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     

Domestic dogs (Canis familiaris) use a physical marker to locate hidden food

Dogs can use the placement of an arbitrary marker to locate hidden food in an object-choice situation. We tested domestic dogs (Canis familiaris) in three studies aimed at pinning down the relative contributions of the human’s hand and the marker itself. We baited one of two cups (outside of the dogs’ view) and gave the dog a communicative cue to find the food. Study 1 systematically varied dogs’ perceptual access to the marker placing event, so that dogs saw either the whole human, the hand only, the marker only, or nothing. Follow-up trials investigated the effect of removing the marker before the dog’s choice. Dogs used the marker as a communicative cue even when it had been removed prior to the dog’s choice and attached more importance to this cue than to the hand that placed it although the presence of the hand boosted performance when it appeared together with the marker. Study 2 directly contrasted the importance of the hand and the marker and revealed that the effect of the marker diminished if it had been associated with both cups. In contrast touching both cups with the hand had no effect on performance. Study 3 investigated whether the means of marker placement (intentional or accidental) had an effect on dogs’ choices. Results showed that dogs did not differentiate intentional and accidental placing of the marker. These results suggest that dogs use the marker as a genuine communicative cue quite independently from the experimenter’s actions.     

Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus)

Sixteen domestic dogs (Canis familiaris) and four horses (Equus caballus) were tested for their ability to use human-given manual and facial cues in an object-choice task. Two of the four horses used touch as a cue and one horse successfully used pointing. The performance of the dogs was considerably better, with 12 subjects able to use pointing as a cue, 4 able to use head orientation and 2 able to use eye gaze alone. Group analysis showed that the dogs performed significantly better in all experimental conditions than during control trials. Dogs were able to use pointing cues even when the cuer’s body was closer to the incorrect object. Working gundogs with specialised training used pointing more successfully than pet dogs and gundog breeds performed better than non-gundog breeds. The results of this experiment suggest that animals’ use of human given communicative signals depends on cognitive ability, the evolutionary consequences of domestication and enculturation by humans within the individual’s lifetime. Received: 15 July 1999 / Accepted after revision: 10 January 2000     

Making inferences about the location of hidden food: social dog, causal ape

Domestic dogs (Canis familiaris) and great apes from the genus Pan were tested on a series of object choice tasks. In each task, the location of hidden food was indicated for subjects by some kind of communicative, behavioral, or physical cue. On the basis of differences in the ecologies of these 2 genera, as well as on previous research, the authors hypothesized that dogs should be especially skillful in using human communicative cues such as the pointing gesture, whereas apes should be especially skillful in using physical, causal cues such as food in a cup making noise when it is shaken. The overall pattern of performance by the 2 genera strongly supported this social-dog, causal-ape hypothesis. This result is discussed in terms of apes' adaptations for complex, extractive foraging and dogs' adaptations, during the domestication process, for cooperative communication with 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     

Can domestic dogs (Canis familiaris) use referential emotional expressions to locate hidden food?

Although many studies have investigated domestic dogs’ (Canis familiaris) use of human communicative cues, little is known about their use of humans’ emotional expressions. We conducted a study following the general paradigm of Repacholi in Dev Psychol 34:1017–1025, (1998) and tested four breeds of dogs in the laboratory and another breed in the open air. In our study, a human reacted emotionally (happy, neutral or disgust) to the hidden contents of two boxes, after which the dog was then allowed to choose one of the boxes. Dogs tested in the laboratory distinguished between the most distinct of the expressed emotions (Happy–Disgust condition) by choosing appropriately, but performed at chance level when the two emotions were less distinct (Happy–Neutral condition). The breed tested in the open air passed both conditions, but this breed’s differing testing setup might have been responsible for their success. Although without meaningful emotional expressions, when given a choice, these subjects chose randomly, their performance did not differ from that in the experimental conditions. Based on the findings revealed in the laboratory, we suggest that some domestic dogs recognize both the directedness and the valence of some human emotional expressions.     

Pointing gestures modulate domestic dogs’ search behavior for hidden objects in a spatial rotation problem

In the spatial domain, domestic dogs are highly inclined to search at the last location where they saw an object disappear and cannot infer that a hidden object has moved imperceptibly from one location to another. In the current study, we examined whether exposure to human social cues modulates dogs’ search behavior for hidden objects. In Experiment 1, twenty dogs were first trained to find an object they saw disappear inside a stationary container in the presence (social group) or absence (non-social group) of pointing gestures. In tests, the containers were rotated 180° around a central axis. The dogs in the non-social group systematically searched at the initial (now incorrect) hiding location, whereas the dogs in the social group chose correctly significantly above chance. In Experiment 2, we tested whether pre-exposure to human pointing has an impact on dogs’ use of gestures. No gestures were given during training and both the social and non-social conditions were administered to each of the ten dogs. In contrast to Experiment 1, the performance of dogs in the social condition dropped significantly and varied substantially from one dog to another. Overall, this study suggests that dogs’ tendency to use human signals is so strong that it even outweighs their spatial bias to search where they saw an object disappear; however, this penchant to use human gestures appears to be dependent on the degree of familiarity of the dog with these signals.     

A comparative study of the use of visual communicative signals in interactions between dogs (Canis familiaris) and humans and cats (Felis catus) and humans

Dogs' (Canis familiaris) and cats' (Felis catus) interspecific communicative behavior toward humans was investigated. In Experiment 1, the ability of dogs and cats to use human pointing gestures in an object-choice task was compared using 4 types of pointing cues differing in distance between the signaled object and the end of the fingertip and in visibility duration of the given signal. Using these gestures, both dogs and cats were able to find the hidden food; there was no significant difference in their performance. In Experiment 2, the hidden food was made inaccessible to the subjects to determine whether they could indicate the place of the hidden food to a naive owner. Cats lacked some components of attention-getting behavior compared with dogs. The results suggest that individual familiarization with pointing gestures ensures high-level performance in the presence of such gestures; however, species-specific differences could cause differences in signaling toward the human.     

Spatial memory of domestic dogs (Canis familiaris) for hidden objects in a detour task

Spatial memory of domestic dogs (Canis familiaris) for hidden objects was investigated via a visible displacement problem of object permanence with a detour paradigm. Experiment 1 showed that dogs were able to spontaneously locate a disappearing object in a detour situation. In Experiments 2 and 3, dead reckoning and allocentric spatial information were put in conflict. Results revealed that dogs simultaneously encoded both sources of information when they had to bypass an obstacle to locate a hidden object. Experiment 3 also revealed that, over the course of testing, dogs gradually learned to rely predominantly on allocentric cues when the detour involved several reorientations. The current study reveals that spatial memory of dogs for hidden objects in a detour task was guided by flexibility in processing spatial information. Dogs could simultaneously encode dead reckoning and allocentric information to locate a disappearing object and used them hierarchically according to the complexity of the detour they encountered in the environment.     

Visual perspective taking by dogs (Canis familiaris) in a Guesser–Knower task: evidence for a canine theory of mind?

We tested domestic dogs (N = 16) in a Guesser–Knower task in which they chose between possible locations for hidden food indicated by human informants. In four experiments, the perceptual access of the Guesser and Knower to the hidden food baiting was manipulated. When informants had differing perceptual access to the baiting, dogs preferred the location indicated by the Knower from the start of testing (Experiment 1), even when baiting was done by a third experimenter (Experiments 2–3). However, when there was no difference in perceptual access and both informants either knew or did not know the food location, dogs had no preference between the informants (Experiment 4). Controls ruled out alternative explanations in terms of associative learning, unintentional and olfactory cues. Analysis of individual data showed no significant heterogeneity across dogs, and results were not correlated with age or sex. Dogs’ performances were superior to those of nonhuman primates in previous studies. Although a mentalistic explanation is not required, results add to evidence that dogs have a remarkable sensitivity to cues related to humans’ attentional state, which enables them to respond as if they had a functional theory of mind in the Guesser–Knower task with human informants.     

Colour cues or spatial cues? Context-dependent preferences in the European greenfinch (<Emphasis Type="Italic">Carduelis chloris</Emphasis>)

Using featural cues such as colour to identify ephemeral food can increase foraging efficiency. Featural cues may change over time however; therefore, animals should use spatial cues to relocate food that occurs in a temporally stable position. We tested this hypothesis by measuring the cue preferences of captive greenfinches Carduelis chloris when relocating food hidden in a foraging tray. In these standardised associative learning trials, greenfinches favoured colour cues when returning to a foraging context that they had encountered before only once (“one-trial test”) but switched to spatial cues when they had encountered that scenario on ten previous occasions (“repeated-trial test”). We suggest that repeated encounters generated a context in which individuals had a prior expectation of temporal stability, and hence context-dependent cue selection. Next, we trained birds to find food in the absence of colour cues but tested them in the presence of visual distracters. Birds were able to learn spatial cues after one encounter, but only when visual distracters were identical in colouration. When a colourful distracter was present in the test phase, cue selection was random. Unlike the first one-trial test, birds were not biased towards this colourful visual distracter. Together, these results suggest that greenfinches are able to learn both cue types, colour cue biases represent learning, not simply distraction, and spatial cues are favoured over colour cues only in temporally stable contexts.     

Does affective information influence domestic dogs’ (<Emphasis Type="Italic">Canis lupus familiaris</Emphasis>) point-following behavior?

Several studies have examined dogs’ (Canis lupus familiaris) comprehension and use of human communicative cues. Relatively few studies have, however, examined the effects of human affective behavior (i.e., facial and vocal expressions) on dogs’ exploratory and point-following behavior. In two experiments, we examined dogs’ frequency of following an adult’s pointing gesture in locating a hidden reward or treat when it occurred silently, or when it was paired with a positive or negative facial and vocal affective expression. Like prior studies, the current results demonstrate that dogs reliably follow human pointing cues. Unlike prior studies, the current results also demonstrate that the addition of a positive affective facial and vocal expression, when paired with a pointing gesture, did not reliably increase dogs’ frequency of locating a hidden piece of food compared to pointing alone. In addition, and within the negative facial and vocal affect conditions of Experiment 1 and 2, dogs were delayed in their exploration, or approach, toward a baited or sham-baited bowl. However, in Experiment 2, dogs continued to follow an adult’s pointing gesture, even when paired with a negative expression, as long as the attention-directing gesture referenced a baited bowl. Together these results suggest that the addition of affective information does not significantly increase or decrease dogs’ point-following behavior. Rather these results demonstrate that the presence or absence of affective expressions influences a dogs’ exploratory behavior and the presence or absence of reward affects whether they will follow an unfamiliar adult’s attention-directing gesture.     

Minding the gap: spatial perseveration error in dogs

We investigated a combination of perseveration and detour behaviour in 50 domestic dogs (Canis familiaris). They were required to make a detour through a gap at one end of a straight barrier in order to reach a target. After one, two, three or four repeats, the gap was moved to the opposite end of the barrier, and the detour behaviour of the dogs was recorded. Although the dogs could solve simple detour tasks (80% correct in the first trial), they committed a perseveration error of following the previously learned route despite the clearly visible change in the location of the gap. This ‘misbehaviour’ occurred in 29 of 30 dogs after only two learning trials. They never reached a 100% correct performance level again even after four runs through the second gap location. The results suggest that dogs are reluctant to unlearn acquired spatial motor responses and reinforced navigation, which has important implications for experimental design, everyday dog training and our understanding of their mental capacities.     

Landmark-based search memory in the domestic dog (Canis familiaris)

Recent studies have suggested that any animal that relies on landmark-based search memory encodes and uses metric properties of space to navigate. So far, however, metric information provided by landmarks has been predominantly investigated in avian species. In the present study, I investigated whether the domestic dog (Canis familiaris), a mammalian species, encodes the distance and direction from landmarks. Dogs were trained to find a ball hidden next to an array of two distinct landmarks that remained at a constant location in a room from trial to trial. After training, the dogs were occasionally tested on unrewarded conditions where the array was either left in its usual position or shifted laterally, perpendicularly, or diagonally relative to the rear wall of the room. Although the dogs significantly shifted their search as a function of the displacement of the landmarks, they did not search at the predicted coordinates of the goal relative to the shift of the landmarks, suggesting that the global cues available in the testing room were also encoded and used by dogs to locate the position of the goal.     

Motivation and memory in zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>) foraging behavior

Remembering combinations of information such as what resources have been seen in which locations could play an important role in enhancing individual survival through increased foraging success. To date, there have been relatively few investigations of avian memory involving more than one category of information. This study explored zebra finches’ (Taeniopygia guttata) capacity to recall two categories in combination, namely food-type and spatial location. Birds were trained to remove variously weighted flaps to find two types of food hidden beneath. Memory for food-types and locations was assessed by pre-feeding the birds to satiety on and devaluing one food-type, and then testing the birds’ efficiency at finding the non-devalued food. When allowed one trial to learn locations of two food rewards that were hidden beneath lightly weighted flaps, birds performed better than chance at locating a food reward. However, they did not preferentially search for the non pre-fed food, suggesting that they were unable to recall both food type and location in combination. Zebra finches made fewer errors when tested on the one-trial task using more heavily weighted flaps than with lightly weighted flaps; there was equivocal evidence that they remembered which food type was hidden where on this task. When given repeated exposures to the locations of the two food rewards, finches located a food reward more accurately than on the one-trial tasks, and were also more likely to recall the locations of the different food types. In this foraging paradigm, experience and motivation may have influenced the birds’ performance.     

Domestic dogs (Canis familiaris) use human gestures but not nonhuman tokens to find hidden food

The authors examined the ability of domestic dogs to use human body cues (gestures) and equivalent-sized nonhuman cues to find hidden food in an object choice paradigm. In Experiment 1 the authors addressed the importance of the human element of the cue, and the effects of size, topography, and familiarity on dogs' success in using cues. Experiment 2 further explored the role of the human as cue-giver, and the impact of a change in the experimenter's attentional state during cue presentation. This included a systematic test of the role inanimate tokens play as cues apart from human placement. Our results indicate that dogs are more sensitive to human cues than equivalent nonhuman cues, and that the size of the cue is a critical element in determining dogs' success in following it.     

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.     

Prospective object search in dogs: mixed evidence for knowledge of <Emphasis Type="Italic">What</Emphasis> and <Emphasis Type="Italic">Where</Emphasis>

We investigated whether two dogs that had been specially trained to retrieve objects by their names were able to integrate information about the identity (What) as well as the location (Where) of those objects so that they could plan their search accordingly. In a first study, two sets of objects were placed in two separate rooms and subjects were asked to retrieve the objects, one after the other. Both dogs remembered the identity of the objects as they reliably retrieved the correct objects. One of the dogs was also able to integrate information about the object’s location as he chose the correct location in which the object had been placed. Further investigation of the second dog’s behavior revealed that she followed a more stereotyped search strategy. Despite this variation in performance, this study provides evidence for the memory of What and Where in a domestic dog and shows the prospective use of such information in a search task.     

Effect of training and familiarity on responsiveness to human cues in domestic dogs (Canis familiaris)

Domestic dogs (Canis familiaris) seem to possess an evolved competency to follow human-given cues, often out-performing their wild progenitor the wolf (Canis lupus) on cue-following tasks. However, domestication may not be solely responsible for the socio-cognitive skills of dogs, with ontogenetic experience also playing a role. This research evaluated the effects of intensive training on cue-following behaviour using an unreinforced object-choice paradigm. The responses of dogs that were trained to competitive levels were compared to those of pet dogs with only basic training, and dogs living in an animal shelter that demonstrated no or only rudimentary following of basic commands. Using a cue-following task where three types of cues were presented by familiar and unfamiliar human partners, the number of cues followed by each training group were recorded. All dogs found cues where gesture was combined with a congruent head and eye movement easier to follow than either gesture or eye gaze alone. Whether the cue-giver was familiar or not had a significant effect on number of cues followed in homed dogs, and the performance of shelter dogs was comparable to the other groups when faced with an unfamiliar cue-giver. Contrary to predictions, level of training did not improve performance on the cue-following task. This work does provide support for the presence of an evolved adaptation to exploit social cues provided by humans that can be augmented by familiarity with the cue giver. However, additional joint activity as experienced in an intensive training regime does not seem to increase accuracy in following human-given cues.     

Visual categorization of natural stimuli by domestic dogs

One of the fundamental issues in the study of animal cognition concerns categorization. Although domestic dogs (Canis familiaris) are on the brink to become one of the model animals in animal psychology, their categorization abilities are unknown. This is probably largely due to the absence of an adequate method for testing dogs’ ability to discriminate between large sets of pictures in the absence of human cueing. Here we present a computer-automated touch-screen testing procedure, which enabled us to test visual discrimination in dogs while social cueing was ruled out. Using a simultaneous discrimination procedure, we first trained dogs (N = 4) to differentiate between a set of dog pictures (N = 40) and an equally large set of landscape pictures. All subjects learned to discriminate between the two sets and showed successful transfer to novel pictures. Interestingly, presentation of pictures providing contradictive information (novel dog pictures mounted on familiar landscape pictures) did not disrupt performance, which suggests that the dogs made use of a category-based response rule with classification being coupled to category-relevant features (of the dog) rather than to item-specific features (of the background). We conclude that dogs are able to classify photographs of natural stimuli by means of a perceptual response rule using a newly established touch-screen procedure. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.