Multimodal communication by captive chimpanzees (Pan troglodytes)

Many studies have shown that apes and monkeys are adept at cross-modal matching tasks requiring the subject to identify objects in one modality when information regarding those objects has been presented in a different modality. However, much less is known about non-human primates’ production of multimodal signaling in communicative contexts. Here, we present evidence from a study of 110 chimpanzees demonstrating that they select the modality of communication in accordance with variations in the attentional focus of a human interactant, which is consistent with previous research. In each trial, we presented desirable food to one of two chimpanzees, turning mid-way through the trial from facing one chimpanzee to facing the other chimpanzee, and documented their communicative displays, as the experimenter turned towards or away from the subjects. These chimpanzees varied their signals within a context-appropriate modality, displaying a range of different visual signals when a human experimenter was facing them and a range of different auditory or tactile (attention-getting) signals when the human was facing away from them; this finding extends previous research on multimodal signaling in this species. Thus, in the impoverished circumstances characteristic of captivity, complex signaling tactics are nevertheless exhibited by chimpanzees, suggesting continuity in intersubjective psychological processes in humans and apes.     

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.     

Olive baboons communicate intentionally by pointing

A pointing gesture creates a referential triangle that incorporates distant objects into the relationship between the signaller and the gesture’s recipient. Pointing was long assumed to be specific to our species. However, recent reports have shown that pointing emerges spontaneously in captive chimpanzees and can be learned by monkeys. Studies have demonstrated that both human children and great apes use manual gestures (e.g. pointing), and visual and vocal signals, to communicate intentionally about out-of-reach objects. Our study looked at how monkeys understand and use their learned pointing behaviour, asking whether it is a conditioned, reinforcement-dependent response or whether monkeys understand it to be a mechanism for manipulating the attention of a partner (e.g. a human). We tested nine baboons that had been trained to exhibit pointing, using operant conditioning. More specifically, we investigated their ability to communicate intentionally about the location of an unreachable food reward in three contexts that differed according to the human partner’s attentional state. In each context, we quantified the frequency of communicative behaviour (auditory and visual signals), including gestures and gaze alternations between the distal food and the human partner. We found that the baboons were able to modulate their manual and visual communicative signals as a function of the experimenter’s attentional state. These findings indicate that monkeys can intentionally produce pointing gestures and understand that a human recipient must be looking at the pointing gesture for them to perform their attention-directing actions. The referential and intentional nature of baboons’ communicative signalling is discussed.     

Tufted capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) show understanding of human attentional states when requesting food held by a human

Researchers have investigated to what extent non-human primates understand others’ attentional states, as this ability is considered an important prerequisite for theory of mind. However, previous studies using food requesting tasks have failed to show that non-human primates attribute perception to others as a function of their attentional states. One possible reason is that food requesting tasks may require subjects not only to take into account an experimenter’s attentional state but also to direct it toward the food. The present study tested tufted capuchin monkeys’ (Cebus apella) understanding of others’ attentional states in a food requesting task. In the first situation, monkeys were required only to attract an experimenter’s attention. In the second situation, the monkeys were required to both attract the experimenter’s attention and direct it toward food on a table. The results revealed that capuchin monkeys showed evidence of understanding the experimenter’s attentional variations only in the former condition. This suggests that previous tasks, requiring referential gestures, lacking in most non-human primates, failed to reveal sensitivity to human attentional states because the subjects might not have understood the requesting situation. In conclusion, capuchin monkeys can understand variations in others’ attentional states, although this ability appears limited compared to what is seen in humans.     

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     

Different social motives in the gestural communication of chimpanzees and human children

Both chimpanzees and human infants use the pointing gesture with human adults, but it is not clear if they are doing so for the same social motives. In two studies, we presented chimpanzees and human 25-month-olds with the opportunity to point for a hidden tool (in the presence of a non-functional distractor). In one condition it was clear that the tool would be used to retrieve a reward for the pointing subject (so the pointing was selfish or 'for-me'), whereas in the other condition it was clear that the tool would be used to retrieve the reward for the experimenter (so the pointing was helpful or 'for-you'). The chimpanzees pointed reliably only when they themselves benefited, whereas the human children pointed reliably no matter who benefited. These results are interpreted as evidence for the especially cooperative nature of human communication.     

Do chimpanzees tailor their gestural signals to fit the attentional states of others?

The use of vocalizations and tactile gestures by seven juvenile chimpanzees was experimentally investigated. The subjects interacted with an experimenter who typically handed them food rewards. In some trials, however, the experimenter waited 20 s before doing so. In these trials the experimenter’s eyes were either open or closed, or the experimenter was either looking away from the subject or looking directly at him/her inquisitively with head movements. Although the chimpanzees produced at least one of the non-visual gestures mentioned (touching/tapping the experimenter or vocalizing) in 72% of all experimental trials, these actions and vocalizations were deployed without regard to the attentional state of their potential recipient, despite evidence that the subjects noticed the postures that defined the experimenter’s attentional state. The results are discussed in the context of the distinction between the evolution of an understanding of seeing/attention as an internal mental state versus an understanding of behavioral postures alone. Recieved: 12 February 1999 / Accepted after revision: 18 August 1999     

Focus on the essential: all great apes know when others are being attentive

When begging for food, all great ape species are sensitive to a human’s attention. However, studies investigating which cues are relevant for chimpanzees to assess the attentional state of others have produced highly inconsistent results. Some have suggested chimpanzees differentiate attention based on the status of the face or even the eyes, while others have indicated that body posture alone is the relevant cue. Kaminski et al. (Anim Cogn 7:216–223, 2004) compared the behaviour of chimpanzees, bonobos and orangutans while begging for food from a human experimenter who systematically varied his face and body orientation. Their results indicated that both factors, face and body orientation, affect apes’ begging behaviour. The authors claimed that while body orientation provides information about the experimenter’s general disposition to offer food, the visibility of the face provides information about the human’s attentional state. In the current study, we tested this hypothesis with all four great apes species. However, unlike Kaminski et al. (Anim Cogn 7:216–223, 2004), the experimenter was able to hand over food regardless of body orientation. The results show that as soon as the offering of the food was no longer restricted, the orientation of the face became the key factor. Therefore, we present the first evidence that all great ape species are able to assess the attentional state of a recipient based on the orientation of the face.     

Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens)

This study examined the communicative behavior of 49 captive chimpanzees (Pan troglodytes), particularly their use of vocalizations, manual gestures, and other auditory- or tactile-based behaviors as a means of gaining an inattentive audience's attention. A human (Homo sapiens) experimenter held a banana while oriented either toward or away from the chimpanzee. The chimpanzees' behavior was recorded for 60 s. Chimpanzees emitted vocalizations faster and were more likely to produce vocalizations as their 1st communicative behavior when a human was oriented away from them. Chimpanzees used manual gestures more frequently and faster when the human was oriented toward them. These results replicate the findings of earlier studies on chimpanzee gestural communication and provide new information about the intentional and functional use of their vocalizations.     

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.     

Gaze alternation in dogs and toddlers in an unsolvable task: evidence of an audience effect

Dogs have been shown to use human-directed gazing behaviour and gaze alternation in numerous contexts; however, it is still unclear whether this behaviour can be considered an intentional and referential communicative act. In the current study, adult dogs and preverbal toddlers were tested using the classic unsolvable task paradigm, but varying the attentional stance of the participating audience (the experimenter and the caregiver). The aims were to assess (1) whether dogs and toddlers would use gaze alternation behaviour in similar manners when the task became unsolvable, and (2) whether both dogs and toddlers would take into account the attentional stance of the audience when initiating a communicative interaction. Results indicated that both toddlers and dogs increased their gaze alternation behaviour between the apparatus and caregiver when the task became unsolvable, and toddlers also showed an increase in pointing behaviour. Furthermore, both species showed a capacity to take into account the attentional stance of the audience when manifesting gaze alternation behaviours towards them. Taken together, these results suggest that gaze alternation is both an intentional and referential communicative act and that both species can take into account the need for audience attention when communicating with them.     

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.     

Exploitation of pointing as a referential gesture in young children, but not adolescent chimpanzees

The ability of adolescent chimpanzees and 2- and 3-year-old children to use pointing gestures to locate hidden surprises was examined in two experiments. The results revealed that although young 2-year-old children appeared to have no difficulty extracting referential information from a pointing gesture (independent of gaze or distance cues) and spontaneously using it to search in specific locations, adolescent chimpanzees appeared to rely on cueconfiguration and distance-based rules. Thus, although these chimpanzees were trained to respond appropriately to the pointing gestures of a human by searching in a particular location, this ability did not easily generalize to situations in which the distance between the pointing hand and the location were more distal. Furthermore, even those chimpanzees that were able to generalize in this fashion appeared to use distance-based cues, not ones based on an appreciation of the internal attentional focus or mental referent of the experimenter as indicated by his pointing gesture.     

I know you are not looking at me: capuchin monkeys’ (<Emphasis Type="Italic">Cebus apella</Emphasis>) sensitivity to human attentional states

The present study asked whether capuchin monkeys recognize human attentional states. The monkeys requested food from the experimenter by extending an arm (pointing) toward the baited one of two transparent cups. On regular trials the experimenter gave the food immediately to the monkeys upon pointing but on randomly inserted test trials she ignored the pointing for 5 s during which she displayed different attentional states. The monkeys looked at the experimenter's face longer when she looked at the monkeys than when she looked at the ceiling in Experiment 1, and longer when she oriented her head midway between the two cups with eyes open than when she did so with eyes closed in Experiment 2. However, the monkeys showed no differential pointing in these conditions. These results suggest that capuchins are sensitive to eye direction but this sensitivity does not lead to differential pointing trained in laboratory experiments. Furthermore, to our knowledge, this is the first firm behavioral evidence that non-human primates attend to the subtle states of eyes in a food requesting task.     

‘Unwilling’ versus ‘unable’: capuchin monkeys’ (Cebus apella) understanding of human intentional action

A sensitivity to the intentions behind human action is a crucial developmental achievement in infants. Is this intention reading ability a unique and relatively recent product of human evolution and culture, or does this capacity instead have roots in our non‐human primate ancestors? Recent work by Call and colleagues (2004) lends credence to the latter hypothesis, providing evidence that chimpanzees are also sensitive to human intentions. Specifically, chimpanzees remained in a testing area longer and exhibited fewer frustration behaviors when an experimenter behaved as if he intended to give food but was unable to do so, than when the experimenter behaved as if he had no intention of giving food. The present research builds on and extends this paradigm, providing some of the first evidence of intention reading in a more distant primate relative, the capuchin monkey (Cebus apella). Like chimpanzees, capuchin monkeys distinguish between different goal‐directed acts, vacating an enclosure sooner when an experimenter acts unwilling to give food than when she acts unable to give food. Additionally, we found that this pattern is specific to animate action, and does not obtain when the same actions are performed by inanimate rods instead of human hands (for a similar logic, see Woodward, 1998 ). Taken together with the previous evidence, the present research suggests that our own intention reading is not a wholly unique aspect of the human species, but rather is shared broadly across the primate order.     

Apes' use of iconic cues in the object-choice task

In previous studies great apes have shown little ability to locate hidden food using a physical marker placed by a human directly on the target location. In this study, we hypothesized that the perceptual similarity between an iconic cue and the hidden reward (baited container) would help apes to infer the location of the food. In the first two experiments, we found that if an iconic cue is given in addition to a spatial/indexical cue - e.g., picture or replica of a banana placed on the target location - apes (chimpanzees, bonobos, orangutans, gorillas) as a group performed above chance. However, we also found in two further experiments that when iconic cues were given on their own without spatial/indexical information (iconic cue held up by human with no diagnostic spatial/indexical information), the apes were back to chance performance. Our overall conclusion is that although iconic information helps apes in the process of searching hidden food, the poor performance found in the last two experiments is due to apes' lack of understanding of the informative (cooperative) communicative intention of the experimenter.     

Spontaneous use of tools as straws in great apes

Great apes can use multiple tools to extract food embedded in substrates and can invent new ways to exploit those resources. We tested five bonobos, five chimpanzees, and six orangutans in a task in which they had to use (and modify) a tool as a straw to drink the juice located inside a container. Experiment 1 showed that four orangutans and one chimpanzee invented the use of a piece of electric cable to get the juice. Experiment 2 investigated whether subjects could transform a non-functional hose into a functional one by removing blockages that impeded the free flow of juice. Orangutans outperformed chimpanzees and bonobos by differentially removing those blockages that prevented the flow of juice, often doing so before attempting to extract the juice. In Experiment 3, we presented chimpanzees and orangutans with four 3-tool sets (each tool set contained a single straw-like tool) and allowed them to select one tool. Unlike chimpanzees, orangutans succeeded in selecting the straw-like tool above chance levels without having to physically manipulate it. We suggest that orangutans’ superior performance is related to their greater reliance on mouth actions during foraging. Experiment 4 investigated whether orangutans were also capable of selecting the suitable tool not by its appearance, but by the effects that it produced. After witnessing the experimenter blow bubbles or absorb liquid with a functional tool but fail to accomplish the same thing with the non-functional tool, orangutans failed to select the functional tool above chance levels.     

Domestic horses send signals to humans when they face with an unsolvable task

Some domestic animals are thought to be skilled at social communication with humans due to the process of domestication. Horses, being in close relationship with humans, similar to dogs, might be skilled at communication with humans. Previous studies have indicated that they are sensitive to bodily signals and the attentional state of humans; however, there are few studies that investigate communication with humans and responses to the knowledge state of humans. Our first question was whether and how horses send signals to their potentially helpful but ignorant caretakers in a problem-solving situation where a food item was hidden in a bucket that was accessible only to the caretakers. We then examined whether horses alter their behaviours on the basis of the caretakers’ knowledge of where the food was hidden. We found that horses communicated to their caretakers using visual and tactile signals. The signalling behaviour of the horses significantly increased in conditions where the caretakers had not seen the hiding of the food. These results suggest that horses alter their communicative behaviour towards humans in accordance with humans’ knowledge state.     

Sensing sociality in dogs: what may make an interactive robot social?

This study investigated whether dogs would engage in social interactions with an unfamiliar robot, utilize the communicative signals it provides and to examine whether the level of sociality shown by the robot affects the dogs’ performance. We hypothesized that dogs would react to the communicative signals of a robot more successfully if the robot showed interactive social behaviour in general (towards both humans and dogs) than if it behaved in a machinelike, asocial way. The experiment consisted of an interactive phase followed by a pointing session, both with a human and a robotic experimenter. In the interaction phase, dogs witnessed a 6-min interaction episode between the owner and a human experimenter and another 6-min interaction episode between the owner and the robot. Each interaction episode was followed by the pointing phase in which the human/robot experimenter indicated the location of hidden food by using pointing gestures (two-way choice test). The results showed that in the interaction phase, the dogs’ behaviour towards the robot was affected by the differential exposure. Dogs spent more time staying near the robot experimenter as compared to the human experimenter, with this difference being even more pronounced when the robot behaved socially. Similarly, dogs spent more time gazing at the head of the robot experimenter when the situation was social. Dogs achieved a significantly lower level of performance (finding the hidden food) with the pointing robot than with the pointing human; however, separate analysis of the robot sessions suggested that gestures of the socially behaving robot were easier for the dogs to comprehend than gestures of the asocially behaving robot. Thus, the level of sociality shown by the robot was not enough to elicit the same set of social behaviours from the dogs as was possible with humans, although sociality had a positive effect on dog–robot interactions.     

How to crack nuts: acquisition process in captive chimpanzees (Pan troglodytes) observing a model

Stone tool use for nut cracking consists of placing a hard-shelled nut onto a stone anvil and then cracking the shell open by pounding it with a stone hammer to get to the kernel. We investigated the acquisition of tool use for nut cracking in a group of captive chimpanzees to clarify what kind of understanding of the tools and actions will lead to the acquisition of this type of tool use in the presence of a skilled model. A human experimenter trained a male chimpanzee until he mastered the use of a hammer and anvil stone to crack open macadamia nuts. He was then put in a nut-cracking situation together with his group mates, who were naïve to this tool use; we did not have a control group without a model. The results showed that the process of acquisition could be broken down into several steps, including recognition of applying pressure to the nut, emergence of the use of a combination of three objects, emergence of the hitting action, using a tool for hitting, and hitting the nut. The chimpanzees recognized these different components separately and practiced them one after another. They gradually united these factors in their behavior leading to their first success. Their behavior did not clearly improve immediately after observing successful nut cracking by a peer, but observation of a skilled group member seemed to have a gradual, long-term influence on the acquisition of nut cracking by naïve chimpanzees.