emergence of gaze alternations, as opposed gaze alternations themselves, that is derived in the human lineage. The distinctively early emergence of gaze alternations in humans may be a critical underpinning for the development of complex human social‐cognitive abilities.     

Now you see me,now you don't: evidence that chimpanzees understand the role of the eyes in attention

Chimpanzees appear to understand something about the attentional states of others; in the present experiment, we investigated whether they understand that the attentional state of a human is based on eye gaze. In all, 116 adult chimpanzees were offered food by an experimenter who engaged in one of the four experimental manipulations: eyes closed, eyes open, hand over eyes, and hand over mouth. The communicative behavior of the chimpanzees was observed. More visible behaviors were produced when the experimenter's eyes were visible than when the experimenter's eyes were not visible. More vocalizations were produced when the experimenter's eyes were closed than when they were open, but there were no differences in other attention getting behaviors. There was no effect of age or rearing history. The results suggest that chimpanzees use the presence of the eyes as a cue that their visual gestures will be effective.     

A comparison of temperament in nonhuman apes and human infants

The adaptive behavior of primates, including humans, is often mediated by temperament. Human behavior likely differs from that of other primates in part due to temperament. In the current study we compared the reaction of bonobos, chimpanzees, orangutans, and 2.5-year-old human infants to novel objects and people - as a measure of their shyness-boldness, a key temperamental trait. Human children at the age of 2.5 years avoided novelty of all kinds far more than the other ape species. This response was most similar to that seen in bonobos and least like that of chimpanzees and orangutans. This comparison represents a first step in characterizing the temperamental profiles of species in the hominoid clade, and these findings are consistent with the hypothesis that human temperament has evolved since our lineage diverged from the other apes in ways that likely have broad effects on behavior. These findings also provide new insights into how species differences in ecology may shape differences in temperament.     

Chimpanzee Use of Human and Conspecific Social Cues to Locate Hidden Food

Two studies are reported in which chimpanzees attempted to use social cues to locate hidden food in one of two possible hiding places. In the first study four chimpanzees were exposed to a local enhancement cue (the informant approached and looked to the location where food was hidden and then remained beside it) and a gaze/point cue (the informant gazed and manually pointed towards the location where the food was hidden). Each cue was given by both a human informant and a chimpanzee informant. In the second study 12 chimpanzees were exposed to a gaze direction cue in combination with a vocal cue (the human informant gazed to the hiding location and produced one of two different vocalizations: a ‘food-bark’ or a human word-form). The results were: (i) all subjects were quite skillful with the local enhancement cue, no matter who produced it; (ii) few subjects were skillful with the gaze/point cue, no matter who produced it (most of these being individuals who had been raised in infancy by humans); and (iii) most subjects were skillful when the human gazed and vocalized at the hiding place, with little difference between the two types of vocal cue. Findings are discussed in terms of chimpanzees’ apparent need for additional cues, over and above gaze direction cues, to indicate the presence of food.     

Perceptual mechanism underlying gaze guidance in chimpanzees and humans

Previous studies comparing eye movements between humans and their closest relatives, chimpanzees, have revealed similarities and differences between the species in terms of where individuals fixate their gaze during free viewing of a naturalistic scene, including social stimuli (e.g. body and face). However, those results were somewhat confounded by the fact that gaze behavior is influenced by low-level stimulus properties (e.g., color and form) and by high-level processes such as social sensitivity and knowledge about the scene. Given the known perceptual and cognitive similarities between chimpanzees and humans, it is expected that such low-level effects do not play a critical role in explaining the high-level similarities and differences between the species. However, there is no quantitative evidence to support this assumption. To estimate the effect of local stimulus saliency on such eye-movement patterns, this study used a well-established bottom-up saliency model. In addition, to elucidate the cues that the viewers use to guide their gaze, we presented scenes in which we had manipulated various stimulus properties. As expected, the saliency model did not fully predict the fixation patterns actually observed in chimpanzees and humans. In addition, both species used multiple cues to fixate socially significant areas such as the face. There was no evidence suggesting any differences between chimpanzees and humans in their responses to low-level saliency. Therefore, this study found a substantial amount of similarity in the perceptual mechanisms underlying gaze guidance in chimpanzees and humans and thereby offers a foundation for direct comparisons between them.     

Chimpanzees and bonobos exhibit divergent spatial memory development

Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (Studies 1 and 2). We then compared older apes using a matched memory choice paradigm (Study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species’ different feeding ecologies. Furthermore, chimpanzees – but not bonobos – showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.     

Species difference in the timing of gaze movement between chimpanzees and humans

How do humans and their closest relatives, chimpanzees, differ in their fundamental abilities for seeing the visual world? In this study, we directly compared the gaze movements of humans and the closest species, chimpanzees, using an eye-tracking system. During free viewing of a naturalistic scene, chimpanzees made more fixations per second (up to four) than did humans (up to three). This species difference was independent of the semantic variability of the presented scenes. The gap–overlap paradigm revealed that, rather than resulting from the sensitivity to the peripherally presented stimuli per se, the species difference reflected the particular strategy each species employed to solve the rivalry between central (fixated) and peripheral stimuli in their visual fields. Finally, when presented with a movie in which small images successively appeared/disappeared at random positions at the chosen presentation rate, chimpanzees tracked those images at the point of fixation for a longer time than did humans, outperforming humans in their speed of scanning. Our results suggest that chimpanzees and humans differ quantitatively in their visual strategies involving the timing of gaze movement. We discuss the functional reasons for each species’ employing such specific strategies.     

Human ostensive signals do not enhance gaze following in chimpanzees,but do enhance object-oriented attention

The previous studies have shown that human infants and domestic dogs follow the gaze of a human agent only when the agent has addressed them ostensively—e.g., by making eye contact, or calling their name. This evidence is interpreted as showing that they expect ostensive signals to precede referential information. The present study tested chimpanzees, one of the closest relatives to humans, in a series of eye-tracking experiments using an experimental design adapted from these previous studies. In the ostension conditions, a human actor made eye contact, called the participant’s name, and then looked at one of two objects. In the control conditions, a salient cue, which differed in each experiment (a colorful object, the actor’s nodding, or an eating action), attracted participants’ attention to the actor’s face, and then the actor looked at the object. Overall, chimpanzees followed the actor’s gaze to the cued object in both ostension and control conditions, and the ostensive signals did not enhance gaze following more than the control attention-getters. However, the ostensive signals enhanced subsequent attention to both target and distractor objects (but not to the actor’s face) more strongly than the control attention-getters—especially in the chimpanzees who had a close relationship with human caregivers. We interpret this as showing that chimpanzees have a simple form of communicative expectations on the basis of ostensive signals, but unlike human infants and dogs, they do not subsequently use the experimenter’s gaze to infer the intended referent. These results may reflect a limitation of non-domesticated species for interpreting humans’ ostensive signals in inter-species communication.     

Responses toward a trapped animal by wild bonobos at Wamba

Chimpanzees and bonobos are the closest living relatives of humans and diverged relatively recently in their phylogenetic history. However, a number of reports have suggested behavioral discrepancies between the two Pan species, such as more cooperative and tolerant social interaction and poorer tool-using repertoires in bonobos. Concerning hunting behavior and meat consumption, recent studies from the field have confirmed both behaviors not only in chimpanzees but also in bonobos. The present study reports an encounter by wild bonobos at Wamba with a duiker trapped in a snare. Bonobos interacted with the live duiker for about 10 min but did not eventually kill the animal. They showed fear responses when the duiker moved and exhibited behaviors related to anxiety and stress such as branch-drag displays and self-scratching. Although bonobos manipulated nearby saplings and parts of the snare, they did not use detached objects to make indirect contact with the duiker. Juveniles and adults of both sexes engaged in active interactions with the trapped duiker. Overall, bonobos’ behavioral responses indicated species-specific cognitive characteristics largely different from those of chimpanzees.     

Chimpanzee gaze following in an object-choice task

Many primate species reliably track and follow the visual gaze of conspecifics and humans, even to locations above and behind the subject. However, it is not clear whether primates follow a human’s gaze to find hidden food under one of two containers in an object-choice task. In a series of experiments six adult female chimpanzees followed a human’s gaze (head and eye direction) to a distal location in space above and behind them, and checked back to the human’s face when they did not find anything interesting or unusual. This study also assessed whether these same subjects would also use the human’s gaze in an object-choice task with three types of occluders: barriers, tubes, and bowls. Barriers and tubes permitted the experimenter to see their contents (i.e., food) whereas bowls did not. Chimpanzees used the human’s gaze direction to choose the tube or barrier containing food but they did not use the human’s gaze to decide between bowls. Our findings allowed us to discard both simple orientation and understanding seeing-knowing in others as the explanations for gaze following in chimpanzees. However, they did not allow us to conclusively choose between orientation combined with foraging tendencies and understanding seeing in others. One interesting possibility raised by these results is that studies in which the human cannot see the reward at the time of subject choice may potentially be underestimating chimpanzees’ social knowledge. Received: 16 February 1998 / Accepted after revision: 5 July 1998     

Comparative and familial analysis of handedness in great apes

Historically, population-level handedness has been considered a hallmark of human evolution. Whether nonhuman primates exhibit population-level handedness remains a topic of considerable debate. This paper summarizes published data on handedness in great apes. Comparative analysis indicated that chimpanzees and bonobos show population-level right handedness, whereas gorillas and orangutans do not. All ape species showed evidence of population-level handedness when considering specific tasks. Familial analyses in chimpanzees indicated that offspring and maternal (but not paternal) handedness was significantly positively correlated, but this finding was contingent upon the classification criteria used to evaluate hand preference. Overall, the proportion of right handedness is lower in great apes compared with humans, and various methodological and theoretical explanations for this discrepancy are discussed.     

Gaze following and gaze priming in lemurs

Although primates have often been found to co-orient visually with other individuals, members of these same species have usually failed to use co-orientation to find hidden food in object-choice experiments. This presents an evolutionary puzzle: what is the function of co-orientation if it is not used for a function as basic as locating resources? Co-orientation responses have not been systematically investigated in object-choice experiments, and requiring co-orientation with humans (as is typical in object-choice tasks) may underestimate other species’ abilities. Using an object-choice task with conspecific models depicted in photographs, we provide experimental evidence that two lemur species (Eulemur fulvus, n = 4, and Eulemur macaco, n = 2) co-orient with conspecifics. Secondly, by analysing together two measures that have traditionally been examined separately, we show that lemurs’ gaze following behaviour and ultimate choice are closely linked. Individuals were more likely to choose correctly after having looked in the same direction as the model, and thus chose objects correctly more often than chance. We propose a candidate system for the evolutionary origins of more complex gaze following: ‘gaze priming.’     

Differential reliance of chimpanzees and humans on automatic and deliberate control of motor actions

Humans are often unaware of how they control their limb motor movements. People pay attention to their own motor movements only when their usual motor routines encounter errors. Yet little is known about the extent to which voluntary actions rely on automatic control and when automatic control shifts to deliberate control in nonhuman primates. In this study, we demonstrate that chimpanzees and humans showed similar limb motor adjustment in response to feedback error during reaching actions, whereas attentional allocation inferred from gaze behavior differed. We found that humans shifted attention to their own motor kinematics as errors were induced in motor trajectory feedback regardless of whether the errors actually disrupted their reaching their action goals. In contrast, chimpanzees shifted attention to motor execution only when errors actually interfered with their achieving a planned action goal. These results indicate that the species differed in their criteria for shifting from automatic to deliberate control of motor actions. It is widely accepted that sophisticated motor repertoires have evolved in humans. Our results suggest that the deliberate monitoring of one’s own motor kinematics may have evolved in the human lineage.     

What makes us human (Homo sapiens)? The challenge of cognitive cross-species comparison

Two major theoretical approaches have dominated the quest for uniquely human cognitive abilities: a developmentalist approach stressing the importance of environmental and social conditions, and a predominant approach in experimental and comparative psychology, the deterministic approach suggesting the effect of environmental and social conditions to be minimal. As a consequence, most claims of human cognitive uniqueness are based on comparisons of White middle class Westerner humans (Homo sapiens) with captive chimpanzees (Pan troglodytes). However, humans are much more than only White middle class Westerners, and chimpanzees are much more than only captives. A review of some data available on different populations of humans and chimpanzees reveals that only the predictions of the developmentalist approach are supported. In addition, systematic biases are too often introduced in experiment protocols when comparing humans with apes that further cast doubts on cross-species comparisons. The author argues that only with consideration of within-species population differences in the cognitive domains and the use of well-matched cross-species experimental procedures will an objective understanding of the different cognitive abilities between species emerge. This will require a shift in the theoretical approach adopted by many in experimental and comparative psychology.     

Cues that chimpanzees do and do not use to find hidden objects

Chimpanzees follow conspecific and human gaze direction reliably in some situations, but very few chimpanzees reliably use gaze direction or other communicative signals to locate hidden food in the object-choice task. Three studies aimed at exploring factors that affect chimpanzee performance in this task are reported. In the first study, vocalizations and other noises facilitated the performance of some chimpanzees (only a minority). In the second study, various behavioral cues were given in which a human experimenter either touched, approached, or actually lifted and looked under the container where the food was hidden. Each of these cues led to enhanced performance for only a very few individuals. In the third study – a replication with some methodological improvements of a previous experiment – chimpanzees were confronted with two experimenters giving conflicting cues about the location of the hidden food, with one of them (the knower) having witnessed the hiding process and the other (the guesser) not. In the crucial test in which a third experimenter did the hiding, no chimpanzee found the food at above chance levels. Overall, in all three studies, by far the best performers were two individuals who had been raised in infancy by humans. It thus seems that while chimpanzees are very good at “behavior reading” of various sorts, including gaze following, they do not understand the communicative intentions (informative intentions) behind the looking and gesturing of others – with the possible exception of enculturated chimpanzees, who still do not understand the differential significance of looking and gesturing done by people who have different knowledge about states of affairs in the world. Received: 8 November 1999 / Accepted after revision: 24 January 2000     

Is chimpanzee (Pan troglodytes) spatial attention reflexively triggered by gaze cue?

Humans show a reflexive shift in spatial attention triggered by gaze cues. Chimpanzees (Pan troglodytes) have an excellent ability to follow another's gaze, but they exhibit a limited capacity to engage in triadic interactions based on joint attention, suggesting the possibility of contributions of the different mechanisms underlying joint attention between humans and chimpanzees. The present study thus examined how the chimpanzee's visual spatial attention is triggered by gaze cues. Two chimpanzees showed no clear signs of attention shift triggered by various kinds of nonfacial and facial stimuli with averted gaze under the letter-discrimination tasks but showed significant cueing effects when the head-turning cue was presented in a quasi-dynamic manner. These cueing effects were, however, affected by the predictability of the gaze cue: Highly predictive gaze cues caused stronger cueing effects than less predictive cues. Thus, these results suggest that the shift in spatial attention caused by gaze cues does occur in chimpanzees, but, in contrast to humans, vulnerability against the cue predictability suggests that the voluntary mechanism contributes more dominantly than the reflexive mechanism to this attention shift.     

From Nonhuman to Human Mind: What Changed and Why?

ABSTRACT— Two questions regarding the human mind challenge evolutionary theory: (a) What features of human psychology have changed since humans' lineage split from that of the other apes such as chimpanzees and bonobos? And (b) what was the process by which such derived psychological features evolved (e.g., what were the selection pressures)? I review some of the latest research on chimpanzee and canine psychology that allows inferences to be made regarding these questions.     

Group differences in the mutual gaze of chimpanzees (Pan troglodytes)

A comparative developmental framework was used to determine whether mutual gaze is unique to humans and, if not, whether common mechanisms support the development of mutual gaze in chimpanzees and humans. Mother-infant chimpanzees engaged in approximately 17 instances of mutual gaze per hour. Mutual gaze occurred in positive, nonagonistic contexts. Mother-infant chimpanzees at a Japanese center exhibited significantly more mutual gaze than those at a center in the United States. Cradling and motor stimulation varied across groups. Time spent cradling infants was inversely related to mutual gaze. It is suggested that in primates, mutual engagement is supported via an interchangeability of tactile and visual modalities. The importance of mutual gaze is best understood within a perspective that embraces both cross-species and cross-cultural data.     

Carryover effect of joint attention to repeated events in chimpanzees and young children

Gaze following is a fundamental component of triadic social interaction which includes events and an object shared with other individuals and is found in both human and nonhuman primates. Most previous work has focused only on the immediate reaction after following another’s gaze. In contrast, this study investigated whether gaze following is retained after the observation of the other’s gaze shift, whether this retainment differs between species and age groups, and whether the retainment depends on the nature of the preceding events. In the social condition, subjects (1- and 2-year-old human children and chimpanzees) witnessed an experimenter who looked and pointed in the direction of a target lamp. In the physical condition, the target lamp blinked but the experimenter did not provide any cues. After a brief delay, we presented the same stimulus again without any cues. All subjects looked again to the target location after experiencing the social condition and thus showed a carryover effect. However, only 2-year-olds showed a carryover effect in the physical condition; 1-year-olds and chimpanzees did not. Additionally, only human children showed spontaneous interactive actions such as pointing. Our results suggest that the difference between the two age groups and chimpanzees is conceptual and not only quantitative.     

Chimpanzees help others with what they want; children help them with what they need

Humans, including young children, are strongly motivated to help others, even paying a cost to do so. Humans’ nearest primate relatives, great apes, are likewise motivated to help others, raising the question of whether the motivations of humans and apes are the same. Here we compared the underlying motivation to help in human children and chimpanzees. Both species understood the situation and helped a conspecific in a straightforward situation. However, when helpers knew that what the other was requesting would not actually help her, only children gave her what she needed instead of giving her what she requested. These results suggest that both chimpanzees and human children help others but the underlying motivation for why they help differs. In comparison to chimpanzees, young children help in a paternalistic manner. The evolutionary hypothesis is that uniquely human socio‐ecologies based on interdependent cooperation gave rise to uniquely human prosocial motivations to help others paternalistically.