Social cognition in domestic horses (Equus caballus)

The social intelligence hypothesis states that the main selection pressures driving increases in brain-to-body ratio are social rather than ecological. The domestic horse is an ideal animal to study within this framework because horses possess rich social lives but inhabit simple ecological environments. Here I assess the abilities of horses within two broad areas of social cognition; the classification of, and the use of information obtained from, social partners. In Section One I demonstrate that horses are capable of cross-modal individual recognition of conspecifics, an ability not previously demonstrated conclusively outside of humans. This ability extends to identifying familiar human companions suggesting that recognition systems are highly plastic in the individuals they can encode. These results also provide the first insights into the brain mechanisms involved in this process by revealing a clear left hemisphere bias in discriminatory ability. In Section Two I investigate the extent to which horses are capable of reading human attentional and communicative cues. It has been suggested that this skill was selected for through the process of domestication, however there have been no systematic studies of domestic animals other than the domestic dog. I found that horses were indeed highly skilled at determining if people were paying attention to them. In contrast they tended to only use basic stimulus enhancement cues to choose a rewarded bucket. A further study of young horses indicated that the ability to detect human attention requires significant experience to develop fully whereas the ability to use stimulus enhancement cues in an object choice task appears to require far less (if any) experience to develop. Overall my thesis extends our knowledge of comparative social cognition and in particular our knowledge of social cognition in horses. Taken together, these results clearly demonstrate that horses do indeed possess some complex socio-cognitive skills

Animals remember previous facial expressions that specific humans have exhibited

For humans, facial expressions are important social signals and how we perceive specific individuals may be influenced by subtle emotional cues that they have given us in past encounters. A wide range of animal species are also capable of discriminating the emotions of others through facial expressions [1–5], and it is clear that remembering emotional experiences with specific individuals could have clear benefits for social bonding and aggression avoidance when these individuals are encountered again. While there is evidence that non-human animals are capable of remembering the identity of individuals who have directly harmed them [6,7], it is not known whether animals may form lasting memories of specific individuals simply by observing subtle emotional expressions that they exhibit on their faces. Here we conducted controlled experiments in which domestic horses were presented with a photograph of an angry or happy human face and several hours later saw the person who had given the expression in a neutral state. Short-term exposure to the facial expression was enough to generate clear differences in subsequent responses to that individual (but not to a different mismatched person), consistent with the past angry expression having been perceived negatively and the happy expression positively. Both humans were blind to the photograph the horses had seen. Our results provide clear evidence that some non-human animals can effectively eavesdrop on the emotional state cues that humans reveal on a moment-to-moment basis, using their memory of these to guide future interactions with particular individuals

The responses of young domestic horses (Equus caballus) to human-given cues

It has been suggested that the process of domestication, at least in some species, has led to an innate predisposition to be skilled at reading human communicative and attentional cues. Adult domestic horses (Equus caballus) are highly sensitive to subtle bodily cues when determining if a person is attending to them but they are less adept at using human communicative cues in object choice tasks. Here we provide the first study into the ontogeny of such skills in order to gain insights into the mechanisms underlying these abilities. Compared with adult horses, youngsters under the age of three could use body orientation but not more subtle cues such as head movement and open/closed eyes to correctly choose an attentive person to approach for food. Across two object choice experiments, the performance of young horses was comparable to that of adult horses – subjects were able to correctly choose a rewarded bucket using marker placement, pointing and touching cues but could not use body orientation, gaze, elbow pointing or tapping cues. Taken together these results do not support the theory that horses possess an innate predisposition to be particularly skilled at using human cues. Horses’ ability to determine whether humans are attending to them using subtle body cues appears to require significant experience to fully develop and their perhaps less remarkable use of limited cues in object choice tasks, although present at a much earlier age, is likely to reflect a more general learning ability related to stimulus enhancement rather than a specific ‘human-reading’ skill

Rising up to the challenge of their rivals: Mare infidelity intensifies stallion response to playback of aggressive conspecific vocalizations

Management tools like immunocontraception can alter the behavior of target animals, but the extent to which they affect non-target individuals has received less attention. The feral horse (Equus caballus) population on Shackleford Banks, North Carolina is an ideal system with which these questions may be explored, as management of the population with the immunocontraceptive agent porcine zona pellucida (PZP) has resulted in an increased propensity for females to change social groups and thus, decreased social stability. During the study, on average, females made 1.4 group changes per day (range = 0—18.5 group changes per day): females previously treated with PZP made 1.8 group changes per day, while females that had never been treated made 1.2 group changes per day. Between May and August, 2017, we used playbacks of aggressive male vocalizations (squeals) and human voices (reciting “hello horse”) to assess changes in stallion responses to male rivals versus socially irrelevant stimuli in the context of female turnover. Over the course of the study, males were observed for 9.4 hours on average (range = 2.4—20.5 hr). Males spent more time vigilant (estimate = 12.431, P = 0.016, ̅squeal = 30 s, ̅control = 19 s) and were more likely to approach the speaker following squeal playbacks than controls (estimate = 2.325, P = 0.039). Males’ latency to return to normal behaviors varied depending on whether the playback was conducted in the weeks before, during, or after group changes occurred (P = 0.025, ̅before = 26 s, ̅during = 39 s, ̅after = 53 s). Male responses were not affected by the total number of female group changes a male experienced during the observation period (P \u3e 0.4), suggesting the effects are more context-dependent and not long-lasting. These findings suggest mare turnover can impact stallion responsiveness to potential rivals. As previously contracepted mares change groups more often than untreated mares and stallions exhibit prolonged responses to aggressive vocalizations after experiencing a female group change, contraception-induced changes to mare behavior may lead to increased male aggression in response to intruding rivals, which could be associated with greater energy expenditure. Finally, our work demonstrates that playback experiments are a useful tool for studying feral horse behavior in the wild. As the need for population control of different species continues to expand, rigorous investigations of immunocontraception’s effects on non-target animals are critical if agencies are to manage populations most effectively

Functionally relevant responses to human facial expressions of emotion in the domestic horse (Equus caballus)

Whether non-human animals can recognize human signals, including emotions, has both scientific and applied importance, and is particularly relevant for domesticated species. This study presents the first evidence of horses’ abilities to spontaneously discriminate between positive (happy) and negative (angry) human facial expressions in photographs. Our results showed that the angry faces induced responses indicative of a functional understanding of the stimuli: horses displayed a left-gaze bias (a lateralization generally associated with stimuli perceived as negative) and a quicker increase in heart rate (HR) towards these photographs. Such lateralized responses towards human emotion have previously only been documented in dogs, and effects of facial expressions on HR have not been shown in any heterospecific studies. Alongside the insights that these findings provide into interspecific communication, they raise interesting questions about the generality and adaptiveness of emotional expression and perception across species

Slow blink eye closure in shelter cats Is related to quicker adoption

The process of domestication is likely to have led to the development of adaptive interspecific social abilities in animals. Such abilities are particularly interesting in less gregarious animals, such as cats. One notable social behaviour that cats exhibit in relation to humans is the slow blink sequence, which our previous research suggests can function as a form of positive communication between cats and humans. This behaviour involves the production of successive half blinks followed by either a prolonged narrowing of the eye or an eye closure. The present study investigates how cat (n = 18) slow blink sequences might affect human preferences during the adoption of shelter cats. Our study specifically tested (1) whether cats’ propensity to respond to human-initiated slow blinking was associated with their speed of rehoming from a shelter environment, and (2) whether cats’ anxiety around humans was related to their tendency to slow blink. Our experiments demonstrated that cats that showed an increased number of and longer eye closures in response to human slow blinks were rehomed faster, and that nervous cats, who had been identified as needing desensitisation to humans, tended to spend more time producing slow blink sequences in response to human slow blinks than a non-desensitisation group. Collectively, these results suggest that the cat slow blink sequence is perceived as positive by humans and may have a dual function—occurring in both affiliative and submissive contexts

Non-random associations in group housed rats (Rattus norvegicus)

Ecological factors, such as predation, have traditionally been used to explain sociability. However, it is increasingly recognised that individuals within a group do not associate randomly, and that these non-random associations can generate fitness advantages. The majority of the empirical evidence on differentiated associations in group-living mammals, however, comes from a limited number of taxa and we still know very little about their occurrence and characteristics in some highly social species, such as rats (Rattus spp.). Here, using network analysis, we quantified association patterns in four groups of male fancy rats. We found that the associations between rats were not randomly distributed and that most individuals had significantly more preferred/avoided associates than expected by random. We also found that these preferences can be stable over time, and that they were not influenced by individuals’ rank position in the dominance hierarchy. Our findings are consistent with work in other mammals, but contrast with the limited evidence available for other rat strains. While further studies in groups with different demographic composition are warranted to confirm our findings, the occurrence of differentiated associations in all male groups of rats have important implications for the management and welfare of captive rat populations