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.

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.

Stereotypic horses (Equus caballus) are not cognitively impaired.

Stereotypies in animals are thought to arise from an interaction between genetic predisposition and sub-optimal housing conditions. In domestic horses, a well-studied stereotypy is crib-biting, an abnormal behaviour that appears to help individuals to cope with stressful situations. One prominent hypothesis states that animals affected by stereotypies are cognitively less flexible compared to healthy controls, due to sensitization of a specific brain area, the basal ganglia. The aim of this study was to test this hypothesis in crib-biting and healthy controls, using a cognitive task, reversal learning, which has been used as a diagnostic for basal ganglia dysfunction. The procedure consisted of exposing subjects to four learning tasks; first and second acquisition, and their reversals. For each task, we measured the number of trials to reach criterion and heart rate and heart-rate variability. Importantly, we did not try to prevent crib-biters from executing their stereotypic behaviour. We found that the first reversal learning task required the largest number of trials, confirming its challenging nature. Interestingly, the second reversal learning task required significantly fewer trials to reach criterion, suggesting generalisation learning. However, we did not find any performance differences across groups; both stereotypic and control animals required a similar numbers of trials and did not differ in their physiological responses. Our results thus challenge the widely held belief that crib-biting horses, and stereotypic animals more generally, are cognitively impaired. We conclude that cognitive underperformance may occur in stereotypic horses if they are prevented from crib-biting to cope with experienced stress.

Expression of emotional valence in pig closed-mouth grunts: Involvement of both source- and filter-related parameters.

Emotion expression plays a crucial role for regulating social interactions. One efficient channel for emotion communication is the vocal-auditory channel, which enables a fast transmission of information. Filter-related parameters (formants) have been suggested as a key to the vocal differentiation of emotional valence (positive versus negative) across species, but variation in relation to emotions has rarely been investigated. Here, whether pig (Sus scrofa domesticus) closed-mouth grunts differ in source- and filter-related features when produced in situations assumed to be positive and negative is investigated. Behavioral and physiological parameters were used to validate the animals' emotional state (both in terms of valence and arousal, i.e., bodily activation). Results revealed that grunts produced in a positive situation were characterized by higher formants, a narrower range of the third formant, a shorter duration, a lower fundamental frequency, and a lower harmonicity compared to negative grunts. Particularly, formant-related parameters and duration made up most of the difference between positive and negative grunts. Therefore, these parameters have the potential to encode dynamic information and to vary as a function of the emotional valence of the emitter in pigs, and possibly in other mammals as well.

Vocal contagion of emotions in non-human animals.

Communicating emotions to conspecifics (emotion expression) allows the regulation of social interactions (e.g. approach and avoidance). Moreover, when emotions are transmitted from one individual to the next, leading to state matching (emotional contagion), information transfer and coordination between group members are facilitated. Despite the high potential for vocalizations to influence the affective state of surrounding individuals, vocal contagion of emotions has been largely unexplored in non-human animals. In this paper, I review the evidence for discrimination of vocal expression of emotions, which is a necessary step for emotional contagion to occur. I then describe possible proximate mechanisms underlying vocal contagion of emotions, propose criteria to assess this phenomenon and review the existing evidence. The literature so far shows that non-human animals are able to discriminate and be affected by conspecific and also potentially heterospecific (e.g. human) vocal expression of emotions. Since humans heavily rely on vocalizations to communicate (speech), I suggest that studying vocal contagion of emotions in non-human animals can lead to a better understanding of the evolution of emotional contagion and empathy.

Perception of emotional valence in horse whinnies.

BACKGROUND: Non-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. RESULTS: We 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. CONCLUSIONS: Horses 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.

Intrasexual selection drives sensitivity to pitch, formants and duration in the competitive calls of fallow bucks.

BACKGROUND: Mammal vocal parameters such as fundamental frequency (or pitch; f o ) and formant dispersion often provide information about quality traits of the producer (e.g. dominance and body size), suggesting that they are sexually selected. However, little experimental evidence exists demonstrating the importance of these cues in intrasexual competition, particularly f o . Male Fallow deer (bucks) produce an extremely low pitched groan. Bucks have a descended larynx and generate f o well below what is expected for animals of their size. Groan parameters are linked to caller dominance, body size and condition, suggesting that groans are the product of sexual selection. Using a playback experiment, we presented bucks with groans that had been manipulated to alter vocal cues to these male characteristics and compared the response to the same, non-modified (natural) groans. RESULTS: We experimentally examined the ability of bucks to utilise putative cues to dominance (f o ), body size (formant frequencies) and condition (groan duration), when assessing competitors. We found that bucks treated groans with lowered f o (more dominant), and lowered formant frequencies (larger caller) as more threatening. By contrast, groans with raised formant frequencies (smaller caller), and shorter durations (more fatigued caller) were treated as less threatening. CONCLUSIONS: Our results indicate that intrasexual selection is driving groans to concurrently convey caller dominance, body size and condition. They represent the first experimental demonstration of the importance of f o in male competition in non-human mammals, and show that bucks have advanced perception abilities that allow them to extract information based on relatively small changes in key parameters.

Goats excel at learning and remembering a highly novel cognitive task.

INTRODUCTION: The computational demands of sociality (maintaining group cohesion, reducing conflict) and ecological problems (extractive foraging, memorizing resource locations) are the main drivers proposed to explain the evolution cognition. Different predictions follow, about whether animals would preferentially learn new tasks socially or not, but the prevalent view today is that intelligent species should excel at social learning. However, the predictions were originally used to explain primate cognition, and studies of species with relatively smaller brains are rare. By contrast, domestication has often led to a decrease in brain size, which could affect cognition. In domestic animals, the relaxed selection pressures compared to a wild environment could have led to reduced social and physical cognition. Goats possess several features commonly associated with advanced cognition, such as successful colonization of new environments and complex fission-fusion societies. Here, we assessed goat social and physical cognition as well as long-term memory of a complex two-step foraging task (food box cognitive challenge), in order to investigate some of the main selection pressures thought to affect the evolution of ungulate cognition. RESULTS: The majority of trained goats (9/12) successfully learned the task quickly; on average, within 12 trials. After intervals of up to 10 months, they solved the task within two minutes, indicating excellent long-term memory. The goats did not learn the task faster after observing a demonstrator than if they did not have that opportunity. This indicates that they learned through individual rather than social learning. CONCLUSIONS: The individual learning abilities and long-term memory of goats highlighted in our study suggest that domestication has not affected goat physical cognition. However, these cognitive abilities contrast with the apparent lack of social learning, suggesting that relatively intelligent species do not always preferentially learn socially. We propose that goat cognition, and maybe more generally ungulate cognition, is mainly driven by the need to forage efficiently in harsh environments and feed on plants that are difficult to access and to process, more than by the computational demands of sociality. Our results could also explain why goats are so successful at colonizing new environments.

Exploring the role of vocalizations in regulating group dynamics.

Because of the diverging needs of individuals, group life can lead to disputes and competition, but it also has many advantages, such as reduced predation risk, information sharing and increased hunting success. Social animals have to maintain group cohesion and need to synchronize activities, such as foraging, resting, social interactions and movements, in order to thrive in groups. Acoustic signals are highly relevant for social dynamics, some because they are long-ranging and others because they are short-ranging, which may serve important within-group functions. However, although there has been an increase in studies concentrating on acoustic communication within groups in the past decade, many aspects of how vocalizations relate to group dynamics are still poorly understood. The aim of this review is to present an overview of our current knowledge on the role of vocalizations in regulating social group dynamics, identify knowledge gaps and recommend potential future research directions. We review the role that vocalizations play in (i) collective movement, (ii) separation risk and cohesion maintenance, (iii) fission-fusion dynamics, and (iv) social networks. We recommend that future studies aim to increase the diversity of studied species and strengthen the integration of state-of-the-art tools to study social dynamics and acoustic signals. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Calls of the little auk (Alle alle) chicks reflect their behavioural contexts.

Animal vocalisations can often inform conspecifics about the behavioural context of production and the underlying affective states, hence revealing whether a situation should be approached or avoided. While this is particularly important for socially complex species, little is known about affective expression in wild colonial animals, and even less to about their young. We studied vocalisations of the little auk (Alle alle) chicks in the Hornsund breeding colony, Svalbard. Little auks are highly colonial seabirds, and adults convey complex behavioural contexts through their calls. We recorded chick calls during two contexts of opposite affective valence: handing by a human, and while they interact with their parents inside the nest. Using permuted discriminant function analysis and a series of linear mixed models, we examined the effect of the production context/associated affective valence on the acoustic parameters of those calls. Calls were reliably classified to their context, with over 97% accuracy. Calls uttered during handling had higher mean entropy, fundamental frequency, as well as lower spectral centre of gravity and a less steep spectral slope compared to calls produced during interactions with a parent inside the nest. The individuality of handling calls, assessed by information content, was lower than the individuality of calls uttered in the nest. These findings suggest that seabird chicks can effectively communicate behavioural/affective contexts through calls, conveying socially important messages early in development. Our results are mostly in line with emotional expression patterns observed across taxa, supporting their evolutionary continuity.

The power of sound: unravelling how acoustic communication shapes group dynamics.

Acoustic signalling is a key mode of communication owing to its instantaneousness and rapid turnover, its saliency and flexibility and its ability to function strategically in both short- and long-range contexts. Acoustic communication is closely intertwined with both collective behaviour and social network structure, as it can facilitate the coordination of collective decisions and behaviour, and play an important role in establishing, maintaining and modifying social relationships. These research topics have each been studied separately and represent three well-established research areas. Yet, despite the close connection of acoustic communication with collective behaviour and social networks in natural systems, only few studies have focused on their interaction. The aim of this theme issue is therefore to build a foundation for understanding how acoustic communication is linked to collective behaviour, on the one hand, and social network structure on the other, in non-human animals. Through the building of such a foundation, our hope is that new questions in new avenues of research will arise. Understanding the links between acoustic communication and social behaviour seems crucial for gaining a comprehensive understanding of sociality and social evolution. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

A model for the noninvasive, habitat-inclusive estimation of upper limit abundance for synanthropes, exemplified by M. fascicularis.

Accurately estimating population sizes for free-ranging animals through noninvasive methods, such as camera trap images, remains particularly limited by small datasets. To overcome this, we developed a flexible model for estimating upper limit populations and exemplified it by studying a group-living synanthrope, the long-tailed macaque (Macaca fascicularis). Habitat preference maps, based on environmental and GPS data, were generated with a maximum entropy model and combined with data obtained from camera traps, line transect distance sampling, and direct sightings to produce an expected number of individuals. The mapping between habitat preference and number of individuals was optimized through a tunable parameter ρ (inquisitiveness) that accounts for repeated observations of individuals. Benchmarking against published data highlights the high accuracy of the model. Overall, this approach combines citizen science with scientific observations and reveals the long-tailed macaque populations to be (up to 80%) smaller than expected. The model's flexibility makes it suitable for many species, providing a scalable, noninvasive tool for wildlife conservation.

Seabird's cry: repertoire and vocal expression of contextual valence in the little auk (Alle alle).

Many seabird species breed in colonies counting up to hundreds of thousands of individuals. Life in such crowded colonies might require special coding-decoding systems to reliably convey information through acoustic cues. This can include, for example, developing complex vocal repertoires and adjusting the properties of their vocal signals to communicate behavioural contexts, and thus regulate social interactions with their conspecifics. We studied vocalisations produced by the little auk (Alle alle)-a highly vocal, colonial seabird-over mating and incubation periods on the SW coast of Svalbard. Using passive acoustic recordings registered in a breeding colony, we extracted eight vocalisation types: single call, clucking, classic call, low trill, short call, short-trill, terror, and handling vocalisation. Calls were grouped by production context (based on the typically associated behaviour), to which a valence (positive vs negative) was later attributed, when possible, according to fitness threats, i.e. predator or human presence (negative) and promoters, i.e. interaction with a partner (positive). The effect of the putative valence on eight selected frequency and duration variables was then investigated. The putative contextual valence significantly affected the acoustic properties of the calls. Calls assigned positive valence had higher fundamental frequency and spectral centre of gravity as well as shorter sound duration than these assigned negative valence. These results indicate that the little auk's vocal communication system may facilitate expression of complex behavioural contexts, and seems to include vocal plasticity within vocalisation types-however, more data are necessary to better understand this effect and possible interplays of other factors.

Social calls of the little auk (Alle alle) reflect body size and possibly partnership, but not sex.

Source-filter theory posits that an individual's size and vocal tract length are reflected in the parameters of their calls. In species that mate assortatively, this could result in vocal similarity. In the context of mate selection, this would mean that animals could listen in to find a partner that sounds-and therefore is-similar to them. We investigated the social calls of the little auk (Alle alle), a highly vocal seabird mating assortatively, using vocalizations produced inside 15 nests by known individuals. Source- and filter-related acoustic parameters were used in linear mixed models testing the possible impact of body size. A principal component analysis followed by a permuted discriminant function analysis tested the effect of sex. Additionally, randomization procedures tested whether partners are more vocally similar than random birds. There was a significant effect of size on the mean fundamental frequency of a simple call, but not on parameters of a multisyllable call with apparent formants. Neither sex nor partnership influenced the calls-there was, however, a tendency to match certain parameters between partners. This indicates that vocal cues are at best weak indicators of size, and other factors likely play a role in mate selection.

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.

Age, empathy, familiarity, domestication and call features enhance human perception of animal emotion expressions.

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.

Classification of pig calls produced from birth to slaughter according to their emotional valence and context of production.

Vocal expression of emotions has been observed across species and could provide a non-invasive and reliable means to assess animal emotions. We investigated if pig vocal indicators of emotions revealed in previous studies are valid across call types and contexts, and could potentially be used to develop an automated emotion monitoring tool. We performed an analysis of an extensive and unique dataset of low (LF) and high frequency (HF) calls emitted by pigs across numerous commercial contexts from birth to slaughter (7414 calls from 411 pigs). Our results revealed that the valence attributed to the contexts of production (positive versus negative) affected all investigated parameters in both LF and HF. Similarly, the context category affected all parameters. We then tested two different automated methods for call classification; a neural network revealed much higher classification accuracy compared to a permuted discriminant function analysis (pDFA), both for the valence (neural network: 91.5%; pDFA analysis weighted average across LF and HF (cross-classified): 61.7% with a chance level at 50.5%) and context (neural network: 81.5%; pDFA analysis weighted average across LF and HF (cross-classified): 19.4% with a chance level at 14.3%). These results suggest that an automated recognition system can be developed to monitor pig welfare on-farm.

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.

Perceptual lateralization of vocal stimuli in goats.

Functional asymmetries, for example, the preferential involvement of 1 brain hemisphere to process stimuli, may increase brain efficiency and the capacity to carry out tasks simultaneously. We investigated which hemisphere was primarily involved in processing acoustic stimuli in goats using a head-orienting paradigm. Three playbacks using goat vocalizations recorded in different contexts: food anticipation (positive), isolation (negative), food frustration (negative), as well as 1 playback involving dog barks (negative) were presented on the left and right sides of the test subjects simultaneously. The head-orienting response (left or right) and latency to resume feeding were recorded. The direction of the head-orienting response did not differ between the various playbacks. However, when the head-orienting response was tested against chance level, goats showed a right bias regardless of the stimuli presented. Goats responded more to dog barks than to food frustration calls, whereas responses to food anticipation and isolation calls were intermediate. In addition, the latency to resume feeding, an indicator of fear reaction, was not affected by the kind of vocalization presented. These results provide evidence for asymmetries in goat vocal perception of emotional-linked conspecific and heterospecific calls. They also suggest involvement of the left brain hemisphere for processing acoustic stimuli, which might have been perceived as familiar and non-threatening.

Elevated Sensitivity to Tactile Stimuli in Stereotypic Horses.

Although stereotypic behaviors are a common problem in captive animals, why certain individuals are more prone to develop them remains elusive. In horses, individuals show considerable differences in how they perceive and react to external events, suggesting that this may partially account for the emergence of stereotypies in this species. In this study, we focused on crib-biting, the most common stereotypy displayed by horses. We compared how established crib-biters ("CB" = 19) and normal controls ("C" = 18) differed in response to a standard "personality" assessment test battery, i.e., reactivity to humans, tactile sensitivity, social reactivity, locomotor activity, and curiosity vs. fearfulness (both in novel and suddenness situations). Our analyses showed that crib-biters only differed from control horses in their tactile sensitivity, suggesting an elevated sensitivity to tactile stimuli. We suggest that this higher tactile sensitivity could be due to altered dopamine or endogenous opioid physiology, resulting from chronic stress exposition. We discuss these findings in relation to the hypothesis that there may be a genetic predisposition for stereotypic behavior in horses, and in relation to current animal husbandry and management practices.