Vocal Expression of Emotions in Mammals: Mechanisms of Production and Evidence

Emotions play a crucial role in an animal’s life because they facilitate responses to external or internal events of significance for the organism. In social species, one of the main functions of emotional expression is to regulate social interactions. There has recently been a surge of interest in animal emotions in several disciplines, ranging from neuroscience to evolutionary zoology. Because measurements of subjective emotional experiences are not possible in animals, researchers use neurophysiological, behavioural and cognitive indicators. However, good indicators, particularly of positive emotions, are still lacking. Vocalizations are linked to the inner state of the caller. The emotional state of the caller causes changes in the muscular tension and action of its vocal apparatus, which in turn, impacts on vocal parameters of vocalizations. By considering the mode of production of vocalizations, we can understand and predict how vocal parameters should change according to the arousal (intensity) or valence (positive/negative) of emotional states. In this paper, I review the existing literature on vocal correlates of emotions in mammals. Non-human mammals could serve as ideal models to study vocal expression of emotions, because, contrary to human speech, animal vocalizations are assumed to be largely free of control and therefore direct expressions of underlying emotions. Furthermore, a comparative approach between humans and other animals would give us a better understanding of how emotion expression evolved. Additionally, these non-invasive indicators could serve various disciplines that require animal emotions to be clearly identified, including psychopharmacology and animal welfare science

Microdialect and Group Signature in the Song of the Skylark Alauda arvensis

The Skylark Alauda arvensis is a territorial species of open landscape in which pairs settle in stable and adjacent territories during the breeding season. Due to the heterogeneity of the habitat, territories are gathered in patches spaced by a few kilometres, in which each male produces very long and complex flight songs as a part of the territorial behaviour. We showed that, in a given patch, all the males (neighbours) share some particular sequences of syllables in their songs, whereas males settled in different patches (strangers) have almost no sequences in common. Such a phenomenon is known as microdialect. To test the hypothesis that these shared sequences support a group signature, we made playback experiments with ‘‘chimeric’’ signals: songs of strangers where the sequences shared by neighbours were artificially inserted. Behavioural responses to playbacks indicated a neighbour-stranger discrimination consistent with the dear enemy phenomenon, i.e. a reduced aggression toward neighbours compared to strangers. Furthermore, the same level of responses, observed when a ‘‘chimeric’’ song and a neighbour song were broadcast, indicated that shared sequences are recognized and identified as markers of the neighbourhood identity

Quality prevails over identity in the sexually selected vocalisations of an ageing mammal

BACKGROUND: Male sexually selected vocalisations generally contain both individuality and quality cues that are crucial in intra- as well as inter-sexual communication. As individuality is a fixed feature whereas male phenotypic quality changes with age, individuality and quality cues may be subjected to different selection pressures over time. Individuality (for example, morphology of the vocal apparatus) and quality (for example, body size and dominance status) can both affect the vocal production mechanism, inducing the same components of vocalisations to convey both kinds of information. In this case, do quality-related changes to the acoustic structure of calls induce a modification of vocal cues to identity from year to year? We investigated this question in fallow deer (Dama dama), in which some acoustic parameters of vocalisations (groans) code for both individuality and quality. RESULTS: We carried out a longitudinal analysis of groan individuality, examining the effects of age and dominance rank on the acoustic structure of groans of the same males recorded during consecutive years. We found both age- and rank-related changes to groans; the minimum values of the highest formant frequencies and the fundamental frequency increased with the age of males and they decreased when males became more dominant. Both age- and rank-related acoustic parameters contributed to individuality. Male quality changed with age, inducing a change in quality-related parameters and thus, a modification of vocal cues to male individuality between years. CONCLUSIONS: The encoding of individuality and quality information in the same components of vocalisations induces a tradeoff between these two kinds of signals over time. Fallow deer vocalisations are honest signals of quality that are not fixed over time but are modified dynamically according to male quality. As they are more reliable cues to quality than to individuality, they may not be used by conspecifics to recognize a given male from one year to another, but potentially used by both sexes to assess male quality during each breeding season

Fallow deer polyandry is related to fertilization insurance

Polyandry is widespread, but its adaptive significance is not fully understood. The hypotheses used to explain its persistence have rarely been tested in the wild and particularly for large, long-lived mammals. We investigated polyandry in fallow deer, using female mating and reproduction data gathered over 10years. Females of this species produce a single offspring (monotocous) and can live to 23years old. Overall, polyandry was evident in 12% of females and the long-term, consistent proportion of polyandrous females observed, suggests that monandry and polyandry represent alternative mating strategies. Females were more likely to be polyandrous when their first mate had previously achieved high numbers of matings during the rut or was relatively old. However, polyandry was not related to the following factors: female age, the stage of the rut, the dominance ranks of mates, or the number of daily matings achieved by males. Polyandrous and monandrous multiple-mating females were not more likely than single-mating females to be observed with an offspring during the following year, and there were no significant differences in offspring size between these females. These results provide support for a fertility insurance hypothesis, with females remating if fertilization from the first mating was uncertain due to possible sperm depletion. The potential for different female mating strategies among large, polygynous mammals has generally been overlooked. Our findings highlight the complexity of female reproductive strategies and the possible trade-offs between fertilization success, preferences for high-quality males, and potential costs of polyandry, particularly for monotocous specie

Cross-species discrimination of vocal expression of emotional valence by Equidae and Suidae.

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

Novel ideas to further expand the applicability of rhythm analysis

The temporal structure of animals’ acoustic signals can inform about context, urgency, species, individual identity, or geographical origin. We present three independent ideas to further expand the applicability of rhythm analysis for isochronous, that is, metronome-like, rhythms. A description of a rhythm or beat needs to include a description of its goodness of fit, meaning how well the rhythm describes a sequence. Existing goodness-of-fit values are not comparable between methods and datasets. Furthermore, they are strongly correlated with certain parameters of the described sequence, for example, the number of elements in the sequence. We introduce a new universal goodness-of-fit value, ugof, comparable across methods and datasets, which illustrates how well a certain beat frequency in Hz describes the temporal structure of a sequence of elements. We then describe two additional approaches to adapt already existing methods to analyze the rhythm of acoustic sequences of animals. The new additions, a slightly modified way to use the already established Fourier analysis and concrete examples on how to use the visualization with recurrence plots, enable the analysis of more variable data, while giving more details than previously proposed measures. New methods are tested on 6 datasets including the very complex flight songs of male skylarks. The ugof is the first goodness-of-fit value capable of giving the information per element, instead of only per sequence. Advantages and possible interpretations of the new approaches are discussed. The new methods enable the analysis of more variable and complex communication signals. They give indications on which levels and structures to analyze and enable to track changes and differences in individuals or populations, for instance, during ontogeny or across regions. Especially, the ugof is not restricted to the analysis of acoustic signals but could for example also be applied on heartbeat measurements. Taken together, the ugof and proposed method additions greatly broaden the scope of rhythm analysis methods

Behaviour of Horses in a Judgment Bias Test Associated with Positive or Negative Reinforcement

Moods can influence our judgment of ambiguous stimuli as positive or negative. Measuring judgment bias in animals is a promising method to objectively assess their emotional states. Our study aimed to develop a cognitive bias test in horses, in order to assess the effect of training using positive reinforcement (PR) or negative reinforcement (NR) on their emotional states. We trained 12 mares to discriminate between a rewarded and a non-rewarded location situated on each side of a paddock. The mares were then trained during five days to perform several exercises using PR (n = 6) for one group, and NR (n = 6) for the other (treatment). Finally, we compared the responses of the two groups to three ambiguous locations situated between the rewarded and non-rewarded locations (judgment bias test). During the training exercises, according to our predictions, behavioural measures suggested that NR mares experienced more negative emotions than PR mares. Surprisingly, the results of the judgment bias test suggest that NR mares were in a more optimistic mood compared to PR mares, despite previously experiencing more negative emotions during the treatment. NR mares could have been more motivated to obtain a food reward than PR mares, which had been rewarded throughout the treatment phase. Alternatively, NR mares could have developed optimistic bias triggered by release from the negative state experienced during treatment. This first attempt to test judgment bias in horses suggests that this is a promising method to measure horse mood. Knowledge about the effect of training methods on the mental health of domesticated animals can add a new dimension to animal welfare, in order to promote better ways to work with animals

Goats distinguish between positive and negative emotion-linked vocalisations

Background Evidence from humans suggests that the expression of emotions can regulate social interactions and promote coordination within a group. Despite its evolutionary importance, social communication of emotions in non-human animals is still not well understood. Here, we combine behavioural and physiological measures, to determine if animals can distinguish between vocalisations linked to different emotional valences (positive and negative). Using a playback paradigm, goats were habituated to listen to a conspecific call associated with positive or negative valence (habituation phase) and were subsequently exposed to a variant of the same call type (contact call) associated with the opposite valence (dishabituation phase), followed by a final call randomly selected from the habituation phase as control (rehabituation phase). The effects of the calls on the occurrence of looking and cardiac responses in these phases were recorded and compared. Results We found that when the valence of the call variant changed, goats were more likely to look at the source of the sound, indicating that they could distinguish calls based on their valence. Heart rate was not affected by the valence of the calls played, whereas heart-rate variability tended to be higher in the habituation and rehabituation phases, when positive calls were played compared to negative ones. Together, the behavioural and physiological measures provide evidence suggesting, first, that goats are able to distinguish call variants based on their valence, and second, that goat behaviour and cardiac responses are affected by call valence. Conclusion This study indicates that auditory modalities are a potent means to communicate emotions in non-human animals. These findings can contribute to our understanding of the evolution of emotion perception in non-human animals.ISSN:1742-999