Elodie F. Briefer

Emotions in Goats: Mapping Physiological, Behavioural and Vocal Profiles

Emotions are important because they enable the selection of appropriate behavioural decisions in response to external or internal events. Techniques for understanding and assessing animal emotions, and particularly positive ones, are lacking. Emotions can be characterized by two dimensions: their arousal (bodily excitation) and their valence (negative or positive). Both dimensions can affect emotions in different ways. It is thus crucial to assess their effects on biological parameters simultaneously, so that accurate indicators of arousal and valence can be identified. To find convenient and noninvasive tools to assess emotions in goats, Capra hircus, we measured physiological, behavioural and vocal responses of goats in four situations: (1) control (no external stimulus, neutral); (2) anticipation of a food reward (positive); (3) food-related frustration (negative); (4) isolation away from conspecifics (negative). These situations were characterized by different levels of arousal, assessed a posteriori by heart rates measured during the tests. We found several clear, reliable indicators of arousal and valence. During situations of higher arousal, goats had lower heart rate variability and higher respiration rates. They displayed more head movements, moved more, had their ears pointed forwards more often and on the side (horizontal) less often and produced more calls. They also produced calls with higher fundamental frequencies and higher energy distribution. In positive situations, goats had their ears oriented backwards less often and spent more time with their tails up than in negative situations. Furthermore, they produced calls in which the fundamental frequencies were less variable. Our methods for assessing the effects of emotional arousal and valence on biological parameters could lead to more effective monitoring and understanding of animal emotions, as well as to a better understanding of the evolution of emotions through cross-species comparisons.

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

BackgroundMale 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.ResultsWe 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.ConclusionsThe 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.

Mutual mother-offspring vocal recognition in an ungulate hider species (Capra hircus).

Parent–offspring recognition can be essential for offspring survival and important to avoid misdirected parental care when progeny mingle in large social groups. In ungulates, offspring antipredator strategies (hiding vs. following) result in differences in mother–offspring interactions, and thus different selection pressures acting on the recognition process during the first weeks of life. Hider offspring are isolated and relatively stationary and silent to avoid detection by predators, whereas follower offspring are mobile and rapidly mix in large social groups. For these reasons, hiders have been suggested to show low offspring call individuality leading to unidirectional recognition of mothers by offspring and followers high offspring call individuality and mutual recognition. We hypothesised that similar differences would exist in hider species between the hiding phase (i.e. unidirectional recognition) and the phase when offspring join social groups (i.e. mutual recognition). We tested these predictions with goats (Capra hircus), a hider species characterised by strong mother–offspring attachment. We compared the individuality of kid and mother calls, and the vocal recognition ability, during the early phase of life when kids are usually hidden and later when kids have typically joined social groups. Contrary to our predictions, we found that both kids and mothers had individualised contact calls and that mutual recognition existed even during the hiding phase. The large differences in the duration of the hiding phase and in the rate of mother–offspring interactions (possibly partially driven by domestication in some species) probably cause variations among hider species in the mother–offspring recognition process.

Mother goats do not forget their kids’ calls

Parent–offspring recognition is crucial for offspring survival. At long distances, this recognition is mainly based on vocalizations. Because of maturation-related changes to the structure of vocalizations, parents have to learn successive call versions produced by their offspring throughout ontogeny in order to maintain recognition. However, because of the difficulties involved in following the same individuals over years, it is not clear how long this vocal memory persists. Here, we investigated long-term vocal recognition in goats. We tested responses of mothers to their kids’ calls 7–13 months after weaning. We then compared mothers’ responses to calls of their previous kids with their responses to the same calls at five weeks postpartum. Subjects tended to respond more to their own kids at five weeks postpartum than 11–17 months later, but displayed stronger responses to their previous kids than to familiar kids from other females. Acoustic analyses showed that it is unlikely that mothers were responding to their previous kids simply because they confounded them with the new kids they were currently nursing. Therefore, our results provide evidence for strong, long-term vocal memory capacity in goats. The persistence of offspring vocal recognition beyond weaning could have important roles in kin social relationships and inbreeding avoidance.

Segregation of information about emotional arousal and valence in horse whinnies

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.

Goats favour personal over social information in an experimental foraging task.

Animals can use their environments more efficiently by selecting particular sources of information (personal or social), according to specific situations. Group-living animals may benefit from gaining information based on the behaviour of other individuals. Indeed, social information is assumed to be faster and less costly to use than personal information, thus increasing foraging efficiency. However, when food sources change seasonally or are randomly distributed, individual information may become more reliable than social information. The aim of this study was to test the use of conflicting personal versus social information in goats (Capra hircus), in a foraging task. We found that goats relied more on personal than social information, when both types of information were available and in conflict. No effect of social rank was found on the occasions when goats followed other demonstrator goats. Goats are selective browsers/grazers and therefore relying on personal rather than social information could be the most efficient way to find patchily distributed resources in highly variable environments. Studies testing specific assumptions regarding the use of different sources of information can extend our understanding of decision making, including observed patterns of social learning.

Assortative mating in fallow deer reduces the strength of sexual selection.

Background Assortative mating can help explain how genetic variation for male quality is maintained even in highly polygynous species. Here, we present a longitudinal study examining how female and male ages, as well as male social dominance, affect assortative mating in fallow deer (Dama dama) over 10 years. Assortative mating could help explain the substantial proportion of females that do not mate with prime-aged, high ranking males, despite very high mating skew. We investigated the temporal pattern of female and male matings, and the relationship between female age and the age and dominance of their mates. Results The peak of yearling female matings was four days later than the peak for older females. Younger females, and especially yearlings, mated with younger and lower-ranking males than older females. Similarly, young males and lower-ranking males mated with younger females than older males and higher-ranking males. Furthermore, the timing of matings by young males coincided with the peak of yearling female matings, whereas the timing of older male matings (irrespective of rank) coincided with the peak of older female matings. Conclusions Assortative mating, through a combination of indirect and/or direct female mate choice, can help explain the persistence of genetic variation for male traits associated with reproductive success.

Response to displaced neighbours in a territorial songbird with a large repertoire

Neighbour recognition allows territory owners to modulate their territorial response according to the threat posed by each neighbour and thus to reduce the costs associated with territorial defence. Individual acoustic recognition of neighbours has been shown in numerous bird species, but few of them had a large repertoire. Here, we tested individual vocal recognition in a songbird with a large repertoire, the skylark Alauda arvensis. We first examined the physical basis for recognition in the song, and we then experimentally tested recognition by playing back songs of adjacent neighbours and strangers. Males showed a lower territorial response to adjacent neighbours than to strangers when we broadcast songs from the shared boundary. However, when we broadcast songs from the opposite boundary, males showed a similar response to neighbours and strangers, indicating a spatial categorisation of adjacent neighbours’ songs. Acoustic analyses revealed that males could potentially use the syntactical arrangement of syllables in sequences to identify the songs of their neighbours. Neighbour interactions in skylarks are thus subtle relationships that can be modulated according to the spatial position of each neighbour.

Does true syntax or simple auditory object support the role of skylark song dialect

Parallels between birdsong and human language are numerous and include particular temporal arrangements of acoustic units and the existence of dialects. In animal communication, modifications of the temporal ordering of existing acoustic units have rarely been clearly linked with changes in information content, particularly in a natural environment. Here, we show that the organization of birdsong units (‘syllables’) in sequences supports interindividual relationships within skylark communities. We manipulated the temporal arrangement of song dialect variants (‘shared phrases’) in the skylark, Alauda arvensis, a songbird with a very large repertoire of syllables and complex song. When tested with playback experiments performed in the field, skylarks were able to perceive subtle differences in the ordering of syllables. Modifications of the syllable ordering within shared phrases changed the information content from ‘group member’ to ‘unfamiliar individual’ and induced more aggressive reactions than shared phrases with a preserved syllable arrangement. Shared phrases often varied between individuals in the number of successive repetitions of similar syllable types, but were very consistent in terms of syllable type ordering. Our results indicate that skylarks rely not simply on the composition in syllable types of shared phrases to recognize group members, but on syllable type ordering. Shared phrases could be perceived by birds as ‘auditory objects’ embedded within songs. Alternatively, birds might identify incorrect phrases using grammatical rules governing the succession of syllables composing the phrases shared by their group. The presence of between-individual variation in phrase length, associated with consistent syllable type ordering revealed by our analysis, suggests that the latter hypothesis is more likely. Our results show that birds perceive disruptions in the natural temporal pattern of song units, and that this temporal pattern is behaviourally salient and carries information.

The physiological consequences of crib-biting in horses in response to an ACTH challenge test.

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 3h. 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.