Going back to "basics": Harlow's learning set task with wolves and dogs.

To survive and reproduce, animals need to behave adaptively by adjusting their behavior to their environment, with learning facilitating some of these processes. Dogs have become a go-to model species in comparative cognition studies, making our understanding of their learning skills paramount at multiple levels, not only with regards to basic research on their cognitive skills and the effects of domestication, but also with applied purposes such as training. In order to tackle these issues, we tested similarly raised wolves and dogs in a serial learning task inspired by Harlow's "learning set." In Phase 1, different pairs of objects were presented to the animals, one of which was baited while the other was not. Both species' performance gradually improved with each new set of objects, showing that they "learnt to learn," but no differences were found between the species in their learning speed. In Phase 2, once subjects had learned the association between one of the objects and the food reward, the contingencies were reversed and the previously unrewarded object of the same pair was now rewarded. Dogs' performance in this task seemed to be better than wolves', albeit only when considering just the first session of each reversal, suggesting that the dogs might be more flexible than wolves. Further research (possibly with the aid of refined methods such as computer-based tasks) would help ascertain whether these differences between wolves and dogs are persistent across different learning tasks.

The Power of Discourse: Associations between Trainers' Speech and the Responses of Socialized Wolves and Dogs to Training.

In a previous study, we found that Positive Reinforcement Training reduced cortisol of wolves and dogs; however, this effect varied across trainer-animal dyads. Here we investigate whether and how the trainers' use of speech may contribute to this effect. Dogs' great interest in high-pitched, intense speech (also known as Dog Directed Speech) has already been reported, but whether and how wolves respond similarly/differently to voice characteristics has never been studied before. We analyzed 270 training sessions, conducted by five trainers, with nine mixed-breed dogs and nine wolves, all human-socialized. Through Generalized Linear Mixed Models, we analyzed the effects of (a) three speech categories (nice, neutral, reprehensive) and laugh; and (b) acoustic characteristics of trainers' voices on animals' responses (correct responses, latency, orientation, time at less than 1 m, non-training behaviors, tail position/movements, cortisol variation). In both subspecies, tail wagging occurred more often in sessions with longer durations of nice speech, and less often in sessions with reprehensive speech. For dogs, the duration of reprehensive speech within a session was also negatively related to correct responses. For wolves, retreat time was associated with more reprehensive speech, whereas duration of nice speech was positively associated with time spent within one meter from the trainer. In addition, most dog behavioral responses were associated with higher average intonations within sessions, while wolf responses were correlated with lower intonations within sessions. We did not find any effects of the variables considered on cortisol variation. Our study highlights the relevance of voice tone and speech in a training context on animals' performances and emotional reactions.

How to improve data quality in dog eye tracking.

Pupil-corneal reflection (P-CR) eye tracking has gained a prominent role in studying dog visual cognition, despite methodological challenges that often lead to lower-quality data than when recording from humans. In the current study, we investigated if and how the morphology of dogs might interfere with tracking of P-CR systems, and to what extent such interference, possibly in combination with dog-unique eye-movement characteristics, may undermine data quality and affect eye-movement classification when processed through algorithms. For this aim, we have conducted an eye-tracking experiment with dogs and humans, and investigated incidences of tracking interference, compared how they blinked, and examined how differential quality of dog and human data affected the detection and classification of eye-movement events. Our results show that the morphology of dogs' face and eye can interfere with tracking methods of the systems, and dogs blink less often but their blinks are longer. Importantly, the lower quality of dog data lead to larger differences in how two different event detection algorithms classified fixations, indicating that the results of key dependent variables are more susceptible to choice of algorithm in dog than human data. Further, two measures of the Nyström & Holmqvist (Behavior Research Methods, 42(4), 188-204, 2010) algorithm showed that dog fixations are less stable and dog data have more trials with extreme levels of noise. Our findings call for analyses better adjusted to the characteristics of dog eye-tracking data, and our recommendations help future dog eye-tracking studies acquire quality data to enable robust comparisons of visual cognition between dogs and humans.

Selective responding to human ostensive communication is an early developing capacity of domestic dogs.

Ostensive communication, communication motivated not only by an informative intention, but also by an intention to make this informative intention overt, is thought to be restricted to human signalers and to rely on metacognitive skills. On the receiver side, human infants and dogs have been found to selectively respond to human ostensive communication, even if it remains unclear whether they are able to discern the underlying intentions. At present only animals with extensive experiences with humans have demonstrated a response to human attention calling, suggesting that this sensitivity may be an exaptation of communicative skills allowing for context-specific responding to intraspecific signals. We investigated whether dogs could respond to subtle cues of ostension without clear attention-calling and how this skill varies across age and with different human-given signals. Using a two-way object choice task, we evaluated whether dogs of different ages followed, with their gaze and with their choices, ostensive human pointing and gaze more than a formally similar but non-ostensive gesture and a directional gaze cue. Dogs followed pointing more than gaze, and older dogs followed the directional cues more accurately than younger dogs. Independent of cue type, we found that dogs of all ages responded to human ostensive signals more than similar directional cues motivated by no communicative intention. Given that dogs are sensitive to subtle cues of ostensive communication from an early age, and that this does not appear to change with age, we suggest that living close to humans may have selected for this skill. RESEARCH HIGHLIGHTS: Like human infants, dogs followed human ostensive cues more than non-ostensive cues both by their approach behavior and their differential looking behavior. Dogs differentiated between ostensive and non-ostensive human cues from an early age on, without their attention having been called explicitly in advance. Dogs followed human-given pointing cues more than human-given gaze cues, independent of age or intention (ostensive or non-ostensive). The early developing sensitivity of dogs to human ostension suggests that living close to humans may have selected for this skill.

Pet dogs' Behavioural Reaction to Their Caregiver's Interactions with a Third Party: Join in or Interrupt?

Pet dogs are promising candidates to study attachment-related and potentially jealousy-like behaviours in non-human animals, as they form a strong and stable bond with their human caregivers who often engage in affiliative interactions with diverse social partners. Nevertheless, it is still debated whether non-human animals are capable of experiencing such complex emotions. Even though caregivers frequently report observations of jealousy-like behaviours in dogs, behavioural studies in dogs have thus far led to contradictory results. Adding to this complexity, dogs appear extraordinarily skilled in understanding humans' communicative behaviour and can flexibly and diversely interact with them in social contexts. Here, we aimed at investigating (1) whether dogs indeed respond in a jealousy-consistent manner when seeing their caregiver interact in an affiliative way with a remotely controlled, realistic-looking fake dog, or (2) whether they would rather synchronize their reaction to the fake dog with the caregiver's behaviour, or (3) whether they respond directly to the caregiver without paying much attention to the third party. To address what drives the dogs' behaviours in this triadic situation, we compared four groups of dogs who first observed and then joined the interaction of either the caregiver or a stranger greeting or medically examining the fake dog. We found that the dogs initially responded negatively or neutrally when the fake dog entered the room but changed to more positive reactions when the caregiver approached the fake dog, especially if initiating a positive interaction. When being released, more dogs showed friendly behaviours towards the fake dog when the caregiver-rather than the stranger-was interacting with it. At the same time, however, the dogs tried to block the interaction of the caregiver with the fake dog more often than the one of the stranger. In conclusion, we did not find clear evidence for jealousy-like behaviours in dogs during the human-fake dog interactions, but we observed indicators of behavioural synchronization with the caregivers, suggesting that the caregivers' affiliative behaviours directed at a third party may more often facilitate positive than negative interactions in dogs.

Secure base effect in former shelter dogs and other family dogs: Strangers do not provide security in a problem-solving task.

Domestic dogs display behavioural patterns towards their owners that fulfil the four criteria of attachment. As such, they use their owners as a secure base, exploring the environment and manipulating objects more when accompanied by their owners than when alone. Although there are some indications that owners serve as a better secure base than other human beings, the evidence regarding a strong owner-stranger differentiation in a manipulative context is not straightforward. In the present study, we conducted two experiments in which pet dogs were tested in an object-manipulation task in the presence of the owner and of a stranger, varying how the human partner would behave (i.e. remaining silent or encouraging the dog, Experiment 1), and when alone (Experiment 2). Further, to gain a better insight into the mechanisms behind a potential owner-stranger differentiation, we investigated the effect of dogs' previous life history (i.e. having lived in a shelter or having lived in the same household since puppyhood). Overall, we found that strangers do not provide a secure base effect and that former shelter dogs show a stronger owner-stranger differentiation than other family dogs. As former shelter dogs show more behavioural signs correlated with anxiety towards the novel environment and the stranger, we concluded that having been re-homed does not necessarily affect the likelihood of forming a secure bond with the new owner but might have an impact on how dogs interact with novel stimuli, including unfamiliar humans. These results confirm the owner's unique role in providing security to their dogs and have practical implications for the bond formation in pet dogs with a past in a shelter.

Wolves, dogs and humans in regular contact can mutually impact each other's skin microbiota.

In contrast to humans and dogs, the skin microbiota of wolves is yet to be described. Here, we investigated the skin microbiota of dogs and wolves kept in outdoor packs at the Wolf Science Center (WSC) via 16S rRNA gene amplicon sequencing. Skin swab samples were also collected from human care takers and their pet dogs. When comparing the three canine groups, representing different degrees of human contact to the care takers and each other, the pet dogs showed the highest level of diversity. Additionally, while human skin was dominated by a few abundant phylotypes, the skin microbiota of the care takers who had particularly close contact with the WSC animals was more similar to the microbiota of dogs and wolves compared to the humans who had less contact with these animals. Our results suggest that domestication may have an impact on the diversity of the skin microbiota, and that the canine skin microbiota can be shared with humans, depending on the level of interaction.

Partial rewarding during clicker training does not improve naïve dogs' learning speed and induces a pessimistic-like affective state.

Clicker training is considered a welfare-friendly way of teaching novel behaviors to animals because it is mostly based on the positive reinforcement. However, trainers largely vary in their way of applying this training technique. According to the most, a reward (e.g., food) should follow every click, while others claim that dogs learn faster when the reward is sometimes omitted. One argument against the use of partial rewarding is that it induces frustration in the animal, raising concerns over its welfare consequences. Here, we investigated the effect of partial rewarding not only on training efficacy (learning speed), but also on dogs' affective state. We clicker-trained two groups of dogs: one group received food after every click while the other group received food only 60% of the time. Considering previous evidence of the influencing role of personality on reactions to frustrated expectations, we included measurements of dogs' emotional reactivity. We compared the number of trials needed to reach a learning criterion and their pessimistic bias in a cognitive bias test. No difference between the two groups emerged in terms of learning speed; however, dogs that were partially rewarded during clicker training showed a more pessimistic bias than dogs that were continuously rewarded. Generally, emotional reactivity was positively associated with a more pessimistic bias. Partial rewarding does not improve training efficacy, but it is associated with a negatively valenced affective state, bringing support to the hypothesis that partial rewarding might negatively affect dogs' welfare.

Individual and group level personality change across the lifespan in dogs.

In humans, age-related changes in personality occur in a non-random fashion with respect to their direction, timing, and magnitude. In dogs, there are still gaps in our knowledge about the detailed dynamics of age-related personality changes. We analysed the personality of 217 Border collies aged from 0.5 to 15 years both cross-sectionally and longitudinally using a test battery, to specify age periods when changes most prominently occur, assess the magnitude of changes, and analyse individual differences in personality change. We found that similar to humans, changes in personality occur unevenly during the dogs' life course, however, their dynamics seems to be specific for each trait. Activity-independence decreased mostly from puppyhood (0.5-1 years) to adolescence (> 1-2 years), then continued to decrease in a slowing rate. Novelty seeking did not change markedly until middle age (> 3-6 years), then showed a steady linear decrease. Problem orientation increased strongly until middle age then showed no marked changes in later age periods. We also revealed individual differences in personality change over time, and showed that a few individuals with potential age-related impairments significantly affected the general age trajectory of some traits. These results raise caution against the over-generalisation of global age trends in dogs.

Comparing the tractability of young hand-raised wolves (Canis lupus) and dogs (Canis familiaris).

Dogs live in 45% of households, integrated into various human groups in various societies. This is certainly not true for wolves. We suggest that dogs' increased tractability (meant as individual dogs being easier to control, handle and direct by humans, in contrast to trainability defined as performance increase due to training) makes a crucial contribution to this fundamental difference. In this study, we assessed the development of tractability in hand-raised wolves and similarly raised dogs. We combined a variety of behavioural tests: fetching, calling, obeying a sit signal, hair brushing and walking in a muzzle. Wolf (N = 16) and dog (N = 11) pups were tested repeatedly, between the ages of 3-24 weeks. In addition to hand-raised wolves and dogs, we also tested mother-raised family dogs (N = 12) for fetching and calling. Our results show that despite intensive socialization, wolves remained less tractable than dogs, especially in contexts involving access to a resource. Dogs' tractability appeared to be less context dependent, as they followed human initiation of action in more contexts than wolves. We found no evidence that different rearing conditions (i.e. intensive socialization vs. mother rearing) would affect tractability in dogs. This suggests that during domestication dogs might have been selected for increased tractability, although based on the current data we cannot exclude that the differential speed of development of dogs and wolves or the earlier relocation of wolves to live as a group explains some of the differences we found.

Behavioural and cognitive changes in aged pet dogs: No effects of an enriched diet and lifelong training.

Dogs demonstrate behavioural changes and cognitive decline during aging. Compared to laboratory dogs, little is known about aging in pet dogs exposed to different environments and nutrition. In this study, we examined the effects of age, an enriched diet and lifelong training on different behavioural and cognitive measures in 119 pet dogs (>6yrs). Dogs were maintained on either an enriched diet or a control diet for one year. Lifelong training was calculated using a questionnaire where owners filled in their dog's training experiences to date. Before commencing the diet and after one year of dietary treatment, they were tested in the Modified Vienna Canine Cognitive Battery (MVCCB) consisting of 11 subtests to examine correlated individual differences in a set of tasks measuring general, social and physical cognition and related behaviours. Fourty two behavioural variables were coded and were subjected to principle component analyses for variable reduction. Twelve subtest level components and two Z-transformed variables were subjected to exploratory factor analysis which resulted in six final factors: Problem solving, Trainability, Sociability, Boldness, Activity-independence and Dependency. Problem solving, Sociability, Boldness, and Dependency showed a linear decline with age, suggesting that the MVCCB can be used as a tool to measure behavioural and cognitive decline in aged pet dogs. An enriched diet and lifelong training had no effect on these factors, calling attention to the fact that the real world impact of nutritional and other interventions in possibly counteracting the effects of aging, should be further investigated in pet dogs living under diverse conditions, in order to understand their ultimate effects.

Dogs wait longer for better rewards than wolves in a delay of gratification task: but why?

Self-control has been shown to be linked with being cooperative and successful in humans and with the g-factor in chimpanzees. As such, it is likely to play an important role in all forms of problem-solving. Self-control, however, does not just vary across individuals but seems also to be dependent on the ecological niche of the respective species. With dogs having been selected to live in the human environment, several domestication hypotheses have predicted that dogs are better at self-control and thus more tolerant of longer delays than wolves. Here we set out to test this prediction by comparing dogs' and wolves' self-control abilities using a delay of gratification task where the animals had to wait for a predefined delay duration to exchange a low-quality reward for a high-quality reward. We found that in our task, dogs outperformed the wolves waiting an average of 66 s vs. 24 s in the wolves. Food quality did not influence how long the animals waited for the better reward. However, dogs performed overall better in motivation trials than the wolves, although the dogs' performance in those trials was dependent on the duration of the delays in the test trials, whereas this was not the case for the wolves. Overall, the data suggest that selection by humans for traits influencing self-control rather than ecological factors might drive self-control abilities in wolves and dogs. However, several other factors might contribute or explain the observed differences including the presence of the humans, which might have inhibited the dogs more than the wolves, lower motivation of the wolves compared to the dogs to participate in the task and/or wolves having a better understanding of the task contingencies. These possible explanations need further exploration.

Training pet dogs for eye-tracking and awake fMRI.

In recent years, two well-developed methods of studying mental processes in humans have been successively applied to dogs. First, eye-tracking has been used to study visual cognition without distraction in unrestrained dogs. Second, noninvasive functional magnetic resonance imaging (fMRI) has been used for assessing the brain functions of dogs in vivo. Both methods, however, require dogs to sit, stand, or lie motionless while yet remaining attentive for several minutes, during which time their brain activity and eye movements are measured. Whereas eye-tracking in dogs is performed in a quiet and, apart from the experimental stimuli, nonstimulating and highly controlled environment, MRI scanning can only be performed in a very noisy and spatially restraining MRI scanner, in which dogs need to feel relaxed and stay motionless in order to study their brain and cognition with high precision. Here we describe in detail a training regime that is perfectly suited to train dogs in the required skills, with a high success probability and while keeping to the highest ethical standards of animal welfare-that is, without using aversive training methods or any other compromises to the dog's well-being for both methods. By reporting data from 41 dogs that successfully participated in eye-tracking training and 24 dogs IN fMRI training, we provide robust qualitative and quantitative evidence for the quality and efficiency of our training methods. By documenting and validating our training approach here, we aim to inspire others to use our methods to apply eye-tracking or fMRI for their investigations of canine behavior and cognition.

Correction: Personality traits in companion dogs-Results from the VIDOPET.

[This corrects the article DOI: 10.1371/journal.pone.0195448.].

Wolves lead and dogs follow, but they both cooperate with humans.

Due to their convergent evolution, dogs have been suggested as a good model for the evolution of human social skills, such as tolerance and cooperativeness. However, recent studies have revealed that wolves (dogs' closest undomesticated relatives) are more tolerant and cooperative with conspecifics than dogs. It is still possible, though, that selection during domestication enhanced cooperative inclinations specifically towards humans, predicting better cooperation with humans in dogs than in wolves. We tested this hypothesis by comparing similarly human-raised wolves and dogs when cooperating with a familiar human partner in a string-pulling task. Both dogs and wolves were highly successful with the human partner, highlighting that dog-human cooperation could have evolved based on wolves' social skills. However, wolves and dogs differed in how they cooperated with their human partners with wolves being more likely to initiate movement leading the interaction with humans, whereas dogs were more likely to wait for the human to initiate action and then follow. Accordingly, we propose that during the course of domestication, after an initial reduction in fear of humans, dogs were selected for increased submissive inclinations (Deferential Behaviour Hypothesis) in order to minimize conflicts over resources, to ensure safe co-habitation and co-working in a way that humans lead and dogs follow.

Effect of Age and Dietary Intervention on Discrimination Learning in Pet Dogs.

Aging is associated with a decline in cognitive functions such as learning, memory, attention, cognitive flexibility, and executive functions. Recent evidence indicates that interventions such as exercise, diet and cognitive training can be used to reduce the rate of age-dependent cognitive decline. In this study, we examined the changes in discrimination learning in older pet dogs, tested whether a dietary intervention counteracts a potential decline in learning and evaluated the influence of lifelong training on learning speed and cognitive flexibility. We included 115 pet dogs (>6 years) of 30 different breeds into one of two treatment groups: either a diet enriched with antioxidants, docosahexaenoic acid (DHA), Phosphatidylserine and tryptophan or a control diet for 1 year. Lifelong training was calculated for each dog using a questionnaire where owners filled their dog's training experiences over years. Dogs were trained to discriminate different pictures at the start of the dietary intervention using a touch screen methodology. After 1 year of dietary intervention, they were tested on a main picture discrimination task where they were confronted with a discrimination of four new pictures. We used the total number of sessions needed to reach learning criterion as a measure of learning speed and the rate of correction trials as a measure of deficit in learning from feedback/cognitive flexibility. In the main discrimination task, we found an influence of neither age nor diet on the speed of learning and deficit in learning from feedback. We did not find any influence of lifelong training either. The null findings were further corroborated by Bayesian statistics. The null findings might be due to the fact that pet dogs live in a stimulating environment which may reduce the rate of cognitive decline and hinder finding an age or diet effect. Also, the similarity between the training and the main discrimination task might have made the main task too easy for the animals to solve. Further studies are warranted to assess the effect of enriched diets on pet dogs using tasks that measure cognitive functions with a higher sensitivity.

The effect of domestication on post-conflict management: wolves reconcile while dogs avoid each other.

Highly cooperative social species are expected to engage in frequent reconciliation following conflicts in order to maintain pack cohesiveness and preserve future cooperation. By contrast, in social species with low reliance on cooperation, reconciliation is expected to be less frequent. Here, we investigate the pattern of reconciliation in four captive wolf packs and four captive dog packs. We provide evidence for reconciliation in captive wolves, which are highly dependent on cooperation between pack members, while domestic dogs, which rely on conspecific cooperation less than wolves, avoided interacting with their partners after conflicts. Occurrence, intensity, latency, duration and initiation of wolf reconciliations appeared to vary as a consequence of a compromise between the costs (e.g. risk of further aggression) and the benefits (e.g. restoring relationship with opponents) of such interactions. Our results are in line with previous findings on various wolf packs living under different social and ecological conditions, suggesting that reconciliation is an important strategy for maintaining functional relationships and pack cohesiveness. However, current results on dogs are in contrast to the only other study showing that reconciliation can occur also in this species. Therefore, the occurrence of reconciliation in dogs may be influenced by social and environmental conditions more than in wolves. Which factors promote and modulate reconciliation in dogs needs to be further investigated.

In wolves, play behaviour reflects the partners' affiliative and dominance relationship.

Puppy packs (consisting of only puppies) and mixed-age packs (composed of puppies and adults) were observed to test whether social play can be used for assessing and establishing social relations in wolves, Canis lupus. Differently from previous studies, we looked at play behaviours in detail, allowing us to categorize play interactions as either competitive or relaxed, and predicted that different types of play would be associated with different relationships between individuals. We found that the more time dyads spent in relaxed play, the more affiliative interactions they exchanged outside of play. In the mixed-age packs, dyads that spent more time in both relaxed and competitive play showed fewer exchanges of aggressive behaviours. Conversely, in puppy packs, the more time dyads spent in competitive play, the more aggressive interactions were exchanged outside of play. Since clear dominance relationships emerged in the mixed-age packs, but not in puppy packs, we suggest that play can help to reduce the frequency of aggressive interactions only when a clear hierarchy exists between pack members. Furthermore, we found that in both puppy and mixed-age packs, dominance relationships were reflected and rarely reversed during play. Finally, dyads with a less clear dominance relationship spent more time playing in a competitive way. Overall, our results support the social assessment hypothesis suggesting that social relationships outside of play are reflected during playful interactions. Moreover, we revealed how different types of play, that is, playing in a competitive or relaxed way, may be related to different social relationships. This distinction between play types has not been acknowledged before but could help researchers better understand the functions of play in different species.

Personality traits in companion dogs-Results from the VIDOPET.

Individual behavioural differences in pet dogs are of great interest from a basic and applied research perspective. Most existing dog personality tests have specific (practical) goals in mind and so focused only on a limited aspect of dogs' personality, such as identifying problematic (aggressive or fearful) behaviours, assessing suitability as working dogs, or improving the results of adoption. Here we aimed to create a comprehensive test of personality in pet dogs that goes beyond traditional practical evaluations by exposing pet dogs to a range of situations they might encounter in everyday life. The Vienna Dog Personality Test (VIDOPET) consists of 15 subtests and was performed on 217 pet dogs. A two-step data reduction procedure (principal component analysis on each subtest followed by an exploratory factor analysis on the subtest components) yielded five factors: Sociability-obedience, Activity-independence, Novelty seeking, Problem orientation, and Frustration tolerance. A comprehensive evaluation of reliability and validity measures demonstrated excellent inter- and intra-observer reliability and adequate internal consistency of all factors. Moreover the test showed good temporal consistency when re-testing a subsample of dogs after an average of 3.8 years-a considerably longer test-retest interval than assessed for any other dog personality test, to our knowledge. The construct validity of the test was investigated by analysing the correlations between the results of video coding and video rating methods and the owners' assessment via a dog personality questionnaire. The results demonstrated good convergent as well as discriminant validity. To conclude, the VIDOPET is not only a highly reliable and valid tool for measuring dog personality, but also the first test to show consistent behavioural traits related to problem solving ability and frustration tolerance in pet dogs.