Monique A. R. Udell

Wolves outperform dogs in following human social cues

Domestic dogs, Canis familiaris, have been shown capable of finding hidden food by following pointing gestures made with different parts of the human body. However, previous studies have reported that hand-reared wolves, C. lupus, fail to locate hidden food in response to similar points in the absence of extensive training. The failure of wolves to perform this task has led to the proposal that the ability to understand others intentions is a derived character in dogs, not present in the ancestral population (wolves). Here we show that wolves, given the right rearing environment and daily interaction with humans, can use momentary distal human pointing cues to find food without training, whereas dogs tested outdoors and dogs at an animal shelter do not follow the same human points. In line with past studies, pet dogs tested indoors were successful in following these points. We also show that the reported failure of wolves in some past studies may be due to differences in the testing environment. Our findings indicate that domestication is not a prerequisite for human-like social cognition in canids, and show the need for additional research on the role of rearing conditions and environmental factors in the development of higher-level cognitive abilities.

What did domestication do to dogs? A new account of dogs' sensitivity to human actions

Over the last two decades increasing evidence for an acute sensitivity to human gestures and attentional states in domestic dogs has led to a burgeoning of research into the social cognition of this highly familiar yet previously under‐studied animal. Dogs (Canis lupus familiaris) have been shown to be more successful than their closest relative (and wild progenitor) the wolf, and than mans closest relative, the chimpanzee, on tests of sensitivity to human social cues, such as following points to a container holding hidden food. The “Domestication Hypothesis” asserts that during domestication dogs evolved an inherent sensitivity to human gestures that their non‐domesticated counterparts do not share. According to this view, sensitivity to human cues is present in dogs at an early age and shows little evidence of acquisition during ontogeny. A closer look at the findings of research on canine domestication, socialization, and conditioning, brings the assumptions of this hypothesis into question. We propose the Two Stage Hypothesis, according to which the sensitivity of an individual animal to human actions depends on acceptance of humans as social companions, and conditioning to follow human limbs. This offers a more parsimonious explanation for the domestic dogs sensitivity to human gestures, without requiring the use of additional mechanisms. We outline how tests of this new hypothesis open directions for future study that offer promise of a deeper understanding of mankinds oldest companion.

Ontogeny's impacts on human–dog communication

Several authors have argued recently that domestication has led to a special sensitivity to human social cues in domestic dogs, Canis familiaris. This sensitivity is not present in dogs closest wild relatives and progenitors, wolves, Canis lupus (Hare et al. 2002; Kubinyi et al. 2007). Furthermore , even puppies too young to have had extensive exposure to humans are able to follow human social cues. Consequently this ability must have a largely innate basis (Hare & Tomasello 2005; Hare et al. 2005). Various forms of cueing the location of hidden food by a human pointing with her limbs have been extensively used as tests of canid comprehension of human intentions (e.g. In a recent paper Riedel et al. (2008) presented data from four age groups of puppies, ranging from 6 to 24 weeks, which, they claimed, indicate that dogs as young as 6 weeks old can use a variety of human communicative gestures to locate hidden food. They believe this suggests that dogs do not acquire these skills mainly because of their experiences in ontogeny (Riedel et al. 2008, page 5). We believe that the results presented by Riedel et al. (2008) do not justify their conclusions. We concentrate our analysis on their experiment 1 because it is the only experiment that tested several different juvenile groups (experiments 2 and 3 compared only young dogs to adults), and it included three different types of point (experiments 2 and 3 presented only one type of point each) and thus three times as many trials as the other two experiments. In experiment 1, 16 puppies at each of four different ages (i.e. 64 dogs in total) were tested on three different types of point and a control condition. The ages tested were 6, 8, 16 and 24 weeks, and the points were Dynamic cross point move (DCPM: experimenter pointed to baited cup with index finger of contralateral hand four times, leaving her hand indicating the cup), Dynamic cross point (DCP: as DCPM but pointing only once) and Marker (M: experimenter placed a piece of wood on top of the baited cup in full view of the dog). In addition, all dogs were tested on control trials in which a cup was baited but no cue was offered. In each case, the oldest dogs performed better on each point type than the youngest dogs. The oldest dogs scored 0.63, 0.81 and 1.19 points …

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 experimenters 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.

The performance of stray dogs (Canis familiaris) living in a shelter on human-guided object-choice tasks.

A decade of research on domestic dogs responsiveness to human actions has led some to believe that all members of the species Canis familiaris possess a human-like social cognition not shared by their nondomesticated relatives. However, comparative studies on diverse populations of domestic dog are lacking, making species-wide generalizations premature. In this study we present the performance of one under-represented population, stray dogs living in shelters, on a human-guided object-choice task. Unlike pet dogs, shelter dogs universally failed to follow a momentary distal point to a target location in initial tests, although they were able to follow a simpler form of human point on the same task. Furthermore, the majority of subjects learned to follow a momentary distal point to a target when given additional training trials (experiment 2). Dogs sensitivity to human gestures may not be entirely explained by phylogenetic variables; rather, the interactions between genetic, developmental and experiential variables must be considered.

Ontogeny and phylogeny: both are essential to human-sensitive behaviour in the genus Canis

In responding to Hare et al. (2010), we wish to start by outlining our substantive areas of agreement. We do not disagree that pet domestic dogs have a remarkable sensitivity to human actions, gestures and intentional movements. We also agree with Hare et al. that the most likely reason why the wolves tested in Udell et al. (2008a) were so responsive to human pointing gestures was because these animals were ‘highly socialized [and] [t]his socialization probably gave [these] subjects significant experience responding to actions similar to human pointing, whether the animal handler was aware of this type of exposure or not’ (Hare et al. 2010, page e6). In that paper we argued that ‘that environment and development affect a social animal’s ability to react in situation appropriate ways to the social cues of other individuals’ (Udell et al. 2008a, page 1772). The crux of our disagreement with Hare et al. (2010) is our belief that socialization and experience are essential for all canids to respond to heteroand conspecific cues. Since at least the 1920s scientists have recognized that heredity alone is insufficient to fully explain a phenotype. Phenotypes can only be characterized as the outcome of a complex interaction between heredity, development and environment (Gottlieb 2002). Unfortunately development and environment receive short shrift in the domestication hypothesis as presented by Hare et al. (2010). To be clear, we do not denyan influence of heredity or domestication on the social behaviour of domestic dogs, we simply do not agree that a hypothesis based on genetic inheritance alone is viable without consideration of the interacting developmental and environmental variables that are necessary for the expression of any phenotype. Our response is organized to match Hare et al.’s (2010) commentary. First, we respond to their review of the literature on the sensitivity of dogs, wolves and foxes to human cues. Second, we discuss their reanalysis of our data comparing the performance of wolves and dogs in responding to a human pointing gesture (Udell et al. 2008a). Third, we consider the data on dogs living in a shelter reported in Hare et al. (2010). Fourth we comment briefly on Hare et al.’s response to Wynne et al.’s (2008) reanalysis of Riedel et al.’s (2008) data on the development of following human points in dog pups, before concluding with some general comments on the roles of ontogeny and phylogeny in the expression of complex interspecies social behaviours.

Can your dog read your mind? Understanding the causes of canine perspective taking

Prior studies have documented the domestic dog’s (Canis lupus familiaris) sensitivity to human attentional state, including a tendency to preferentially beg for food from attentive individuals and an ability to selectively perform forbidden behaviors when humans are not looking. Due to the success of dogs on perspective-taking tasks, some have hypothesized that domestic dogs may have theory of mind, or the ability to infer what other individuals know. Here we provide the first evidence that nondomesticated canids, grey wolves (Canis lupus), are also sensitive to human attentional state under some conditions. We also demonstrate that dogs do not display an undifferentiated sensitivity to all visual cues of attentional state. Rather, dogs are more sensitive to stimuli encountered in their home environment. Some dogs perform poorly on perspective-taking tasks. These findings have important implications for the interpretation of research designed to understand complex social cognition across species.

Breed differences in dogs sensitivity to human points: A meta-analysis

The last decade has seen a substantial increase in research on the behavioral and cognitive abilities of pet dogs, Canis familiaris. The most commonly used experimental paradigm is the object-choice task in which a dog is given a choice of two containers and guided to the reinforced object by human pointing gestures. We review here studies of this type and attempt a meta-analysis of the available data. In the meta-analysis breeds of dogs were grouped into the eight categories of the American Kennel Club, and into four clusters identified by Parker and Ostrander [Parker, H.G., Ostrander, E.A., 2005. Canine genomics and genetics: running with the pack. PLoS Genet. 1, 507-513] on the basis of a genetic analysis. No differences in performance between breeds categorized in either fashion were identified. Rather, all dog breeds appear to be similarly and highly successful in following human points to locate desired food. We suggest this result could be due to the paucity of data available in published studies, and the restricted range of breeds tested.

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.

Exploring breed differences in dogs (Canis familiaris): does exaggeration or inhibition of predatory response predict performance on human-guided tasks?

Domestic dogs, Canis familiaris, responsiveness to human action has been a topic of scientific interest for almost two decades. However, are all breeds of domestic dog equally prepared to succeed on human-guided object-choice tasks? In the current study we compared three breeds of dog with distinct predatory motor pattern sequences still under direct selection pressure today based on their traditional working roles. Airedale terriers (hunting dogs) are bred for a fully intact predatory sequence, matching the wild-type form. Border collies (herding dogs) are bred for an exaggeration of the eye-stalk-chase component of the predatory sequence. Anatolian shepherds (livestock-guarding dogs) are bred for the inhibition of the full predatory sequence. Here we asked whether and how these opposing selection pressures correspond with each breeds tendency to track and follow a human point to a target in an object-choice task. Our results suggest that the presence or exaggeration of key components of the predatory sequence may in fact predict superior initial performance on pointing tasks when compared to a breed selected for its inhibited predatory response. This is the first time relative success on a pointing task has been tied to a known heritable behavioural mechanism (breed-specific motor patterns). However, we also demonstrate that breed-specific differences can sometimes be overcome with additional experience. Thus, an individuals performance on human-guided tasks is still best predicted by a combination of genetic and lifetime factors. Broader implications for the understanding and investigation of canine social cognition are discussed.