Studying vocal correlates of emotions is important to provide a better understanding of the evolution of emotion expression through cross-species comparisons. Emotions are composed of two main dimensions: emotional arousal (calm versus excited) and valence (negative versus positive). These two dimensions could be encoded in different vocal parameters (segregation of information) or in the same parameters, inducing a trade-off between cues indicating emotional arousal and valence. We investigated these two hypotheses in horses. We placed horses in five situations eliciting several arousal levels and positive as well as negative valence. Physiological and behavioral measures collected during the tests suggested the presence of different underlying emotions. First, using detailed vocal analyses, we discovered that all whinnies contained two fundamental frequencies (“F0” and “G0”), which were not harmonically related, suggesting biphonation. Second, we found that F0 and the energy spectrum encoded arousal, while G0 and whinny duration encoded valence. Our results show that cues to emotional arousal and valence are segregated in different, relatively independent parameters of horse whinnies. Most of the emotion-related changes to vocalizations that we observed are similar to those observed in humans and other species, suggesting that vocal expression of emotions has been conserved throughout evolution.

Vocal expression of emotions has been suggested to be conserved throughout evolution. However, since vocal indicators of emotions have never been compared between closely related species using similar methods, it remains unclear whether this is the case. Here, we investigated vocal indicators of emotional valence (negative versus positive) in Przewalski’s horses, in order to find out if expression of valence is similar between species and notably among Equidae through a comparison with previous results obtained in domestic horse whinnies. We observed Przewalski’s horses in naturally occurring contexts characterised by positive or negative valence. As emotional arousal (bodily activation) can act as a confounding factor in the search for indicators of valence, we controlled for its effect on vocal parameters using a behavioural indicator (movement). We found that positive and negative situations were associated with specific types of calls. Additionally, the acoustic structure of calls differed according to the valence. There were some similarities but also striking differences in expression of valence between Przewalski’s and domestic horses, suggesting that vocal expression of emotional valence, unlike emotional arousal, could be species specific rather than conserved throughout evolution.

BackgroundNon-human animals often produce different types of vocalisations in negative and positive contexts (i.e. different valence), similar to humans, in which crying is associated with negative emotions and laughter is associated with positive ones. However, some types of vocalisations (e.g. contact calls, human speech) can be produced in both negative and positive contexts, and changes in valence are only accompanied by slight structural differences. Although such acoustically graded signals associated with opposite valence have been highlighted in some species, it is not known if conspecifics discriminate them, and if contagion of emotional valence occurs as a result. We tested whether domestic horses perceive, and are affected by, the emotional valence of whinnies produced by both familiar and unfamiliar conspecifics. We measured physiological and behavioural reactions to whinnies recorded during emotionally negative (social separation) and positive (social reunion) situations.ResultsWe show that horses perceive acoustic cues to both valence and familiarity present in whinnies. They reacted differently (respiration rate, head movements, height of the head and latency to respond) to separation and reunion whinnies when produced by familiar, but not unfamiliar individuals. They were also more emotionally aroused (shorter inter-pulse intervals and higher locomotion) when hearing unfamiliar compared to familiar whinnies. In addition, the acoustic parameters of separation and reunion whinnies affected the physiology and behaviour of conspecifics in a continuous way. However, we did not find clear evidence for contagion of emotional valence.ConclusionsHorses are thus able to perceive changes linked to emotional valence within a given vocalisation type, similar to perception of affective prosody in humans. Whinnies produced in either separation or reunion situations seem to constitute acoustically graded variants with distinct functions, enabling horses to increase their apparent vocal repertoire size.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0193-1) contains supplementary material, which is available to authorized users.

Simple SummaryAnimal welfare today is assessed based on both the physical and mental health of animals. However, measuring animal mental health, which includes emotions (i.e., short-term positive or negative reactions to specific events), remains a challenge. Since animals are known to use vocalizations to communicate their emotions to their peers, knowledge about how the structure of vocalizations changes with emotions could be very useful in order to develop noninvasive indicators for assessing animal welfare under captive conditions. The aim of this study was thus to investigate if the type of calls (i.e., grunt, scream, or squeal) or the acoustic structure of the calls emitted by captive wild boars changed according to the emotions they were experiencing. We found that wild boars used different types of calls in positive and negative situations. We also found that their acoustic structure changed according to the emotions. Indeed, calls produced in positive situations were generally shorter and at lower frequencies than those produced in negative situations. It thus seems that wild boars express their emotional state through their vocalizations. Overall, our study gives us better knowledge about how the emotions of captive wild boars could be assessed, and how this compares to domestic pigs.AbstractMeasuring emotions in nonhuman mammals is challenging. As animals are not able to verbally report how they feel, we need to find reliable indicators to assess their emotional state. Emotions can be described using two key dimensions: valence (negative or positive) and arousal (bodily activation or excitation). In this study, we investigated vocal expression of emotional valence in wild boars (Sus scrofa). The animals were observed in three naturally occurring situations: anticipation of a food reward (positive), affiliative interactions (positive), and agonistic interactions (negative). Body movement was used as an indicator of emotional arousal to control for the effect of this dimension. We found that screams and squeals were mostly produced during negative situations, and grunts during positive situations. Additionally, the energy quartiles, duration, formants, and harmonicity indicated valence across call types and situations. The mean of the first and second formants also indicated valence, but varied according to the call type. Our results suggest that wild boars can vocally express their emotional states. Some of these indicators could allow us to identify the emotional valence that wild boars are experiencing during vocal production and thus inform us about their welfare.

• The function of stereotypic behavior (crib-biting) is not clear.• We used an ACTH challenge test to test the coping hypothesis of stereotypies.• We compared adrenal and sympathetic responses of stereotypic and control horses.• We found higher cortisol responses in the stereotypic group compared to controls.• Our results suggest that crib-biting is a coping strategy serving to reduce stress. a b s t r a c t a r t i c l e i n f o Stereotypies are repetitive and relatively invariant patterns of behavior, which are observed in a wide range of species in captivity. Stereotypic behavior occurs when environmental demands produce a physiological response that, if sustained for an extended period, exceeds the natural physiological regulatory capacity of the organism, particularly in situations that include unpredictability and uncontrollability. One hypothesis is that stereotypic behavior functions to cope with stressful environments, but the existing evidence is contradictory. To address the coping hypothesis of stereotypies, we triggered physiological reactions in 22 horses affected by stereotypic behavior (crib-biters) and 21 non-crib-biters (controls), using an ACTH challenge test. Following administration of an ACTH injection, we measured saliva cortisol every 30 min and heart rate (HR) continuously for a period of 3 h. We did not find any differences in HR or HR variability between the two groups, but crib-biters (Group CB) had significantly higher cortisol responses than controls (Group C; mean ± SD: CB, 5.84 ± 2.62 ng/ml, C, 4.76 ± 3.04 ng/ml). Moreover, crib-biters that did not perform the stereotypic behavior during the 3-hour test period (Group B) had significantly higher cortisol levels than controls, which was not the case of crib-biters showing stereotypic behavior (Group A) (B, 6.44 ± 2.38 ng/ml A, 5.58 ± 2.69 ng/ml). Our results suggest that crib-biting is a coping strategy that helps stereotypic individuals to reduce cortisol levels caused by stressful situations. We conclude that preventing stereotypic horses from crib-biting could be an inappropriate strategy to control this abnormal behavior, as it prevents individuals from coping with situations that they perceive as stressful.

Vocalizations constitute an effective way to communicate both emotional arousal (bodily activation) and valence (negative/positive). There is strong evidence suggesting that the convergence of vocal expression of emotional arousal among animal species occurs, hence enabling cross-species perception of arousal, but it is not clear if the same is true for emotional valence. Here, we conducted a large online survey to test the ability of humans to perceive emotions in the contact calls of several wild and domestic ungulates produced in situations of known emotional arousal (previously validated using either heart rate or locomotion) and valence (validated based on the context of production and behavioural indicators of emotions). Participants (1024 respondents from 48 countries) were able to rate above chance levels the arousal level of vocalizations of three of the six ungulate species and the valence of four of them. Percentages of correct ratings did not differ a lot across species for arousal (49–59%), while they showed much more variation for valence (33–68%). Interestingly, several factors such as age, empathy, familiarity and specific features of the calls enhanced these scores. These findings suggest the existence of a shared emotional system across mammalian species, which is much more pronounced for arousal than valence.

Background Discrimination and perception of emotion expression regulate interactions between conspecifics and can lead to emotional contagion (state matching between producer and receiver) or to more complex forms of empathy (e.g., sympathetic concern). Empathy processes are enhanced by familiarity and physical similarity between partners. Since heterospecifics can also be familiar with each other to some extent, discrimination/perception of emotions and, as a result, emotional contagion could also occur between species. Results Here, we investigated if four species belonging to two ungulate Families, Equidae (domestic and Przewalski’s horses) and Suidae (pigs and wild boars), can discriminate between vocalizations of opposite emotional valence (positive or negative), produced not only by conspecifics, but also closely related heterospecifics and humans. To this aim, we played back to individuals of these four species, which were all habituated to humans, vocalizations from a unique set of recordings for which the valence associated with vocal production was known. We found that domestic and Przewalski’s horses, as well as pigs, but not wild boars, reacted more strongly when the first vocalization played was negative compared to positive, regardless of the species broadcasted. Conclusions Domestic horses, Przewalski’s horses and pigs thus seem to discriminate between positive and negative vocalizations produced not only by conspecifics, but also by heterospecifics, including humans. In addition, we found an absence of difference between the strength of reaction of the four species to the calls of conspecifics and closely related heterospecifics, which could be related to similarities in the general structure of their vocalization. Overall, our results suggest that phylogeny and domestication have played a role in cross-species discrimination/perception of emotions.

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