Behavioral cues that great apes use to forage for hidden food

We conducted three studies to examine whether the four great ape species (chimpanzees, bonobos, gorillas, and orangutans) are able to use behavioral experimenter-given cues in an object-choice task. In the subsequent experimental conditions subjects were presented with two eggs, one of which contained food and the other did not. In Study 1 the experimenter examined both eggs by smelling or shaking them, but only made a failed attempt to open (via biting) the egg containing food. In a control condition, the experimenter examined and attempted to open both eggs, but in reverse order to control for stimulus enhancement. The apes significantly preferred the egg that was first examined and then bitten, but had no preference in a baseline condition in which there were no cues. In Study 2, we investigated whether the apes could extend this ability to cues not observed in apes so far (i.e., attempting to pull apart the egg), as well as whether they made this discrimination based on the function of the action the experimenter performed. Subjects significantly preferred eggs presented with this novel cue, but did not prefer eggs presented with a novel but functionally irrelevant action. In Study 3, apes did not interpret human actions as cues to food-location when they already knew that the eggs were empty. Thus, great apes were able to use a variety of experimenter-given cues associated with foraging actions to locate hidden food and thereby were partially sensitive to the general purpose underlying these actions.     

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.     

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.     

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.     

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     

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.     

Great apes infer others’ goals based on context

In previous studies claiming to demonstrate that great apes understand the goals of others, the apes could potentially have been using subtle behavioral cues present during the test to succeed. In the current studies, we ruled out the use of such cues by making the behavior of the experimenter identical in the test phase of both the experimental and control conditions; the only difference was the preceding “context.” In the first study, apes interpreted a human’s ambiguous action as having the underlying goal of opening a box, or not, based on that human’s previous actions with similar boxes. In the second study, chimpanzees learned that when a human stood up she was going to go get food for them, but when a novel, unexpected event happened, they changed their expectation—presumably based on their understanding that this new event led the human to change her goal. These studies suggest that great apes do not need concurrent behavioral cues to infer others’ goals, but can do so from a variety of different types of cues—even cues displaced in time.     

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.     

Bonobos, chimpanzees, gorillas, and orang utans use feature and spatial cues in two spatial memory tasks

Animals commonly use feature and spatial strategies when remembering places of interest such as food sources or hiding places. We conducted three experiments with great apes to investigate strategy preferences and factors that may shape them. In the first experiment, we trained 17 apes to remember 12 different food locations on the floor of their sleeping room. The 12 food locations were associated with one feature cue, so that feature and spatial cues were confounded. In a single test session, we brought the cues into conflict and found that apes, irrespective of species, showed a preference for a feature strategy. In the second experiment, we used a similar procedure and trained 25 apes to remember one food location on a platform in front of them. On average, apes preferred to use a feature strategy but some individuals relied on a spatial strategy. In the final experiment, we investigated whether training might influence strategy preferences. We tested 21 apes in the platform set-up and found that apes used both, feature and spatial strategies irrespective of training. We conclude that apes can use feature and spatial strategies to remember the location of hidden food items, but that task demands (e.g. different numbers of search locations) can influence strategy preferences. We found no evidence, however, for the role of training in shaping these preferences.     

Reorientation in a two-dimensional environment: II. Do pigeons (Columba livia) encode the featural and geometric properties of a two-dimensional schematic of a room?

Pigeons (Columba livia) searched for a hidden target area in images showing a schematic rectangular environment. The absolute position of the goal varied across trials but was constant relative to distinctive featural cues and geometric properties of the environment. Pigeons learned to use both of these properties to locate the goal. Transformation tests showed that pigeons could use either the color or shape of the features, but performance was better with color cues present. Pigeons could also use a single featural cue at an incorrect corner to distinguish between the correct corner and the geometrically equivalent corner; this indicates that they did not simply use the feature at the correct corner as a beacon. Interestingly, pigeons that were trained with features spontaneously encoded geometry. The encoded geometric information withstood vertical translations but not orientation transformations.     

Reorienting in images of a three-dimensional environment

Adult humans searched for a hidden goal in images depicting 3-dimensional rooms. Images contained either featural cues, geometric cues, or both, which could be used to determine the correct location of the goal. In Experiment 1, participants learned to use featural and geometric information equally well. However, men and women showed significant differences in their use of distant featural cues and the spontaneous encoding of geometric information when trained with features present. Transformation tests showed that participants could use either the color or the shape of the features independently to locate the goal. Experiment 2 showed that participants could use either configural or surface geometry when searching for the goal. However, their weighing of these geometric cues was dependent on initial training experience.     

Taï chimpanzees anticipate revisiting high-valued fruit trees from further distances

The use of spatio-temporal memory has been argued to increase food-finding efficiency in rainforest primates. However, the exact content of this memory is poorly known to date. This study investigated what specific information from previous feeding visits chimpanzees (Pan troglodytes verus), in Taï National Park, Côte d’Ivoire, take into account when they revisit the same feeding trees. By following five adult females for many consecutive days, we tested from what distance the females directed their travels towards previously visited feeding trees and how previous feeding experiences and fruit tree properties influenced this distance. To exclude the influence of sensory cues, the females’ approach distance was measured from their last significant change in travel direction until the moment they entered the tree’s maximum detection field. We found that chimpanzees travelled longer distances to trees at which they had previously made food grunts and had rejected fewer fruits compared to other trees. In addition, the results suggest that the chimpanzees were able to anticipate the amount of fruit that they would find in the trees. Overall, our findings are consistent with the hypothesis that chimpanzees act upon a retrieved memory of their last feeding experiences long before they revisit feeding trees, which would indicate a daily use of long-term prospective memory. Further, the results are consistent with the possibility that positive emotional experiences help to trigger prospective memory retrieval in forest areas that are further away and have fewer cues associated with revisited feeding trees.     

Landmark use by Clark’s nutcrackers (Nucifraga columbiana): influence of disorientation and cue rotation on distance and direction estimates

Many species have been shown to encode multiple sources of information to orient. To examine what kinds of information animals use to locate a goal we manipulated cue rotation, cue availability, and inertial orientation when the food-storing Clark’s nutcracker (Nucifraga columbiana) was searching for a hidden goal in a circular arena. Three groups of birds were used, each with a different goal–landmark distance. As the distance between the goal and the landmark increased, nutcrackers were less accurate in finding the correct direction to the goal than they were at estimating the distance (Experiment 1). To further examine what cues the birds were using to calculate direction, the featural cues within the environment were rotated by 90° and the birds were either oriented when searching (Experiments 2 and 3) or disoriented (Experiment 3). In Experiment 4, all distinctive visual cues were removed (both internal and external to the environment), a novel point of entry was used and the birds were either oriented or disoriented. We found that disorienting the nutcrackers so that they could not use inertial cues did not influence the birds’ total search error. The birds relied heavily but not completely on cues within the environment, as rotating available cues caused them to systematically shift their search behavior. In addition, the birds also relied to some extent on Earth-based cues. These results show the flexible nature of cue use by the Clark’s nutcracker. Our study shows how multiple sources of spatial information may be important for extracting multiple bearings for navigation.     

Gorillas’ (Gorilla gorilla) use of experimenter-given manual and facial cues in an object-choice task

Several experiments have been performed to examine the great apes’ use of experimenter-given manual and visual cues in object-choice tasks. Considering their use of referential gestures in gaze-following paradigms, great apes perform surprisingly unsuccessfully in object-choice tasks. However, the large majority of object-choice experiments have been conducted with chimpanzees (Pan troglodytes) with very few experiments including other great ape species, making it difficult to generalize about the great apes. Interestingly, the only object-choice task conducted with gorillas (Gorilla gorilla) has indicated successful use of both manual and visual cues. It was the aim of the present study to gather more data on gorillas’ use of human manual and facial cues on the object-choice task. Gorilla subjects in this study did not show consistent use of three types of referential cues.     

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     

Sensory information and associative cues used in food detection by wild vervet monkeys

Understanding animals’ spatial perception is a critical step toward discerning their cognitive processes. The spatial sense is multimodal and based on both the external world and mental representations of that world. Navigation in each species depends upon its evolutionary history, physiology, and ecological niche. We carried out foraging experiments on wild vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda, to determine the types of cues used to detect food and whether associative cues could be used to find hidden food. Our first and second set of experiments differentiated between vervets’ use of global spatial cues (including the arrangement of feeding platforms within the surrounding vegetation) and/or local layout cues (the position of platforms relative to one another), relative to the use of goal-object cues on each platform. Our third experiment provided an associative cue to the presence of food with global spatial, local layout, and goal-object cues disguised. Vervets located food above chance levels when goal-object cues and associative cues were present, and visual signals were the predominant goal-object cues that they attended to. With similar sample sizes and methods as previous studies on New World monkeys, vervets were not able to locate food using only global spatial cues and local layout cues, unlike all five species of platyrrhines thus far tested. Relative to these platyrrhines, the spatial location of food may need to stay the same for a longer time period before vervets encode this information, and goal-object cues may be more salient for them in small-scale space.     

Why cast shadows are expendable: insensitivity of human observers and the inherent ambiguity of cast shadows in pictorial art

The kinds of visual cues artists choose to use or not use in their work can offer insight into perceptual processes. On the basis of the observed paucity of the use of cast shadow in pictorial art, we hypothesized that cast shadows might be relatively expendable as pictorial cues. In this study, we investigated two potential reasons for this expendability: first, viewers might be insensitive to much of the information that cast shadows provide; and, second, ambiguities about what is shadow and what is pigment can often be resolved only through motion-something that static media are ill-equipped to deal with. In experiment 1, we used a visual-search paradigm in which viewers had to determine if there were odd cast shadows in sets of 4, 8, 16, and 32 objects. In experiment 2, viewers had to discriminate between shadow/pigment ambiguities in both still and moving images. Our results demonstrate that viewers are neither particularly sensitive to static cast-shadow incongruities, nor are they able to disambiguate cast shadow from pigment without continuous motion information. Taken together, these results may help explain why cast shadows are relatively rare in static pictorial work.     

Chimpanzee (Pan troglodytes) spatial problem solving with the use of mirrors and televised equivalents of mirrors

Two adult male chimpanzees reached through a hole in the wall of their home cage and, by tracking the images of their hands and of an otherwise hidden target object in a mirror or closed-circuit television picture, moved their hands in whichever direction was necessary to make contact with the target object. They discriminated between live video images and tapes and performed effectively when the target objects were presented in novel locations and when the video picture was presented at random in different orientations. There was thus no consistent relation between the location of images on the monitor and the location of their real-world counterparts. Comparable performances in monkeys and nonprimates seem unlikely.     

Tests for cognitive mapping in Clark's nutcrackers (Nucifraga columbiana)

In these experiments, the authors examined the nature of the spatial information that Clark's nutcrackers (Nucifraga columbiana) use during navigation and whether this information is represented in the form of a cognitive map. In Experiment 1, nutcrackers were able to use distal cues to locate a small hidden goal. In Experiments 2 and 3, nutcrackers were given the opportunity to develop a map of a room by viewing local subsets of the landmarks in the room at a goal during training. During transfer tests, nutcrackers were presented with a landmark panorama that was not previously seen at the goal. Of 3 nutcrackers that had learned the relationship between distal cues and the goal, 3 were able to locate the goal during transfer, indicating they may have developed a cognitive map. Experiments 4 and 5 suggest that the simpler mechanism of vector integration may have been used by some nutcrackers during the transfer tests.     

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