Intra and interspecific audience effect on domestic dogs' behavioural displays and facial expressions.

The aim of the current study was to investigate the influence of both intra- and interspecific audiences on dogs' facial expressions and behaviours. Forty-six dogs were exposed to three test conditions in which a food reward, initially available, was denied when in the presence of either a human (Human condition) or a dog audience (Dog condition), or in the absence of a visible audience (Non-social condition). Salivary cortisol was collected to evaluate the stress/arousal activation in the different conditions. Compared to the Non-social condition, the presence of a conspecific evoked more facial expressions, according to the DogFACS (Facial Action Coding System, an anatomically based tool to analyze facial expressions in domestic dogs), (EAD105-Ears downward), displacement behaviours (AD137-Nose licking, AD37-Lip wiping), tail wagging, whining, and panting (AD126). When facing a conspecific, dogs assumed a more avoidant attitude, keeping a distance and not looking at the stimuli, compared to when in the presence of the human partner. Dogs also exhibited more facial expressions (EAD102-Ears Adductor, EAD104-Ears Rotator), displacement behaviours (AD137-Nose licking, AD37-Lip wiping), panting (AD126) and whining when facing the conspecific than the human partner. Post-test cortisol was not influenced by any condition, and no association between pre-test cortisol and behavioural variables was found, thus strong differences in the levels of stress/arousal were unlikely to be responsible for differences in behavior between conditions. Considering the current results in the context of the available literature, we suggest that the higher displacement behaviors exhibited with the conspecifics were likely due to an increased level of uncertainty regarding the situations.

Street-wise dog testing: Feasibility and reliability of a behavioural test battery for free-ranging dogs in their natural habitat.

Behavioural scientists are increasingly recognizing the need to conduct experiments in the wild to achieve a comprehensive understanding of their species' behaviour. For domestic dogs (Canis familiaris), such progress has been slow. While the life in human households is often regarded as dogs' natural habitat, this classification disregards most of the global dog population. The value of experimentally testing free-ranging dogs' cognition and behaviour is increasingly being recognized, but no comprehensive test batteries have been conducted on those populations so far, leaving the feasibility and reliability of such endeavours unknown. This study is the starting point to fill this gap by pioneering and validating an elaborate behavioural test battery on street-living dogs. Therein, six common temperament tests (human-/conspecific-directed sociability, neophobia, tractability) and dog-human communication paradigms (pointing, inaccessible object) were adapted to the street conditions. We evaluated the feasibility of the test battery, the coding reliability of the measures, and investigated their temporal consistency in a retest of the same individuals six weeks later (test-retest reliability). The test battery proved feasible with most dogs participating in all subtests, and it showed satisfactory inter- and intra-rater reliability (0.84 and 0.93 respectively), providing evidence that complex behavioural tests can be conducted even in highly variable street conditions. Retesting revealed that some behaviours could be captured reliably across time, especially when the subtest was particularly engaging (e.g., human approach, point following). In contrast, the low retest reliability for subtests relying on sustained novelty and behaviours that were highly susceptible to disturbances (e.g., gazing) reflects the difficulties of street dog testing, including standardisation in disturbance-prone environments, ecology-dependent adaptation of methods, and intrinsic differences between pet and free-ranging dogs. With some adaptations, this test battery can be valuable in investigating cognition and behavioural profiles in such an understudied population as free-ranging dogs.

Village dogs match pet dogs in reading human facial expressions.

Most studies on dogs' cognitive skills in understanding human communication have been conducted on pet dogs, making them a role model for the species. However, pet dogs are just a minor and particular sample of the total dog world population, which would instead be better represented by free-ranging dogs. Since free-ranging dogs are still facing the selective forces of the domestication process, they indeed represent an important study subject to investigate the effect that such a process has had on dogs' behavior and cognition. Despite only a few studies on free-ranging dogs (specifically village dogs) having been conducted so far, the results are intriguing. In fact, village dogs seem to place a high value on social contact with humans and understand some aspects of humans' communication. In this study we aimed to investigate village dogs' ability in understanding a subtle human communicative cue: human facial expressions, and compared them with pet dogs, who have already provided evidence of this social skill. We tested whether subjects were able to distinguish between neutral, happy, and angry human facial expressions in a test mimicking a potential real-life situation, where the experimenter repeatedly performed one facial expression while eating some food, and ultimately dropped it on the ground. We found evidence that village dogs, as well as pet dogs, could distinguish between subtle human communicative cues, since they performed a higher frequency of aversive gazes (looking away) in the angry condition than in the happy condition. However, we did not find other behavioral effects of the different conditions, likely due to the low intensity of the emotional expression performed. We suggest that village dogs' ability in distinguishing between human facial expressions could provide them with an advantage in surviving in a human-dominated environment.

Similar behavioral but different endocrine responses to conspecific interactions in hand-raised wolves and dogs.

Domestication has altered dogs' conspecific social organization compared to their closest, non-domesticated relatives, gray wolves. Wolves live in packs whose survival depends on coordinated behavior, but dogs rely less on conspecifics, which predicts greater cohesiveness in wolf than dog packs. Endocrine correlates such as oxytocin and glucocorticoids modulate group cohesion resulting in species-specific differences in social interactions. We found that although wolves' and dogs' observable behavioral reactions to a territorial threat and separation from the pack were similar, hormonal responses differed. Wolves' but not dogs' oxytocin and glucocorticoid concentrations correlated positively with territorial behaviors and only wolves showed increased glucocorticoid concentrations after separation from their pack. Together, results suggest stronger emotional activation to threats to group integrity in wolves than dogs, in line with their socio-ecology.

Appeasement function of displacement behaviours? Dogs' behavioural displays exhibited towards threatening and neutral humans.

Appeasement signals are behavioural patterns displaying an animal's non-aggressive attitude and are hypothesized to reduce the aggressive behaviours in the receiver. In domestic dogs, specific displacement behaviours (i.e., behavioural patterns exhibited without an apparent function related to the ongoing situation), have been suggested to function as appeasement signals. To test this possibility, we assessed whether the occurrence of these behaviours was dependent on a social conflict context, predicting that, if displacement behaviours also function as appeasement signals, they should be more prevalent in a conflict vs. non-conflict context. Fifty-three dogs were exposed to two unfamiliar humans approaching them in either a mildly threatening or neutral way. We categorized the attitude of the dogs towards the strangers as "reactive", i.e., barking and lunging towards the stimulus, and "non-reactive", i.e., remaining passive in front of the stimuli. We coded dogs' displacement activities and modelled their duration or frequency as a function of the interaction between the test condition and the attitude of the dog. Displacement behaviours of "blinking", "nose licking" and "lip wiping" were associated with a "non-reactive" attitude, independently from the test condition, confirming an association with a non-aggressive intention. "Head turning" was associated with a "non-reactive" attitude in the threatening condition. In conclusion, dogs with a non-aggressive attitude exhibited more putative appeasement signals; however, these were not strictly associated with a conflict-ridden situation, calling for further investigation of their function.

Wolves and dogs fail to form reputations of humans after indirect and direct experience in a food-giving situation.

Reputation is a key component in social interactions of group-living animals and appears to play a role in the establishment of cooperation. Animals can form reputations of individuals by directly interacting with them or by observing them interact with a third party, i.e., eavesdropping. Previous research has focused on whether dogs (Canis lupus familiaris) can eavesdrop on humans because of their ability to cooperate with humans, however the results are mixed and if they can eavesdrop, it is unknown whether this ability evolved during the domestication process or whether it was inherited from their ancestor, wolves (Canis lupus). Our study investigated whether equally hand-raised, pack-living dogs and wolves can form reputations of humans in a food-giving situation through indirect and/or direct experience. The experimental procedure comprised three parts: baseline (to test whether the subject preferred a person prior to the experiment), observation and testing. In the observation phase, the subject observed two humans interact with a dog demonstrator-one acted generously and fed the dog, and the other acted selfishly and refused to feed the dog. The subject could then choose which person to approach in the test phase. In the following experience phase, the animals interacted directly with the same two humans who behaved either in a generous or selfish manner. Then, they were again given a choice whom to approach. We found that dogs and wolves, at the group level, did not differentiate between a generous or selfish partner after indirect or direct experience, but wolves were more attentive towards the generous person during the observation phase and some dogs and wolves did prefer the generous partner, at least after indirect and direct experience was combined. Our study suggests that reputation formation may be more difficult than expected for animals and we emphasise the importance of context when studying reputation formation in animals.

Audience effect on domestic dogs' behavioural displays and facial expressions.

In the present study we investigated the influence of positive and negative arousal situations and the presence of an audience on dogs' behavioural displays and facial expressions. We exposed dogs to positive anticipation, non-social frustration and social frustration evoking test sessions and measured pre and post-test salivary cortisol concentrations. Cortisol concentration did not increase during the tests and there was no difference in pre or post-test concentrations in the different test conditions, excluding a different level of arousal. Displacement behaviours of "looking away" and "sniffing the environment" occurred more in the frustration-evoking situations compared to the positive anticipation and were correlated with cortisol concentrations. "Ears forward" occurred more in the positive anticipation condition compared to the frustration-evoking conditions, was positively influenced by the presence of an audience, and negatively correlated to the pre-test cortisol concentrations, suggesting it may be a good indicator of dogs' level of attention. "Ears flattener", "blink", "nose lick", "tail wagging" and "whining" were associated with the presence of an audience but were not correlated to cortisol concentrations, suggesting a communicative component of these visual displays. These findings are a first step to systematically test which subtle cues could be considered communicative signals in domestic dogs.

Comparing wolves and dogs: current status and implications for human 'self-domestication'.

Based on claims that dogs are less aggressive and show more sophisticated socio-cognitive skills compared with wolves, dog domestication has been invoked to support the idea that humans underwent a similar 'self-domestication' process. Here, we review studies on wolf-dog differences and conclude that results do not support such claims: dogs do not show increased socio-cognitive skills and they are not less aggressive than wolves. Rather, compared with wolves, dogs seek to avoid conflicts, specifically with higher ranking conspecifics and humans, and might have an increased inclination to follow rules, making them amenable social partners. These conclusions challenge the suitability of dog domestication as a model for human social evolution and suggest that dogs need to be acknowledged as animals adapted to a specific socio-ecological niche as well as being shaped by human selection for specific traits.

Life experience rather than domestication accounts for dogs' increased oxytocin release during social contact with humans.

Dogs' increased human-directed sociability compared to wolves may be the result of increased oxytocin system activity and decreased stress responses, but comparative studies accounting for life experience are lacking. We compared hand-raised, pack-living wolves' and dogs' behavior and hormone concentrations after interacting with a closely bonded and a familiar human. Both preferred the bonded partner, but dogs showed less variability in human-directed sociability than wolves. Physical contact was not associated with oxytocin but correlated positively with glucocorticoids in the pack-living animals when the human was not bonded. To clarify the role of life experience, we tested pet dogs and found that oxytocin concentrations correlated positively with physical contact with their owners, while glucocorticoids remained unaffected. Results show that, given similar experiences, wolf-dog differences in human-directed sociability and associated hormones are subtle and indicate that factors related to life as a pet dog rather than domestication account for oxytocin release during human-dog interactions.

Artificially elevated oxytocin concentrations in pet dogs are associated with higher proximity-maintenance and gazing towards the owners.

The relationship between dogs and their owners is characterized by an affective and enduring bond. It has been suggested that oxytocin might be the underlying mechanism driving this relationship, however evidence is mixed. In this study we tested whether intranasally administered oxytocin (compared to saline) would influence dogs' behavioural synchrony and shared attention towards their owners. Each individuals' pre and post administration oxytocin concentrations (measured in urine) were included in the analyses. Urinary oxytocin concentrations after administrations were positively associated with dogs' duration of social proximity and looking behaviours towards their owners supporting the role of oxytocin in modulating dogs' human-directed social behaviours.

Validation of a commercial enzyme immunoassay to assess urinary oxytocin in humans.

Within the last decade, oxytocin (OT) has attracted a lot of attention in the context of various human social behaviors. Besides its importance in regulating physiological processes in females related to giving birth and lactation, OT is involved in the establishment and maintenance of social relationships, trust and emotion recognition. However, results are not always consistent across studies, which may partly be due to the incomplete validation of methods used to assess OT levels. Carefully validating a method before its use is of crucial importance to ensure that it can be used to accurately, reliably and repeatedly assess OT levels. With this study we evaluated a commercially available Enzyme Immunoassay to assess OT in human urine samples by conducting a careful analytical validation. Results indicate that, with regard to parallelism and immunoreactivity, human urinary OT can be assessed reliably. However, extraction methods need further improvement to optimize measures of accuracy and extraction efficiency, especially in the lower range of the assay system. Tests on OT stability indicate that OT is affected by degradation when stored at 4°C or room temperature. Storing urine samples over longer periods revealed that OT levels are most stable when stored as ethanol extracts at -20°C compared to being stored as samples at -20°C or -80°C. Although some of the validated parameters did not reach the intended quality criteria, this study highlights the importance of such in depth validation procedures and reporting results to make them available to researchers embarking on projects utilizing such methods.

Do dogs eavesdrop on human interactions in a helping situation?

Eavesdropping is the acquisition of information by observing third-party interactions. Considering dogs' (Canis lupus familiaris) dependence on humans, it would be beneficial for them to eavesdrop on human interactions to choose an appropriate partner to associate with. Previous studies have found that dogs preferred a human who acted generously or cooperatively towards another human over one who acted selfishly or non-cooperatively, however they often did not control for potential location biases. This study controlled for local enhancement and investigated whether dogs derive and act on information about unfamiliar humans through reputation-like inferences by observing third-party interactions. 42 dogs participated in the experiment, which consisted of an observation phase and a test phase. In the observation phase, the animals observed a human with a box of food ask for help to open it from two people-one was helpful and the other was not. The test phase consisted of the impossible task and a choice test. Half of the sample was tested in the experimental condition and the other half was tested in the side control condition, where the two people swapped positions before the test phase. The results of the impossible task showed that dogs only looked at the helpful person first when the people stayed on the same side as they did in the observation phase. In the choice test, dogs chose at random, regardless of whether the people stayed on the same side or swapped positions. Our findings provide tentative support for a local enhancement interpretation of eavesdropping.

What matters for cooperation? The importance of social relationship over cognition.

Cooperation is vital for the survival of many species and has been extensively researched at the ultimate level however, there is a considerable degree of variation within a given species in the extent of cooperative behaviours exhibited. Possible factors that have been discussed to contribute to this variation are the social relationship between the cooperating individuals, but also non-social factors such as inhibitory control. Investigating the performance of wolves, a highly cooperative species, in three experimental cooperative tasks; a coordination (string-pulling) task, a prosocial task and an inequity aversion task, we found that the social relationship between the partners had the largest effects on all tasks, while non-social factors (inhibition, learning speed, causal understanding and persistence) had rather unpredicted, or no effects. The results support the potential importance of relational factors, rather than motivation and cognitive abilities, in driving cooperative interactions.

No evidence for a relationship between breed cooperativeness and inequity aversion in dogs.

Inequity aversion, the resistance to inequitable outcomes, has been demonstrated in a wide variety of animal species. Inequity aversion was hypothesised to have co-evolved with cooperation but only limited evidence supports this. Dogs provide a suitable model species to test this hypothesis as dogs were previously shown to be inequity averse and dog breeds vary in the extent to which they were selected for cooperativeness. Here, we compared the response of 12 individuals of "cooperative worker" breeds with that of 12 individuals of "independent worker" breeds in the "paw task" previously used to demonstrate inequity aversion in dogs. We also compared the two breed groups' subsequent social behaviours in a food tolerance test and free interaction session. Although subjects in both breed groups were inequity averse, we found no considerable difference between the groups in the extent of the negative response to inequity or in the impact of the inequity on subsequent social behaviours. However, we found differences between the breed groups in the response to reward omission with cooperative breeds tending to work for longer than independent breeds. Additionally, in the free interaction session, individuals of cooperative breeds spent more time in proximity to their partner in the baseline condition than individuals of independent breeds. Overall, our results do not provide support for the hypothesis that inequity aversion and cooperation co-evolved. However, they illuminate potential differences in selection pressures experienced by cooperative worker and independent worker dog breeds throughout their evolutionary history.

The Effect of Domestication and Experience on the Social Interaction of Dogs and Wolves With a Human Companion.

The results of current wolf-dog studies on human-directed behaviors seem to suggest that domestication has acted on dogs' general attitudes and not on specific socio-cognitive skills. A recent hypothesis suggests that domestication may have increased dogs' overall sociability (hypersociability hypothesis). The aim of the present study was to test one aspect of the hypersociability hypothesis, whereby dogs should be more interested in social human contact compared to wolves, and to investigate the relative roles of both domestication and experience on the value that dogs attribute to human social contact. We compared equally raised wolves and dogs kept at the Wolf Science Center (WSCw, WSCd) but also dogs with different human socialization experiences i.e., pet dogs and free-ranging dogs. We presented subjects with a simple test, divided in two phases: in the Pre-test phase animals were exposed to two people in succession. One person invited the animal for a social/cuddle session (contact provider) and the other fed the animal (food provider). In the Test phase, animals could choose which of the two persons to approach, when both stood in a neutral posture. We directly compared WSCd with WSCw and free-ranging dogs with pet dogs. We found that in the Pre-test, WSCd and free-ranging dogs spent more time with the contact provider than WSCw and pet dogs, respectively. The results regarding the free-ranging dog and pet dog comparison were surprising, hence we conducted a follow-up testing pet dogs in a familiar, distraction-free area. Free-ranging dogs and this group of pet dogs did not differ in the time spent cuddling. In the test phase, WSCd were more likely than WSCw to approach the two experimenters. However, neither for the WSCd-WSCw comparison nor for the free-ranging dogs-pet dogs comparison, we could find a clear preference for one person over the other. Our findings support the idea that domestication has affected dogs' behavior in terms of their overall interest in being in proximity with a human partner also in case of dogs with a relatively sparse socialization experience (free-ranging dogs). However, it remains unclear what the driving motivation to interact with the human may be.

Why do dogs look back at the human in an impossible task? Looking back behaviour may be over-interpreted.

The impossible task paradigm has been extensively used to study the looking back behaviour in dogs. This behaviour is commonly considered a social problem-solving strategy: dogs facing an unsolvable task, soon give up and look back at the experimenter to ask for help. We aimed to test if the looking back in an impossible task does indeed represent a social problem-solving strategy. We used a modified version of the classic impossible task, in which the subjects simultaneously faced three possible and one impossible trials. Additionally, subjects were tested in four different conditions: social condition (with an unknown experimenter); asocial condition (subject alone); 'dummy' human condition (with a 'dummy' human); object condition (with a big sheet of cardboard). Finally, we compared two populations of dogs differing in their experience of receiving help from humans: 20 pet dogs tested in their houses and 31 free-ranging dogs tested in Morocco. We found that the pet dogs and free-ranging dogs had similar persistence in interacting with the impossible task in all conditions. Moreover, subjects looked back with similar latencies at the human, at the dummy human and at the object. Overall, pet dogs looked back longer at the human than free-ranging dogs. This could be interpreted as pet dogs being more attracted to humans and/or having a stronger association between humans and food than free-ranging dogs. Concluding, the looking back in an impossible task does not represent a problem-solving strategy. This behaviour seems rather linked to the subject's persistence, to the salience of the stimuli presented, and potentially to the past reinforcement history.

Investigating Indirect and Direct Reputation Formation in Asian Elephants (Elephas maximus).

Reputation is a key component in social interactions of group-living animals and appears to play a role in the establishment of cooperation. Animals can form a reputation of an individual by directly interacting with them or by observing them interact with a third party, i.e., eavesdropping. Elephants are an interesting taxon in which to investigate eavesdropping as they are highly cooperative, large-brained, long-lived terrestrial mammals with a complex social organisation. The aim of this study was to investigate whether captive Asian elephants (Elephas maximus) could form reputations of humans through indirect and/or direct experience in two different paradigms: (1) a cooperative string-pulling task and (2) a scenario requiring begging. Fourteen captive Asian elephants in Thailand participated in an experimental procedure that consisted of three parts: baseline, observation, and testing. In the observation phase, the subject saw a conspecific interact with two people-one cooperative/generous and one non-cooperative/selfish. The observer could then choose which person to approach in the test phase. The elephants were tested in a second session 2-5 days later. We found no support for the hypothesis that elephants can form reputations of humans through indirect or direct experience, but these results may be due to challenges with experimental design rather than a lack of capacity. We discuss how the results may be due to a potential lack of ecological validity in this study and the difficulty of assessing motivation and attentiveness in elephants. Furthermore, we highlight the importance of designing future experiments that account for the elephants' use of multimodal sensory information in their decision-making.

Wolves and dogs recruit human partners in the cooperative string-pulling task.

In comparison to non-human animals, humans are highly flexible in cooperative tasks, which may be a result of their ability to understand a partner's role in such interactions. Here, we tested if wolves and dogs could flexibly adjust their behaviour according to whether they needed a partner to solve a cooperative loose string-pulling paradigm. First, we presented animals with a delay condition where a human partner was released after the subject so that the animal had to delay pulling the string to enable coordinated pulling with the human partner. Subsequently, we investigated whether subjects would recruit a partner depending on whether they could operate the apparatus alone, or help from a partner was required. Both wolves and dogs successfully waited in the delay condition in 88% of the trials. Experimental subjects were also successful in recruiting a partner, which occurred significantly more often in the cooperation trials than in the solo pulling condition. No species differences were found in either experiment. These results suggest that both wolves and dogs have some understanding of whether a social partner is needed to accomplish a task, which enables behavioural coordination and cooperation.

The Role of Oxytocin in the Dog-Owner Relationship.

Oxytocin (OT) is involved in multiple social bonds, from attachment between parents and offspring to "friendships". Dogs are an interesting species in which to investigate the link between the oxytocinergic system and social bonds since they establish preferential bonds with their own species but also with humans. Studies have shown that the oxytocinergic system may be involved in the regulation of such inter-specific relationships, with both dogs and their owners showing an increase in OT levels following socio-positive interactions. However, no direct comparison has been made in dogs' OT reactivity following a social interaction with the owner vs. a familiar (but not bonded) person, so it is unclear whether relationship type mediates OT release during socio-positive interactions or whether the interaction per se is sufficient. Here we investigated OT reactivity in both dogs and owners, following a socio-positive interaction with each other or a familiar partner. Results showed neither the familiarity with the partner, nor the type of interaction affected OT reactivity (as measured in urine) in either dogs or owners. Given the recent mixed results on the role of oxytocin in dog-human interactions, we suggest there is a need for greater standardization of methodologies, an assessment of overall results taking into account 'publication bias' issues, and further studies investigating the role of relationship quality and interaction type on OT release.