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.

Dogs take into account the actions of a human partner in a cooperative task.

Humans stand out for their capacity to flexibly cooperate, possibly because they understand their partners' role. Researchers have explored if such understanding is unique to humans by assessing whether non-human species wait to manipulate a cooperative apparatus until a delayed partner arrives. If animals do wait, then it is assumed that they recognize the need for a partner. However, success in these tasks may be the result of social facilitation, while failure may be due to poor inhibitory control. Moreover, this approach does not test if animals take their partners' actions into account. Here we trained dogs to press a button simultaneously with their human partner. Afterwards, we tested them in several conditions to disentangle which elements of their partner's behaviour they take into account. Dogs waited to press the button until the delayed partner arrived, the button was available to the partner and the partner acted (pressed the button). We found no relationship between inhibitory control and success. We conclude that dogs are not merely reacting to the presence of their human partners, but are also taking their actions into account when coordinating with them.

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.

Is dogs' heritable performance in socio-cognitive tasks truly social?

Recently, Bray et al. (2021) showed that behavioural performance in cognitive tasks involving humans is highly heritable in dog puppies. Although the paper shows substantial heritability of specific behavioural traits, the absence of control conditions does not allow for strong support of the authors' claim that the cognitive performance they measured represents a special sensitivity to human cooperative-communicative acts.

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.

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.

Importance of a species' socioecology: Wolves outperform dogs in a conspecific cooperation task.

A number of domestication hypotheses suggest that dogs have acquired a more tolerant temperament than wolves, promoting cooperative interactions with humans and conspecifics. This selection process has been proposed to resemble the one responsible for our own greater cooperative inclinations in comparison with our closest living relatives. However, the socioecology of wolves and dogs, with the former relying more heavily on cooperative activities, predicts that at least with conspecifics, wolves should cooperate better than dogs. Here we tested similarly raised wolves and dogs in a cooperative string-pulling task with conspecifics and found that wolves outperformed dogs, despite comparable levels of interest in the task. Whereas wolves coordinated their actions so as to simultaneously pull the rope ends, leading to success, dogs pulled the ropes in alternate moments, thereby never succeeding. Indeed in dog dyads it was also less likely that both members simultaneously engaged in other manipulative behaviors on the apparatus. Different conflict-management strategies are likely responsible for these results, with dogs' avoidance of potential competition over the apparatus constraining their capacity to coordinate actions. Wolves, in contrast, did not hesitate to manipulate the ropes simultaneously, and once cooperation was initiated, rapidly learned to coordinate in more complex conditions as well. Social dynamics (rank and affiliation) played a key role in success rates. Results call those domestication hypotheses that suggest dogs evolved greater cooperative inclinations into question, and rather support the idea that dogs' and wolves' different social ecologies played a role in affecting their capacity for conspecific cooperation and communication.

Dogs and wolves do not differ in their inhibitory control abilities in a non-social test battery.

Being able to inhibit certain behaviours is of clear advantage in various situations. In particular, it has been suggested that inhibitory control plays a role in problem-solving and cooperation. Interspecific differences in the capacity for inhibitory control have been attributed to social and ecological factors, while one additional factor, namely domestication, has received only little attention so far. Dogs are an interesting species to test the effects of socio-ecological factors and also the influence of domestication on inhibitory control abilities. While dogs might have been selected for enhanced inhibition skills during domestication, the predictions derived from their socio-ecological background are reversed. Wolves are cooperative hunters and breeders, while dogs predominately scavenge and raise their young alone, accordingly, it would be predicted that dogs show impaired inhibitory control abilities since they no longer rely on these coordinated actions. To test these hypotheses, we assessed inhibitory control abilities in dogs and wolves raised and kept under similar conditions. Moreover, considering the problem of context-specificity in inhibitory control measures, we employed a multiple-test-approach. In line with previous studies, we found that the single inhibition tests did not correlate with each other. Using an exploratory approach, we found three components that explained the variation of behaviours across tests: motivation, flexibility, and perseveration. Interestingly, these inhibition components did not differ between dogs and wolves, which contradicts the predictions based on their socio-ecological backgrounds but also suggests that at least in tasks with minimal human influence, domestication did not affect dogs' inhibitory control abilities, thus raising questions in regard to the selection processes that might have affected inhibitory control abilities during the course of domestication.

Analytical validation of an Enzyme Immunoassay for the measurement of urinary oxytocin in dogs and wolves.

Assessing changes in oxytocin (OT) levels in response to a variety of social stimuli has become of major interest in the field of behavioral endocrinology. OT is involved in the regulation of various aspects of social behavior such as tolerance, and the formation and maintenance of social bonds but also the regulation of stress. All of these aspects have been identified as potential targets of selection during the domestication process. Therefore, comparing the role of the oxytocinergic system in various aspects of dog and wolf social behavior, might help to understand whether this system was involved in the domestication process. Studies assessing OT levels in dogs and wolves have used invasively collected plasma and serum samples and non-invasively collected urine samples. However, when using an assay system on a new species a careful and complete validation of the method is of crucial importance, and to date no proper validation, to assess urinary OT levels in dogs and wolves, has been reported. We therefore conducted an analytical validation of an Enzyme Immunoassay (EIA) for the measurement of OT in urine of dogs and wolves, using a commercially available EIA. Stability tests revealed that OT levels degrade over time when stored at 4 °C, but are little affected by repeated thawing. In addition, our results indicate that the variance in OT levels is slightly lower when phosphoric acid is added following collection to prevent OT degradation. Long term storage tests revealed that urinary OT levels are least variable when stored as extracts in ethanol at -20 °C, rather than as unextracted urine samples. Validation results were acceptable with regard to parallelism, but values for accuracy and extraction efficiency were not meeting the standard criteria usually applied to steroid EIAs, especially when assessed for the lower range of the assay. The results of this study highlight the importance of an analytical assay validation, since even if validation parameters are not optimal, if published, they allow readers to estimate the relevance of studies using the validated method.

Cognitive Aging in Dogs.

A decline in the physical or mental health of older dogs can be a challenge for the owners, whose relationship with their dog is compromised by the cognitive and behavioral changes in their dogs. Although dog owners tend to consider many physiological and behavioral changes in old dogs as part of the normal aging process, it is important to differentiate between normal aging and pathologic aging, since behavioral changes may be the first indication of declining health and welfare in old dogs. Most reviews on cognitive aging in dogs have focused on translational approaches to human Alzheimer's disease; from a practical perspective, however, understanding normal cognitive aging in pet dogs and screening cognitively affected dogs are important in their own right. Here we review the literature on different cognitive functions that decline during aging, signs of cognitive dysfunction, screening methods, and preventive measures for age-related cognitive decline. Moreover, we discuss the drawbacks of using questionnaires as subjective measures of aging and propose the development of objective methods to distinguish normal cognitive aging from severe cognitive dysfunction. We suggest that multi-targeted approaches that combine owner-evaluated questionnaires with neuropsychological tests can be most effective in screening cognitively affected dogs from normally aging dogs. Regarding preventive measures, we conclude that combinations of dietary intervention and behavioral enrichment may be more beneficial than single-pathway manipulations in delaying cognitive aging or retaining various cognitive functions during aging.

Inequity aversion in dogs: a review.

The study of inequity aversion in animals debuted with a report of the behaviour in capuchin monkeys (Cebus apella). This report generated many debates following a number of criticisms. Ultimately, however, the finding stimulated widespread interest, and multiple studies have since attempted to demonstrate inequity aversion in various other non-human animal species, with many positive results in addition to many studies in which no response to inequity was found. Domestic dogs represent an interesting case as, unlike many primates, they do not respond negatively to inequity in reward quality but do, however, respond negatively to being unrewarded in the presence of a rewarded partner. Numerous studies have been published on inequity aversion in dogs in recent years. Combining three tasks and seven peer-reviewed publications, over 140 individual dogs have been tested in inequity experiments. Consequently, dogs are one of the best studied species in this field and could offer insights into inequity aversion in other non-human animal species. In this review, we summarise and critically evaluate the current evidence for inequity aversion in dogs. Additionally, we provide a comprehensive discussion of two understudied aspects of inequity aversion, the underlying mechanisms and the ultimate function, drawing on the latest findings on these topics in dogs while also placing these developments in the context of what is known, or thought to be the case, in other non-human animal species. Finally, we highlight gaps in our understanding of inequity aversion in dogs and thereby identify potential avenues for future research in this area.

Is a local sample internationally representative? Reproducibility of four cognitive tests in family dogs across testing sites and breeds.

A fundamental precept of the scientific method is reproducibility of methods and results, and there is growing concern over the failure to reproduce significant results. Family dogs have become a favoured species in comparative cognition research, but they may be subject to cognitive differences arising from genetic (breeding lines) or cultural differences (e.g. preferred training methods). Such variation is of concern as it affects the validity and generalisability of experimental results. Despite its importance, this problem has not been specifically addressed to date. Therefore, we aimed to test the influence of three factors on reproducibility: testing site (proximal environment), breed and sex (phenotype). The same experimenter tested cognitive performance by more than 200 dogs in four experiments. Additionally, dogs' performance was tested in an obedience task administered by the owner. Breed of dog and testing site were found to influence the level of performance only mildly, and only in a means-end experiment and the obedience task. Our findings demonstrate that by applying the same test protocols on sufficiently large samples, the reported phenomena in these cognitive tests can be reproduced, but slight differences in performance levels can occur between different samples. Accordingly, we recommend the utilisation of well-described protocols supported by video examples of the whole experimental procedure. Findings should focus on the main outcome variables of the experiments, rather than speculating about the general importance of small or secondary performance outcomes which are more susceptible to random or local noise.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Individual and group level trajectories of behavioural development in Border collies.

In order to assess dogs' personality changes during ontogeny, a cohort of 69 Border collies was followed up from six to 18-24 months. When the dogs were 6, 12, and 18-24 months old, their owners repeatedly filled in a dog personality questionnaire (DPQ), which yielded five personality factors divided into fifteen facets. All five DPQ factors were highly correlated between the three age classes, indicating that the dogs' personality remained consistent relative to other individuals. Nonetheless, at the group level significant changes with age were found for four of the five DPQ factors. Fearfulness, Aggression towards People, Responsiveness to Training and Aggression towards Animals increased with age; only Activity/Excitability did not change significantly over time. These changes in DPQ factor scores occurred mainly between the ages of 6 and 12 months, although some facets changed beyond this age. No sex differences were found for any of the tested factors or facets, suggesting that individual variation in personality was greater than male/female differences. There were significant litter effects for the factors Fearfulness, Aggression towards People and Activity/Excitability, indicating either a strong genetic basis for these traits or a high influence of the shared early environment. To conclude, from the age of six months, consistency in personality relative to other individuals can be observed in Border collies. However, at the group level, increases in fearful and aggressive behaviours occur up to 12 months and for some traits up to two years, highlighting the need for early interventions. Follow-up studies are needed to assess trajectories of personality development prior to six months and after two years, and to include a wider variety of breeds.

Testing the myth: tolerant dogs and aggressive wolves.

Cooperation is thought to be highly dependent on tolerance. For example, it has been suggested that dog-human cooperation has been enabled by selecting dogs for increased tolerance and reduced aggression during the course of domestication ('emotional reactivity hypothesis'). However, based on observations of social interactions among members of captive packs, a few dog-wolf comparisons found contradictory results. In this study, we compared intraspecies aggression and tolerance of dogs and wolves raised and kept under identical conditions by investigating their agonistic behaviours and cofeeding during pair-wise food competition tests, a situation that has been directly linked to cooperation. We found that in wolves, dominant and subordinate members of the dyads monopolized the food and showed agonistic behaviours to a similar extent, whereas in dogs these behaviours were privileges of the high-ranking individuals. The fact that subordinate dogs rarely challenged their higher-ranking partners suggests a steeper dominance hierarchy in dogs than in wolves. Finally, wolves as well as dogs showed only rare and weak aggression towards each other. Therefore, we suggest that wolves are sufficiently tolerant to enable wolf-wolf cooperation, which in turn might have been the basis for the evolution of dog-human cooperation (canine cooperation hypothesis).

Long-term fidelity of foraging techniques in common marmosets (Callithrix jacchus).

The formation of behavioral traditions has been considered as one of the main building blocks of culture. Numerous studies on social learning in different animal species provide evidence for their capability of successful transmission of information. However, questions concerning the memory and maintenance of this information have received comparably little attention. After the innovation and initial spread of a novel behavior, the behavior should stabilize and be maintained over time. Otherwise, the behavioral pattern might collapse and no tradition formation would be possible. The aim of this study was to investigate long-term preferences in a two-action manipulation task in common marmosets (Callithrix jacchus). Three captive family groups (23 individuals in total) were trained on one of two possible techniques to open a wooden box and gain access to a food reward, by either pulling or pushing a flap door. The training phase took place in a family group setting, while the test phase was conducted individually. Although the subjects could experience the alternative technique during the test sessions, the majority preferentially used the technique learned in the group setting. Moreover, the subjects were re-tested six times over a period of more than four years, in order to examine the fidelity of their preferences. The longest break without exposure the task lasted for 3.5 years. In all tests, the marmosets showed a similar preference as in the first test block shortly after the training. To our knowledge, this is the first lab study that experimentally demonstrates memory and fidelity of experimentally seeded information in a manipulation task over a time period of several years, supporting the assumption that socially learned foraging techniques can lead to relatively stable behavioral traditions.

Dogs' use of the solidity principle: revisited.

A wealth of comparative data has been accumulated over the past decades on how animals acquire and use information about the physical world. Domestic dogs have typically performed comparably poorly in physical cognition tasks, though in a recent study Kundey et al. (Anim Cogn 13:497-505, 2010) challenged this view and concluded that dogs understand that objects cannot pass through solid barriers. However, the eight subjects in the study of Kundey et al. may have solved the task with the help of perceptual cues, which had not been controlled for. Here, we tested dogs with a similar task that excluded these cues. In addition, unlike the set-up of Kundey et al., our set-up allowed the subjects to observe the effect of the solid barrier. Nevertheless, all 28 subjects failed to solve this task spontaneously and showed no evidence of learning across 50 trials. Our results therefore call into question the earlier suggestion that dogs have, or can acquire, an understanding of the solidity principle.

Dogs learn to solve the support problem based on perceptual cues.

Numerous recent studies have investigated how animals solve means-end tasks and unraveled considerable variation in strategies used by different species. Domestic dogs (Canis familiaris) have typically performed comparably poorly in physical cognition tasks, but a recent study showed that they can solve the on-off condition of the support problem, where they are confronted with two boards, one with a reward placed on it and the other with a reward placed next to it. To explore which strategies dogs use to solve this task, we first tested 37 dogs with the on-off condition tested previously and then tested subjects that passed this condition with three transfer tasks. For the contact condition, the inaccessible reward was touching the second board. For the perceptual containment condition, the inaccessible reward was surrounded on three sides by the second board, but not supported by it, whereas for the gap condition, discontinuous boards were used. Unlike in the previous study, our subjects did not perform above chance level in the initial trials of the on-off condition, but 13 subjects learned to solve it. Their performance in the transfer tasks suggests that dogs can learn to solve the support problem based on perceptual cues, that they can quickly adopt new cues when old ones become unreliable, but also that some apparently inherent preferences are hard to overcome. Our study contributes to accumulating evidence demonstrating that animals typically rely on a variety of perceptual cues to solve physical cognition tasks, without developing an understanding of the underlying causal structure.

Free-ranging dogs match a human's preference in a foraging task.

Social learning is a mechanism used by many species to efficiently gain information about their environment. Although many animals live in an environment where members of other species are present, little is known about interspecific social learning. Domesticated and urbanized species provide the opportunity to investigate whether nonhuman animals can learn from heterospecifics such as humans, who are integral parts of their social landscape. Although domestic dogs Canis familiaris have been intensively researched for their ability to learn from humans, most studies have focused on dogs living as pets. However, free-ranging dogs represent the majority of the world's dog population, they live alongside humans, scavenge on human refuse, and are subject to natural and sexual selection. Thus, free-ranging dogs with extensive exposure to humans and their artifacts provide the opportunity to investigate interspecific social learning in a naturalistic setting, where learning from humans might be a benefit for them. Here we tested individual free-ranging dogs in a between-subject design: Dogs in the control group could spontaneously choose between two novel and differently patterned food-delivering boxes. In the experimental group, instead, dogs could first observe an unfamiliar human approaching and eating from 1 of the 2 boxes. We provide the first evidence that free-ranging dogs match the choice of an unfamiliar human. These results show that at least simple forms of interspecific social learning might be involved in dogs' success in living alongside humans in a complex urbanized environment.

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.