Leanne Proops

Cross-modal individual recognition in domestic horses (Equus caballus).

Individual recognition is considered a complex process and, although it is believed to be widespread across animal taxa, the cognitive mechanisms underlying this ability are poorly understood. An essential feature of individual recognition in humans is that it is cross-modal, allowing the matching of current sensory cues to identity with stored information about that specific individual from other modalities. Here, we use a cross-modal expectancy violation paradigm to provide a clear and systematic demonstration of cross-modal individual recognition in a nonhuman animal: the domestic horse. Subjects watched a herd member being led past them before the individual went of view, and a call from that or a different associate was played from a loudspeaker positioned close to the point of disappearance. When horses were shown one associate and then the call of a different associate was played, they responded more quickly and looked significantly longer in the direction of the call than when the call matched the herd member just seen, an indication that the incongruent combination violated their expectations. Thus, horses appear to possess a cross-modal representation of known individuals containing unique auditory and visual/olfactory information. Our paradigm could provide a powerful way to study individual recognition across a wide range of species.

Attributing attention: the use of human-given cues by domestic horses (Equus caballus)

Recent research has shown that domestic dogs are particularly good at determining the focus of human attention, often outperforming chimpanzees and hand-reared wolves. It has been suggested that the close evolutionary relationship between humans and dogs has led to the development of this ability; however, very few other domestic species have been studied. We tested the ability of 36 domestic horses to discriminate between an attentive and inattentive person in determining whom to approach for food. The cues provided were body orientation, head orientation or whether the experimenters’ eyes were open or closed. A fourth, mixed condition was included where the attentive person stood with their body facing away from the subjects but their head turned towards the subject while the inattentive person stood with their body facing the subject but their head turned away. Horses chose the attentive person significantly more often using the body cue, head cue, and eye cue but not the mixed cue. This result suggests that domestic horses are highly sensitive to human attentional cues, including gaze. The possible role of evolutionary and environmental factors in the development of this ability is discussed.

Cross-modal individual recognition in domestic horses (Equus caballus) extends to familiar humans

It has recently been shown that some non-human animals can cross-modally recognize members of their own taxon. What is unclear is just how plastic this recognition system can be. In this study, we investigate whether an animal, the domestic horse, is capable of spontaneous cross-modal recognition of individuals from a morphologically very different species. We also provide the first insights into how cross-modal identity information is processed by examining whether there are hemispheric biases in this important social skill. In our preferential looking paradigm, subjects were presented with two people and playbacks of their voices to determine whether they were able to match the voice with the person. When presented with familiar handlers subjects could match the specific familiar person with the correct familiar voice. Horses were significantly better at performing the matching task when the congruent person was standing on their right, indicating marked hemispheric specialization (left hemisphere bias) in this ability. These results are the first to demonstrate that cross-modal recognition in animals can extend to individuals from phylogenetically very distant species. They also indicate that processes governed by the left hemisphere are central to the cross-modal matching of visual and auditory information from familiar individuals in a naturalistic setting.

The use of human-given cues by domestic horses, Equus caballus, during an object choice task

Selection pressures during domestication are thought to lead to an enhanced ability to use human-given cues. Horses fulfil a wide variety of roles for humans and have been domesticated for at least 5000 years but their ability to read human cues has not been widely studied. We tested the ability of 28 horses to attend to human-given cues in an object choice task. We included five different cues: distal sustained pointing, momentary tapping, marker placement, body orientation and gaze (head) alternation. Horses were able to use the pointing and marker placement cues spontaneously but not the tapping, body orientation and gaze alternation cues. The overall pattern of responding suggests that horses may use cues that provide stimulus enhancement at the time of choice and do not have an understanding of the communicative nature of the cues given. As such, their proficiency at this task appears to be inferior to that of domestic dogs, Canis lupus familiaris, but similar to that of domestic goats, Caprus hircus.

Spatial cognition and perseveration by horses, donkeys and mules in a simple A not B detour task.

We investigated perseveration and detour behaviour in 36 equids (Equuscaballus, E. asinus, E. caballus × E. asinus) and compared these data to those of a previous study on domestic dogs (Canisfamiliaris). The animals were required to make a detour through a gap at one end of a straight barrier in order to reach a visible target. After one, two, three or four repeats (A trials), the gap was moved to the opposite end of the barrier (B trials). We recorded initial deviations from the correct solution path and the latency to crossing the barrier. In the A trials, mules crossed the barrier significantly faster than their parental species, the horses and donkeys. In the B trials, following the change of gap location, all species showed a reduction in performance. Both dogs and horses exhibited significant spatial perseveration, going initially to the previous gap location. Donkeys and mules, however, performed at chance level. Our results suggest that hybrid vigour in mules extends to spatial abilities.

Social relations in a mixed group of mules, ponies and donkeys reflect differences in equid type

Donkeys and mules are frequently kept as companion animals for horses and ponies, with these different equids often being considered a homogenous group. However, the extent to which domestic equids form inter-specific bonds and display similar social behaviour when living in a mixed herd has not previously been studied. Here we compare the social organization of these three (sub)species when housed together, providing the first systematic analysis of how genetic hybridization is expressed in the social behaviour of mules. A group of 16 mules, donkeys and ponies was observed for 70h and preferred associates, dominance rank and the linearity of the groups hierarchy was determined. The different equids formed distinct affiliative groups that were ordered in a linear hierarchy with ponies as the most dominant, mules in the middle ranks and donkeys in the lowest ranks. Within each equid subgroup, the strength of the hierarchy also varied. Thus in the present study, the three (sub)species displayed different social organization and levels of dominance and preferred to associate with animals of the same equid type, given the opportunity. These results suggest that different domestic equid (sub)species display variations in social behaviour that are likely to have a strong genetic basis.

Horses discriminate between facial expressions of conspecifics

In humans, facial expressions are rich sources of social information and have an important role in regulating social interactions. However, the extent to which this is true in non-human animals, and particularly in non-primates, remains largely unknown. Therefore we tested whether domestic horses (Equus caballus) could discriminate between facial expressions of their conspecifics captured in different contexts, and whether viewing these expressions elicited functionally relevant reactions. Horses were more likely to approach photographic stimuli displaying facial expressions associated with positive attention and relaxation, and to avoid stimuli displaying an expression associated with aggression. Moreover, differing patterns of heart rate changes were observed in response to viewing the positive anticipation and agonistic facial expressions. These results indicate that horses spontaneously discriminate between photographs of unknown conspecifics portraying different facial expressions, showing appropriate behavioural and physiological responses. Thus horses, an animal far-removed from the primate lineage, also have the ability to use facial expressions as a means of gaining social information and potentially regulating social interactions.

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. Although 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 can 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 that 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.

Domestic horses (Equus caballus) prefer to approach humans displaying a submissive body posture rather than a dominant body posture

Signals of dominance and submissiveness are central to conspecific communication in many species. For domestic animals, sensitivities to these signals in humans may also be beneficial. We presented domestic horses with a free choice between two unfamiliar humans, one adopting a submissive and the other a dominant body posture, with vocal and facial cues absent. Horses had previously been given food rewards by both human demonstrators, adopting neutral postures, to encourage approach behaviour. Across four counterbalanced test trials, horses showed a significant preference for approaching the submissive posture in both the first trial and across subsequent trials, and no individual subject showed an overall preference for dominant postures. There was no significant difference in latency to approach the two postures. This study provides novel evidence that domestic horses may spontaneously discriminate between, and attribute communicative significance to, human body postures of dominance; and further, that familiarity with the signaller is not a requirement for this response. These findings raise interesting questions about the plasticity of social signal perception across the species barrier.

Horses give functionally relevant responses to human facial expressions of emotion: a response to Schmoll (2016).

Our paper demonstrates that horses show a quicker increase in heart rate when presented with photographic stimuli depicting angry versus happy human faces. We also use lateralized looking at each stimulus as a means of investigating how the image is perceived and found a strong left gaze/right