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.     

Do common ravens (<Emphasis Type="Italic">Corvus corax</Emphasis>) rely on human or conspecific gaze cues to detect hidden food?

The ability of non-human animals to use experimenter-given cues in object-choice tasks has recently gained interest. In such experiments, the location of hidden food is indicated by an experimenter, e.g. by gazing, pointing or touching. Whereas dogs apparently outperform all other species so far tested, apes and monkeys have problems in using such cues. Since only mammalian species have been tested, information is lacking about the evolutionary origin of these abilities. We here present the first data on object-choice tasks conducted with an avian species, the common raven. Ravens are highly competitive scavengers, possessing sophisticated cognitive skills in protecting their food caches and pilfering others’ caches. We conducted three experiments, exploring (i) which kind of cues ravens use for choosing a certain object, (ii) whether ravens use humans’ gaze for detecting hidden food and (iii) whether ravens would find hidden food in the presence of an informed conspecific who potentially provides gaze cues. Our results indicate that ravens reliably respond to humans’ touching of an object, but they hardly use point and gaze cues for their choices. Likewise, they do not perform above chance level in the presence of an informed conspecific. These findings mirror those obtained for primates and suggest that, although ravens may be aware of the gaze direction of humans and conspecifics, they apparently do not rely on this information to detect hidden food.     

Use of experimenter-given cues in dogs

Since the observations of O. Pfungst the use of human-provided cues by animals has been well-known in the behavioural sciences (“Clever Hans effect”). It has recently been shown that rhesus monkeys (Macaca mulatta) are unable to use the direction of gazing by the experimenter as a cue for finding food, although after some training they learned to respond to pointing by hand. Direction of gaze is used by chimpanzees, however. Dogs (Canis familiaris) are believed to be sensitive to human gestural communication but their ability has never been formally tested. In three experiments we examined whether dogs can respond to cues given by humans. We found that dogs are able to utilize pointing, bowing, nodding, head-turning and glancing gestures of humans as cues for finding hidden food. Dogs were also able to generalize from one person (owner) to another familiar person (experimenter) in using the same gestures as cues. Baseline trials were run to test the possibility that odour cues alone could be responsible for the dogs’ performance. During training individual performance showed limited variability, probably because some dogs already “knew” some of the cues from their earlier experiences with humans. We suggest that the phenomenon of dogs responding to cues given by humans is better analysed as a case of interspecific communication than in terms of discrimination learning. Received: 30 May 1998 / Accepted after revision: 6 September 1998     

Children's understanding of communicative intentions in the middle of the second year of life

Two tasks were administered to 40 children aged from 16 to 20 months (mean age = 18;1), to evaluate children's understanding of declarative and informative intention [Behne, T., Carpenter, M., & Tomasello, M. (2005). One-year-olds comprehend the communicative intentions behind gestures in a hiding game. Developmental Science, 8, 492–499; Camaioni, L., Perucchini, P., Bellagamba, F., & Colonnesi, C. (2004). The role of declarative pointing in developing a theory of mind. Infancy, 5, 291–308]. In the first task, children had to respond to the experimenter who pointed at a distal object; in the second task, children had to find a toy in a hiding game after the experimenter indicated the correct location either by pointing or by gazing. In the first task, most children responded to the declarative gesture by “commenting” on the pointed object instead of just looking; however, looking responses were more frequent than commenting responses. In the second task, children chose the correct location of the object significantly more frequently when the informative gesture was the point than when it was the gaze; moreover, there were significantly more correct choices than incorrect choices in the point but not in the gaze condition. Finally, no significant relation was found between tasks. Taken together, the findings support the view that infants’ developing understanding of communicative intention is a complex process in which general cognitive abilities and contextual factors are equally important.     

Chimpanzees’ (Pan troglodytes) use of gaze cues in object-choice tasks: different methods yield different results

To assess the influence of different procedures on chimpanzees' performance in object-choice tasks, five adult chimpanzees were tested using three experimenter-given cues to food location: gazing, glancing, and pointing. These cues were delivered to the subjects in an identical fashion but were deployed within the context of two distinct meta-procedures that have been previously employed with this species with conflicting results. In one procedure, the subjects entered the test unit and approached the experimenter (who had already established the cue) on each trial. In the other procedure, the subjects stayed in the test unit throughout a session, witnessed the hiding procedure, and waited for a delay of 10 s during which the cue was provided. The subjects scored at high levels far exceeding chance in response to the gaze cue only when they approached the experimenter for each trial. They performed at chance levels when they stayed inside the test unit throughout the session. They scored at chance levels on all other cues irrespective of the procedure. These findings imply that (a) chimpanzees can immediately exploit social gaze cues, and (b) previous conflicting findings were likely due to the different meta-procedures that were used.     

Do chimpanzees know what others can and cannot do? Reasoning about ‘capability’

Much recent comparative work has been devoted to exploring what nonhuman primates understand about physical causality. However, few laboratory experiments have attempted to test what nonhumans understand about what physical acts others are capable of performing. We tested seven chimpanzees’ ability to predict which of two human experimenters could deliver a tray containing a food reward. In the ‘floor’ condition, legs were required to push the tray toward the subject. In the ‘lap’ condition, arms were required to hand the tray to the subject. In Exp. 1, chimpanzees begged (by gesturing) to either an experimenter whose legs were not visible (LNV) or whose arms were not visible (ANV). Rather than flexibly altering their preferences between conditions, the chimpanzees preferred the ANV experimenter regardless of the task. In subsequent experiments, we manipulated various factors that might have controlled the chimpanzees’ preferences, such as (a) distance between experimenter and subject (Experiment 2), (b) amount of occlusion of experimenters’ body (Experiments 2 and 3), (c) contact with the food tray (Experiments 3 and 4) and (d) positioning of barriers that either impeded the movement of the limbs or not (Experiment 5). The chimpanzees’ performance was best explained by attention to cues such as perceived proximity, contact, and maximal occlusion of body that although highly predictive in certain tasks, were irrelevant in others. When the discriminative role of such cues was eliminated, performance fell to chance levels, indicating that chimpanzees do not spontaneously (or after considerable training) use limb visibility as a cue to predict the ability of a human to perform particular physical tasks. Thus, the current findings suggest a possible failure of causal reasoning in the context of reasoning about the use of the limbs to perform physical acts.     

Chimpanzee (Pan troglodytes) intentional communication is not contingent upon food

Studies of great apes have revealed that they use manual gestures and other signals to communicate about distal objects. There is also evidence that chimpanzees modify the types of communicative signals they use depending on the attentional state of a human communicative partner. The majority of previous studies have involved chimpanzees requesting food items from a human experimenter. Here, these same communicative behaviors are reported in chimpanzees requesting a tool from a human observer. In this study, captive chimpanzees were found to gesture, vocalize, and display more often when the experimenter had a tool than when she did not. It was also found that chimpanzees responded differentially based on the attentional state of a human experimenter, and when given the wrong tool persisted in their communicative efforts. Implications for the referential and intentional nature of chimpanzee communicative signaling are discussed.     

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     

"Constructive" enumeration by chimpanzees (Pan troglodytes) on a computerized task

Two chimpanzees used a joystick to collect dots, one at a time, on a computer monitor (see video-clip in the electronic supplementary material), and then ended a trial when the number of dots collected was equal to the Arabic numeral presented for the trial. Both chimpanzees performed substantially and reliably above chance in collecting a quantity of dots equal to the target numeral, one chimpanzee for the numerals 1–7, and the second chimpanzee for the numerals 1–6. Errors that were made were seldom discrepant from the target by more than one dot quantity, and the perceptual process subitization was ruled out as an explanation for the performance. Additionally, analyses of trial duration data indicated that the chimpanzees were responding based on the numerosity of the constructed set rather than on the basis of temporal cues. The chimpanzees' decreasing performance with successively larger target numerals, however, appeared to be based on a continuous representation of magnitude rather than a discrete representation of number. Therefore, chimpanzee counting in this type of experimental task may be a process that represents magnitudes with scalar variability in that the memory for magnitudes associated with each numeral is imperfect and the variability of responses increases as a function of the numeral's value. Accepted after revision: 11 June 2001 Electronic Publication     

A simple but powerful test of perseverative search in dogs and toddlers

Perseverative (A-not-B) errors during the search of a hidden object were recently described in both dogs and 10-month-old infants. It was found that ostensive cues indicating a communicative intent of the person who hides the object played a major role in eliciting perseverative errors in both species. However, the employed experimental set-up gave rise to several alternative explanations regarding the source of these errors. Here we present a simplified protocol that eliminates the ambiguities present in the original design. Using five consecutive object hiding events to one of two locations in a fixed order (“AABBA”), we tested adult companion dogs and human children (24 months old). The experimenter performed the hiding actions while giving ostensive cues in each trial and moved the target object to the given location in a straight line. Our results show that in the B trials, both 24-month-old children and dogs could not reliably find the hidden object, and their performance in the first B trials was significantly below that of any of the A trials. These results are the first to show that the tendency for perseverative errors in an ostensive-communicative context is a robust phenomenon among 2-year-old children and dogs, and not the by-product of a topographically elaborate hiding event.     

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.     

Cues to food location that domestic dogs (Canis familiaris) of different ages do and do not use

The results of three experiments are reported. In the main study, a human experimenter presented domestic dogs (Canis familiaris) with a variety of social cues intended to indicate the location of hidden food. The novel findings of this study were: (1) dogs were able to use successfully several totally novel cues in which they watched a human place a marker in front of the target location; (2) dogs were unable to use the marker by itself with no behavioral cues (suggesting that some form of human behavior directed to the target location was a necessary part of the cue); and (3) there were no significant developments in dogs’ skills in these tasks across the age range 4 months to 4 years (arguing against the necessity of extensive learning experiences with humans). In a follow-up study, dogs did not follow human gaze into “empty space” outside of the simulated foraging context. Finally, in a small pilot study, two arctic wolves (Canis lupus) were unable to use human cues to locate hidden food. These results suggest the possibility that domestic dogs have evolved an adaptive specialization for using human-produced directional cues in a goal-directed (especially foraging) context. Exactly how they understand these cues is still an open question. Received: 28 April 2000 / Accepted after revision: 2 September 2000     

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.     

Chimpanzees (Pan troglodytes) remember the location of a hidden food item after altering their orientation to a spatial array

Two chimpanzees (Pan troglodytes) had a direct view of an experimenter placing a food item beneath one of several cups within a horizontal spatial array. The chimpanzees then were required to move around the spatial array, shifting their orientation to the array by 180 degrees . Both chimpanzees remembered the location of the food item. In the next experiment, a visual barrier was placed between the chimpanzees and the spatial array after the food item had been hidden to prevent visual tracking of the location of the object during the chimpanzees' movement. One chimpanzee remembered the location of the hidden item in this variation. These results demonstrate another capacity for spatial memory in this species that complements data indicating chimpanzee spatial memory for invisible displacements, array rotations, and array transpositions.     

One-year-olds’ understanding of nonverbal gestures directed to a third person

We investigated whether infants comprehend others’ nonverbal communicative intentions directed to a third person, in an ‘overhearing’ context. An experimenter addressed an assistant and indicated a hidden toy's location by either gazing ostensively or pointing to the location for her. In a matched control condition, the experimenter performed similar behaviors (absent-minded gazing and extended index finger) but did not communicate ostensively with the assistant. Infants could then search for the toy. Eighteen-month-old infants were skillful in using both communicative cues to find the hidden object, whereas 14-month-olds performed above chance only with the pointing cue. Neither age group performed above chance in the control condition. This study thus shows that by 14–18 months of age, infants are beginning to monitor and comprehend some aspects of third party interactions.     

Intentional behaviour in dog-human communication: an experimental analysis of “showing” behaviour in the dog

Despite earlier scepticism there is now evidence for simple forms of intentional and functionally referential communication in many animal species. Here we investigate whether dogs engage in functional referential communication with their owners. “Showing” is defined as a communicative action consisting of both a directional component related to an external target and an attention-getting component that directs the attention of the perceiver to the informer or sender. In our experimental situation dogs witness the hiding of a piece of food (or a favourite toy) which they cannot get access to. We asked whether dogs would engage in “showing” in the presence of their owner. To control for the motivational effects of both the owner and the food on the dogs’ behaviour, control observations were also staged where only the food (or the toy) or the owner was present. Dogs’ gazing frequency at both the food (toy) and the owner was greater when only one of these was present. In other words, dogs looked more frequently at their owner when the food (toy) was present, and they looked more at the location of the food (toy) when the owner was present. When both the food (toy) and the owner were present a new behaviour, “gaze alternation”, emerged which was defined as changing the direction of the gaze from the location of the food (toy) to looking at the owner (or vice versa) within 2 s. Vocalisations that occurred in this phase were always associated with gazing at the owner or the location of the food. This behaviour, which was specific to this situation, has also been described in chimpanzees, a gorilla and humans, and has often been interpreted as a form of functionally referential communication. Based on our observations we argue that dogs might be able to engage in functionally referential communication with their owner, and their behaviour could be described as a form of “showing”. The contribution of domestication and individual learning to the well-developed communicative skills in dogs is discussed and will be the subject of further studies. Received: 3 April 2000 / Accepted after revision: 2 September 2000     

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.     

Understanding communicative intentions and semiotic vehicles by children and chimpanzees

Developmental and comparative studies of the ability to understand communicative intentions using object-choice tasks raise questions concerning the semiotic properties of the communicative signals, and the roles of rearing histories, language and familiarity. We adapted a study by Tomasello, Call, and Gluckman (1997), in which a “helper” indicated the location of a hidden reward to children of three ages (18, 24, and 30 months) and to four chimpanzees, by means of one of four cues: Pointing, Marker, Picture and Replica. For the chimpanzees, we controlled for familiarity by using two helpers, one unfamiliar and one highly familiar. Even 18-months performed well on Pointing and Marker, while only the oldest group clearly succeeded with Picture and Replica. Performance did not correlate with scores for the Swedish Early Communicative Development Inventory (SECDI). While there were no positive results for the chimpanzees on the group level, and no effect of familiarity, two chimpanzees succeeded on Pointing and Marker. Results support proposals of a species difference in understanding communicative intentions, but also highlight the need to distinguish these from the complexity of semiotic vehicles and to consider both factors.     

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     

Tactics to obtain a hidden food item in chimpanzee pairs (Pan troglodytes)

Five dyads of chimpanzees were tested in a competitive situation, as a pilot study to examine chimpanzees' understanding of conspecifics' knowledge. A human experimenter baited one of five containers in an outdoor enclosure. Chimpanzee A (witness) could see where the food was hidden, while chimpanzee B (witness-of-witness) could not see the baited place but could observe the chimpanzee A watching the food being hidden. Then the two were released into the enclosure. This procedure was repeated for a certain number of days along with a control condition in which neither could see the baited location. The witness-of-witness developed tactics to forestall the witness in two pairs. The witness misled the witness-of-witness by taking a route to an empty container in several cases. These episodes might represent examples of deception. Tactics and counter-tactics thus developed through the interaction between the witness and the witness-of-witness, illustrating the high social intelligence of chimpanzees. An examination of the changes in tactics suggests a possibility that the witness-of-witness understands the witness's knowledge of the location of hidden food. Accepted after revision: 22 May 2001 Electronic Publication