Domestic Dogs Use Contextual Information and Tone of Voice when following a Human Pointing Gesture

Domestic dogs are skillful at using the human pointing gesture. In this study we investigated whether dogs take contextual information into account when following pointing gestures, specifically, whether they follow human pointing gestures more readily in the context in which food has been found previously. Also varied was the human''s tone of voice as either imperative or informative. Dogs were more sustained in their searching behavior in the ‘context’ condition as opposed to the ‘no context’ condition, suggesting that they do not simply follow a pointing gesture blindly but use previously acquired contextual information to inform their interpretation of that pointing gesture.Dogs also showed more sustained searching behavior when there was pointing than when there was not, suggesting that they expect to find a referent when they see a human point. Finally, dogs searched more in high-pitched informative trials as opposed to the low-pitched imperative trials, whereas in the latter dogs seemed more inclined to respond by sitting. These findings suggest that a dog''s response to a pointing gesture is flexible and depends on the context as well as the human''s tone of voice.     

Dogs’ Eavesdropping from People’s Reactions in Third Party Interactions

Eavesdropping involves the acquisition of information from third-party interactions, and can serve to indirectly attribute reputation to individuals. There is evidence on eavesdropping in dogs, indicating that they can develop a preference for people based on their cooperativeness towards others. In this study, we tested dogs’ eavesdropping abilities one step further. In a first experiment, dogs could choose between cooperative demonstrators (the donors) who always gave food to an approaching third person (the beggar); here, the only difference between donors was whether they received positive or negative reactions from the beggar (through verbal and gestural means). Results showed that dogs preferentially approached the donor who had received positive reactions from the beggar. By contrast, two different conditions showed that neither the beggar’s body gestures nor the verbal component of the interaction on their own were sufficient to affect the dogs’ preferences. We also ran two further experiments to test for the possibility of dogs’ choices being driven by local enhancement. When the donors switched places before the choice, dogs chose at random. Similarly, in a nonsocial condition in which donors were replaced by platforms, subjects chose at chance levels. We conclude that dogs’ nonrandom choices in the present protocol relied on the simultaneous presence of multiple cues, such as the place where donors stood and several features of the beggar’s behavior (gestural and verbal reactions, and eating behavior). Nonetheless, we did not find conclusive evidence that dogs discriminated the donors by their physical features, which is a prerequisite of reputation attribution.     

What Are You or Who Are You? The Emergence of Social Interaction between Dog and an Unidentified Moving Object (UMO)

Robots offer new possibilities for investigating animal social behaviour. This method enhances controllability and reproducibility of experimental techniques, and it allows also the experimental separation of the effects of bodily appearance (embodiment) and behaviour. In the present study we examined dogs’ interactive behaviour in a problem solving task (in which the dog has no access to the food) with three different social partners, two of which were robots and the third a human behaving in a robot-like manner. The Mechanical UMO (Unidentified Moving Object) and the Mechanical Human differed only in their embodiment, but showed similar behaviour toward the dog. In contrast, the Social UMO was interactive, showed contingent responsiveness and goal-directed behaviour and moved along varied routes. The dogs showed shorter looking and touching duration, but increased gaze alternation toward the Mechanical Human than to the Mechanical UMO. This suggests that dogs’ interactive behaviour may have been affected by previous experience with typical humans. We found that dogs also looked longer and showed more gaze alternations between the food and the Social UMO compared to the Mechanical UMO. These results suggest that dogs form expectations about an unfamiliar moving object within a short period of time and they recognise some social aspects of UMOs’ behaviour. This is the first evidence that interactive behaviour of a robot is important for evoking dogs’ social responsiveness.     

Are Dogs Able to Communicate with Their Owners about a Desirable Food in a Referential and Intentional Way?

The ability of dogs to use human communicative signals has been exhaustively studied. However, few studies have focused on the production of communicative signals by dogs. The current study investigated if dogs are able to communicate by using directional signals towards some desirable object in the environment and also if they show an apparent intention to manipulate their owner’s behavior in order to receive it. Some operational criteria were used to investigate referential and intentional communication: the signal should be influenced by the audience and by the recipient’s direction of visual attention; the sender should display gaze alternations between the recipient and the object and attention-getting behaviors, and, finally, the sender should persist and elaborate the communication when attempts to manipulate the recipient failed. Aiming to investigate these criteria in dogs, 29 subjects were tested using an experimental set up in which they could see a desirable but unreachable food and they needed the cooperation of their owners in order to receive it. This study found evidence of all operational criteria, especially for gaze alternation between the owner and the food, which suggested that some dogs’ communicative behaviors could be functionally referential and intentional. Nevertheless, similar to other studies about social cognition in animals, it is not possible to distinguish if the dog’s behaviors are based on simple mechanisms or on a theory of mind about their owners.     

Adapting to the human world: Dogs’ responsiveness to our social cues

Dogs are more skilful than a host of other species at tasks which require they respond to human communicative gestures in order to locate hidden food. Four basic interpretations for this proficiency surface from distilling the research findings. One possibility is that dogs simply have more opportunity than other species to learn to be responsive to human social cues. A different analysis suggests that the domestication process provided an opening for dogs to apply general cognitive problem-solving skills to a novel social niche. Some researchers go beyond this account and propose that dogs’ co-evolution with humans equipped them with a theory of mind for social exchanges. Finally, a more prudent approach suggests that sensitivity to the behaviours of both humans and conspecifics would be particularly advantageous for a social scavenger like the dog. A predisposition to attend to human actions allows for rapid early learning of the association between gestures and the availability of food.     

An Investigation on Social Representations: Inanimate Agent Can Mislead Dogs (Canis familiaris) in a Food Choice Task

The nature of mental representation of others plays a crucial role in social interactions. Dogs present an ideal model species for the investigation of such mental representations because they develop social ties with both conspecifics and heterospecifics. Former studies found that dogs’ preference for larger food quantity could be reversed by humans who indicate the smaller quantity. The question is whether this social bias is restricted to human partners. We suggest that after a short positive social experience, an unfamiliar moving inanimate agent (UMO) can also change dogs’ choice between two food quantities. We tested four groups of dogs with different partners: In the (1) Helper UMO and (2) Helper UMO Control groups the partner was an interactive remote control car that helped the dog to obtain an otherwise unreachable food. In the (3) Non-helper UMO and (4) Human partner groups dogs had restricted interaction with the remote control car and the unfamiliar human partners. In the Human partner, Helper UMO and Helper UMO Control groups the partners were able to revert dogs’ choice for the small amount by indicating the small one, but the Non-helper UMO was not. We suggest that dogs are able to generalize their wide range of experiences with humans to another type of agent as well, based on the recognition of similarities in simple behavioural patterns.     

Dog’s Discrimination of Human Selfish and Generous Attitudes: The Role of Individual Recognition,Experience, and Experimenters’ Gender

Discrimination of and memory for others’ generous and selfish behaviors could be adaptive abilities in social animals. Dogs have seemingly expressed such skills in both direct and indirect interactions with humans. However, recent studies suggest that their capacity may rely on cues other than people’s individual characteristics, such as the place where the person stands. Thus, the conditions under which dogs recognize individual humans when solving cooperative tasks still remains unclear. With the aim of contributing to this problem, we made dogs interact with two human experimenters, one generous (pointed towards the food, gave ostensive cues, and allowed the dog to eat it) and the other selfish (pointed towards the food, but ate it before the dog could have it). Then subjects could choose between them (studies 1-3). In study 1, dogs took several training trials to learn the discrimination between the generous and the selfish experimenters when both were of the same gender. In study 2, the discrimination was learned faster when the experimenters were of different gender as evidenced both by dogs’ latencies to approach the bowl in training trials as well as by their choices in preference tests. Nevertheless, dogs did not get confused by gender when the experimenters were changed in between the training and the choice phase in study 3. We conclude that dogs spontaneously used human gender as a cue to discriminate between more and less cooperative experimenters. They also relied on some other personal feature which let them avoid being confused by gender when demonstrators were changed. We discuss these results in terms of dogs’ ability to recognize individuals and the potential advantage of this skill for their lives in human environments.     

Aggressive Bimodal Communication in Domestic Dogs,Canis familiaris

Evidence of animal multimodal signalling is widespread and compelling. Dogs’ aggressive vocalisations (growls and barks) have been extensively studied, but without any consideration of the simultaneously produced visual displays. In this study we aimed to categorize dogs’ bimodal aggressive signals according to the redundant/non-redundant classification framework. We presented dogs with unimodal (audio or visual) or bimodal (audio-visual) stimuli and measured their gazing and motor behaviours. Responses did not qualitatively differ between the bimodal and two unimodal contexts, indicating that acoustic and visual signals provide redundant information. We could not further classify the signal as ‘equivalent’ or ‘enhancing’ as we found evidence for both subcategories. We discuss our findings in relation to the complex signal framework, and propose several hypotheses for this signal’s function.     

The effect of ostensive cues on dogs’ performance in a manipulative social learning task

In contrast to animal social learning (e.g. dogs learning from observing another dog), humans typically teach by attracting the attention of the learner. Also during the training of dogs, humans tend to attract their attention in a similar way. Here, we investigated dogs’ ability to learn both from a dog and a human demonstrator in a manipulative task, where the models demonstrated which part of a box to manipulate in order to get a food reward. We varied the communicative context both during the dog and during the human demonstration comparably: a second experimenter directed the attention of the subjects to the model (dog/human ostensive demonstration) or remained silent (dog/human non-ostensive demonstration). Moreover, we investigated whether the training level of the dogs (well-trained vs. untrained) affected how the dogs performed in the manipulative tasks after the different demonstrations.We found that better trained dogs showed significantly better problem solving abilities. They paid more attention to the human demonstration than to the dog model, whereas such a difference in attentiveness of the less trained dogs was not found. Despite slight differences in paying attention to the different demonstrators, the presence of human or the dog demonstrators exerted equally effectiveness on the test performance of the dogs. However, the effectiveness of the demonstrations was significantly reduced if ostensive cues were given during the demonstrations by a second experimenter. Analysis of attentiveness and activity of the observer dogs during the demonstrations indicates that the reason for this negative effect was a combination of distracted attention paid to the demonstration and a higher level of excitement in the ostensive than in the non-ostensive demonstrations.This study suggests that third party communication during demonstration attracts dogs’ attention to the communicator instead of paying close attention to the model. We suggest that precise timing and synchronization of attention-calling and demonstration is necessary to avoid this distracting effect.     

Explaining Dog Wolf Differences in Utilizing Human Pointing Gestures: Selection for Synergistic Shifts in the Development of Some Social Skills

Background

The comparison of human related communication skills of socialized canids may help to understand the evolution and the epigenesis of gesture comprehension in humans. To reconcile previously contradicting views on the origin of dogs'' outstanding performance in utilizing human gestures, we suggest that dog-wolf differences should be studied in a more complex way.

Methodology/Principal Findings

We present data both on the performance and the behaviour of dogs and wolves of different ages in a two-way object choice test. Characteristic behavioural differences showed that for wolves it took longer to establish eye contact with the pointing experimenter, they struggled more with the handler, and pups also bit her more before focusing on the human''s signal. The performance of similarly hand-reared 8-week-old dogs and wolves did not differ in utilizing the simpler proximal momentary pointing. However, when tested with the distal momentary pointing, 4-month-old pet dogs outperformed the same aged hand reared wolves. Thus early and intensive socialisation does not diminish differences between young dogs and wolves in behaviour and performance. Socialised adult wolves performed similarly well as dogs in this task without pretraining. The success of adult wolves was accompanied with increased willingness to cooperate.

Conclusion/Significance

Thus, we provide evidence for the first time that socialised adult wolves are as successful in relying on distal momentary pointing as adult pet dogs. However, the delayed emergence of utilising human distal momentary pointing in wolves shows that these wild canines react to a lesser degree to intensive socialisation in contrast to dogs, which are able to control agonistic behaviours and inhibition of actions in a food related task early in development. We suggest a “synergistic” hypothesis, claiming that positive feedback processes (both evolutionary and epigenetic) have increased the readiness of dogs to attend to humans, providing the basis for dog-human communication.     

Variation in withholding of information in three monkey species

Studies on tactical deception have reported that informed subordinates can withhold information from naive dominants, but they have not directly compared species'' performance. Here, we compared the performance in two withholding-of-information tasks of three monkey species differing in the strictness of their dominance hierarchy and degree of fission–fusion dynamics: spider monkeys, capuchin monkeys and long-tailed macaques. Food was hidden from the dominants'' view either inside an opaque box or in a transparent box that could only be opened by knowledgeable subordinates. All species were capable of withholding information, with subjects refraining from interacting with the box when the dominant was nearby. Spider monkeys were the most efficient at retrieving food, by timing it when the dominant was far from the box. Capuchin monkeys were also quite efficient when alone at the box, but they lost much of the food when manipulating the box with the dominant nearby. The results supported our predictions based on interspecific differences in the strictness of the dominance hierarchy and the degree of fission–fusion dynamics, with the former constraining the subjects'' tendency to approach the box and the latter affecting the subjects’ tendency to wait for the appropriate situation to retrieve the food.     

Visual Cues Given by Humans Are Not Sufficient for Asian Elephants (Elephas maximus) to Find Hidden Food

Recent research suggests that domesticated species – due to artificial selection by humans for specific, preferred behavioral traits – are better than wild animals at responding to visual cues given by humans about the location of hidden food. \Although this seems to be supported by studies on a range of domesticated (including dogs, goats and horses) and wild (including wolves and chimpanzees) animals, there is also evidence that exposure to humans positively influences the ability of both wild and domesticated animals to follow these same cues. Here, we test the performance of Asian elephants (Elephas maximus) on an object choice task that provides them with visual-only cues given by humans about the location of hidden food. Captive elephants are interesting candidates for investigating how both domestication and human exposure may impact cue-following as they represent a non-domesticated species with almost constant human interaction. As a group, the elephants (n = 7) in our study were unable to follow pointing, body orientation or a combination of both as honest signals of food location. They were, however, able to follow vocal commands with which they were already familiar in a novel context, suggesting the elephants are able to follow cues if they are sufficiently salient. Although the elephants’ inability to follow the visual cues provides partial support for the domestication hypothesis, an alternative explanation is that elephants may rely more heavily on other sensory modalities, specifically olfaction and audition. Further research will be needed to rule out this alternative explanation.     

Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns

Appropriate response to companions’ emotional signals is important for all social creatures. The emotional expressions of humans and non-human animals have analogies in their form and function, suggesting shared evolutionary roots, but very little is known about how animals other than primates view and process facial expressions. In primates, threat-related facial expressions evoke exceptional viewing patterns compared with neutral or positive stimuli. Here, we explore if domestic dogs (Canis familiaris) have such an attentional bias toward threatening social stimuli and whether observed emotional expressions affect dogs’ gaze fixation distribution among the facial features (eyes, midface and mouth). We recorded the voluntary eye gaze of 31 domestic dogs during viewing of facial photographs of humans and dogs with three emotional expressions (threatening, pleasant and neutral). We found that dogs’ gaze fixations spread systematically among facial features. The distribution of fixations was altered by the seen expression, but eyes were the most probable targets of the first fixations and gathered longer looking durations than mouth regardless of the viewed expression. The examination of the inner facial features as a whole revealed more pronounced scanning differences among expressions. This suggests that dogs do not base their perception of facial expressions on the viewing of single structures, but the interpretation of the composition formed by eyes, midface and mouth. Dogs evaluated social threat rapidly and this evaluation led to attentional bias, which was dependent on the depicted species: threatening conspecifics’ faces evoked heightened attention but threatening human faces instead an avoidance response. We propose that threatening signals carrying differential biological validity are processed via distinctive neurocognitive pathways. Both of these mechanisms may have an adaptive significance for domestic dogs. The findings provide a novel perspective on understanding the processing of emotional expressions and sensitivity to social threat in non-primates.     

Our Faces in the Dog's Brain: Functional Imaging Reveals Temporal Cortex Activation during Perception of Human Faces

Dogs have a rich social relationship with humans. One fundamental aspect of it is how dogs pay close attention to human faces in order to guide their behavior, for example, by recognizing their owner and his/her emotional state using visual cues. It is well known that humans have specific brain regions for the processing of other human faces, yet it is unclear how dogs’ brains process human faces. For this reason, our study focuses on describing the brain correlates of perception of human faces in dogs using functional magnetic resonance imaging (fMRI). We trained seven domestic dogs to remain awake, still and unrestrained inside an MRI scanner. We used a visual stimulation paradigm with block design to compare activity elicited by human faces against everyday objects. Brain activity related to the perception of faces changed significantly in several brain regions, but mainly in the bilateral temporal cortex. The opposite contrast (i.e., everyday objects against human faces) showed no significant brain activity change. The temporal cortex is part of the ventral visual pathway, and our results are consistent with reports in other species like primates and sheep, that suggest a high degree of evolutionary conservation of this pathway for face processing. This study introduces the temporal cortex as candidate to process human faces, a pillar of social cognition in dogs.     

Knower–guesser differentiation in ravens: others' viewpoints matter

Differentiating between individuals with different knowledge states is an important step in child development and has been considered as a hallmark in human evolution. Recently, primates and corvids have been reported to pass knower–guesser tasks, raising the possibility of mental attribution skills in non-human animals. Yet, it has been difficult to distinguish ‘mind-reading’ from behaviour-reading alternatives, specifically the use of behavioural cues and/or the application of associatively learned rules. Here, I show that ravens (Corvus corax) observing an experimenter hiding food are capable of predicting the behaviour of bystanders that had been visible at both, none or just one of two caching events. Manipulating the competitors'' visual field independently of the view of the test-subject resulted in an instant drop in performance, whereas controls for behavioural cues had no such effect. These findings indicate that ravens not only remember whom they have seen at caching but also take into account that the other''s view was blocked. Notably, it does not suffice for the birds to associate specific competitors with specific caches. These results support the idea that certain socio-ecological conditions may select for similar cognitive abilities in distantly related species and that some birds have evolved analogous precursors to a human theory-of-mind.     

The SNPs of Melanocortin 4 Receptor (MC4R) Associated with Body Weight in Beagle Dogs

Melanocortin 4 receptor (MC4R), which is associated with inherited human obesity, is involoved in food intake and body weight of mammals. To study the relationships between MC4R gene polymorphism and body weight in Beagle dogs, we detected and compared the nucleotide sequence of the whole coding region and 3′- and 5′- flanking regions of the dog MC4R gene (1214 bp). In 120 Beagle dogs, two SNPs (A420C, C895T) were identified and their relation with body weight was analyzed with RFLP-PCR method. The results showed that the SNP at A420C was significantly associated with canine body weight trait when it changed amino acid 101 of the MC4R protein from asparagine to threonine,while canine body weight variations were significant in female dogs when MC4R nonsense mutation at C895T. It suggested that the two SNPs might affect the MC4R gene’s function which was relative to body weight in Beagle dogs. Therefore, MC4R was a candidate gene for selecting different size dogs with the MC4R SNPs (A420C, C895T) being potentially valuable as a genetic marker.     

Domestic dogs' (Canis familiaris) understanding of Projected Video Images of a Human Demonstrator in an Object‐choice Task

Presenting animals with artificial visual stimuli is a key element of many recent behavioral experiments largely because images are easier to control and manipulate than live demonstrations. Determining how animals process images is crucial for being able to correctly interpret subjects' reactions toward these stimuli. In this study, we aimed to use the framework proposed by Fagot et al. (2010) Proc. Natl. Acad. Sci. USA 107 , 519 to classify how dogs perceive life‐sized projected videos. First, we tested whether dogs can use pre‐recorded and hence non‐interactive, video footage of a human to locate a hidden reward in a three‐way choice task. Secondly, we investigated whether dogs solve this task by means of referential understanding. To achieve this, we separated the location of the video projection from the location where dogs had to search for the hidden reward. Our results confirmed that dogs can reliably use pre‐recorded videos of a human as a source of information when the demonstration and the hiding locations are in the same room. However, they did not find the hidden object above the chance level when the hiding locations were in a separate room. Still, further analysis found a positive connection between the attention paid to the projection and the success rate of dogs. This finding suggests that the factor limiting dogs' performance was their attention and that with further training they might be able to master tasks involving referential understanding.     

Wolves Are Better Imitators of Conspecifics than Dogs

Domestication is thought to have influenced the cognitive abilities of dogs underlying their communication with humans, but little is known about its effect on their interactions with conspecifics. Since domestication hypotheses offer limited predictions in regard to wolf-wolf compared to dog-dog interactions, we extend the cooperative breeding hypothesis suggesting that the dependency of wolves on close cooperation with conspecifics, including breeding but also territory defense and hunting, has created selection pressures on motivational and cognitive processes enhancing their propensity to pay close attention to conspecifics’ actions. During domestication, dogs’ dependency on conspecifics has been relaxed, leading to reduced motivational and cognitive abilities to interact with conspecifics. Here we show that 6-month-old wolves outperform same aged dogs in a two-action-imitation task following a conspecific demonstration. While the wolves readily opened the apparatus after a demonstration, the dogs failed to solve the problem. This difference could not be explained by differential motivation, better physical insight of wolves, differential developmental pathways of wolves and dogs or a higher dependency of dogs from humans. Our results are best explained by the hypothesis that higher cooperativeness may come together with a higher propensity to pay close attention to detailed actions of others and offer an alternative perspective to domestication by emphasizing the cooperativeness of wolves as a potential source of dog-human cooperation.     

A Single-fly Assay for Foraging Behavior in Drosophila

For many animals, hunger promotes changes in the olfactory system in a manner that facilitates the search for appropriate food sources. In this video article, we describe an automated assay to measure the effect of hunger or satiety on olfactory dependent food search behavior in the adult fruit fly Drosophila melanogaster. In a light-tight box illuminated by red light that is invisible to fruit flies, a camera linked to custom data acquisition software monitors the position of six flies simultaneously. Each fly is confined to walk in individual arenas containing a food odor at the center. The testing arenas rest on a porous floor that functions to prevent odor accumulation. Latency to locate the odor source, a metric that reflects olfactory sensitivity under different physiological states, is determined by software analysis. Here, we discuss the critical mechanics of running this behavioral paradigm and cover specific issues regarding fly loading, odor contamination, assay temperature, data quality, and statistical analysis.     

When dogs look back: inhibition of independent problem-solving behaviour in domestic dogs (Canis lupus familiaris) compared with wolves (Canis lupus)

Domestic dogs have been recognized for their social sensitivity and aptitude in human-guided tasks. For example, prior studies have demonstrated that dogs look to humans when confronted with an unsolvable task; an action often interpreted as soliciting necessary help. Conversely, wolves persist on such tasks. While dogs'' ‘looking back’ behaviour has been used as an example of socio-cognitive advancement, an alternative explanation is that pet dogs show less persistence on independent tasks more generally. In this study, pet dogs, shelter dogs and wolves were given up to three opportunities to open a solvable puzzle box: when subjects were with a neutral human caretaker, alone and when encouraged by the human. Wolves were more persistent and more successful on this task than dogs, with 80% average success rate for wolves versus a 5% average success rate for dogs in both the human-in and alone conditions. Dogs showed increased contact with the puzzle box during the encouragement condition, but only a moderate increase in problem-solving success. Social sensitivity appears to play an important role in pet and shelter dogs'' willingness to engage in problem-solving behaviour, which could suggest generalized dependence on, or deference to, human action.