Emotional contagion in nonhuman animals: A review

ADVANCED REVIEW Emotional contagion in nonhuman animals: A review Ana Pérez-Manrique | Antoni Gomila Department of Psychology, Human Evolution and Cognition Group (EvoCog), UIB, IFISC, Associated Unit to CSIC, Palma, Spain Correspondence Ana Pérez-Manrique, Department of Psychology, Human Evolution and Cognition Group (EvoCog), UIB, IFISC, Associated Unit to CSIC, Palma, Spain. Email: [email protected] Funding information Spanish Ministry of Education, Culture and Sport, Grant/Award Number: AP2012-3501; Spanish Government, Grant/Award Number: FFI2017-86351-R; Ministerio de Ciencia, Innovaci ony Universidades (MCIU), the Agencia Estatal de Investigaci on (AEI) and the European Regional Development Funds (ERDF, EU), Grant/Award Number: FFI2017-86351-R Edited by Juan-Carlos G omez, Editor Abstract Emotional contagion, the emotional state-matching of an individual with another, seems to be crucial for many social species. In recent years evidence on emotional contagion in different animal species has accumulated. However, despite its adaptative advantages and its presumed simplicity, the study and direct demonstration of this phenomenon present more complexities than previously thought. For these reasons, a review of the literature on emotional contagion in nonhuman species is timely to integrate current findings. In this paper thus, we carry out a comprehensive review of the most relevant studies on emotional contagion in animals and discuss the main problems and challenges of the field. We conclude that more research is needed to broaden our understanding of the mechanisms and functions of emotional contagion and the extent to which this process is present in a wide variety of species. Furthermore, the comparative study of emotional contagion would benefit from the use of systematized paradigms including both behavioral and physiological measures and the simultaneous recording of the responses of the interacting individuals to reliably assess an emotional state-matching between them and reliable controls. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Psychology > Comparative Psychology Psychology > Emotion and Motivation KEYWORDS animal emotional empathy, comparative psychology, emotional contagion 1|INTRODUCTION Emotional contagion is broadly defined as the emotional state-matching of a subject with another (de Waal, 2008; Shamay-Tsoory, 2011). This automatic emotional response that matches the perceived emotion of another individual involves changes at the neurophysiological, cognitive, and behavioral dimensions. It has been considered as the most basic form of empathy (de Waal, 2007; Preston & de Waal, 2002), but it is not clear that all empathic behaviors involve a core process of emotional contagion (Isern-Mas & Gomila, 2019; Yamamoto, 2017). Emotional contagion has also been related to motor mimicry: motor mimicry has been considered as the underlying mechanism of emotional Received: 12 May 2020 Revised: 9 March 2021 Accepted: 25 March 2021 DOI: 10.1002/wcs.1560 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. © 2021 The Authors. WIREs Cognitive Science published by Wiley Periodicals LLC. WIREs Cogn Sci. 2022;13:e1560. wires.wiley.com/cogsci 1of26 https://doi.org/10.1002/wcs.1560 matching (Hatfield, Cacioppo, & Rapson, 1994; Preston & de Waal, 2002). When an observer mimics the display of another, induces in itself the perceived emotional state (Niedenthal, 2007; de Waal and Preston, 2017). The evidence of the relevance of motor mimicry in emotional contagion is extensive for facial displays (see e.g., Palagi et al., 2020; Campbell & de Waal, 2011; Davila-Ross et al., 2008; Norscia & Palagi, 2011; Palagi et al., 2009; Palagi et al., 2018; Palagi et al., 2019; de Waal and Preston, 2017). Motor mimicry, though, is interesting on its own, as it can occur without emotion contagion (for a review, see Chartrand & Lakin, 2013; Duffy & Chartrand, 2015). Overall, emotional contagion processes do not seem to be cognitively demanding and thus might be important evolutionary adaptations for a wide number of social species. Emotional contagion may provide important adaptive advantages to species that need to interact with others and engage in parental care. For these species, adopting the same emotional state of their group, mate or offspring could be vital in certain contexts. For example, the rapid spread of fear among group members could allow that most individuals in a group escape from potential danger. Emotional contagion is a way to acquire valuable information about environmental threats without directly experiencing them (Decety et al., 2012; Preston & de Waal, 2002). Furthermore, being able to emotionally resonate with others may be crucial for effective communication and social cohesion (de Vignemont & Singer, 2006; Decety et al., 2012). Besides, emotional contagion may help promote social bonds, restore relationships after agonistic interactions, reduce stress levels, enhance social acceptance, and mark others as similar to self (Decety et al., 2012; Uchino et al., 1996). As a consequence, emotional contagion may provide the primary motivation for prosocial responses (de Vignemont & Singer, 2006; Decety et al., 2012; Yamamoto, 2017). And, in species endowed with further cognitive abilities, emotional contagion may underlie more complex empathic behaviors such as helping (Pérez-Manrique & Gomila, 2018). Finally, in many cases, parental care relies on the ability to be affected by the emotional expressions of the offspring, allowing parents to respond with care to the needs of their young (Darwin, 1897; Preston & de Waal, 2002). This capacity could thus provide an important fitness advantage for the offspring (Decety et al., 2012). Despite the supposed importance of emotional contagion in numerous aspects of animals' social life and its presumed simplicity, the study and direct demonstration of this phenomenon present more complexities than would be expected, and neither its features are as well defined as assumed by most of the scientific community (Adriaense et al., 2020). Nevertheless, momentum in the study of emotional contagion in nonhuman animals has been gathering in the past decade. For these reasons, a review of the available evidence and pending challenges seems timely. We have decided to organize the studies on emotional contagion in groups of species, and order them according to the number of studies available. In so doing, we hope to provide a clear panoramic vision of the experimental paradigms, variables measured, and modulating factors, as a way to propose how to improve research in this field and get clearer results. After the revision of literature, we will discuss the methods, concepts and main problems of the field, and will propose solutions for future studies on emotional contagion in nonhuman animals. 2|STUDIES ON EMOTIONAL CONTAGION IN NONHUMAN ANIMALS 2.1 |Mammals 2.1.1 |Rodents Rodents have become consolidated as an ideal model for assessing emotional processes in animals and the neural substrates involved. In recent years, many studies have focused on emotional contagion of pain, distress and fear. These studies reveal that rodents are highly attuned to the affective state of their group partners (see reviews HernandezLallement et al., 2020; Keum & Shin, 2016; Kim et al., 2019; Meyza & Knapska, 2018; Meyza et al., 2017; Mogil, 2012; Panksepp & Lahvis, 2011). Studies on emotional contagion of negative emotions (fear, distress, and pain) Studies on emotional contagion of fear, distress and pain in rodents can be broadly divided into five categories, depending on the type of stimulus to which the observer animal is exposed (Meyza et al., 2017): A conspecific receiving aversive physical stimulation, a fear-conditioned conspecific reacting to the conditioned stimulus, a distressed conspecific due to a previously experienced event, a conspecific in various degrees of pain, and a conspecific subjected to a social stressor. 2of26 PÉREZ-MANRIQUE AND GOMILA 1. The first category includes experiments in which rodents observe a conspecific (demonstrator) experiencing aversive stimulation (e.g., foot-shocks), in occasions paired with a conditioned stimulus (e.g., a tone). This paradigm serves to assess the observer's responses to demonstrators' fear and pain reactions. As rodents usually express fear by freezing (defensive immobility) (Sivaselvachandran et al., 2016), this is the most used behavioral variable in experiments assessing emotional contagion of fear. In two seminal studies, a rat (Rattus norvegicus) had to press a lever to either obtain food while observing another rat receiving electrical shocks (Church, 1959) or to stop the shocks delivered to a conspecific (Rice, 1964). Both studies showed that the exposure to a conspecific's distress decreased the observers' rate of lever pressing, behavior that was interpreted as a signal of fear (Estes & Skinner, 1941). Interestingly, rats that during the training phase received a synchronous shock with a partner expressed a strong drop in lever pressing compared to the other groups (rats that received shocks in isolation, and the no-shock group). This behavior was observed even when rats were deprived of food (Church, 1959). However, in the experiment of Rice (1964), it was not clear whether this effect and the observers' fear-related responses were due to the features of the apparatus or triggered by the sight of the distressed conspecific. Some recent and more controlled studies have provided mixed results on the response of rodents to the exposure of conspecifics being subjected to physical stressors. Four studies showed that neither the visual (Sanders et al., 2013) nor auditory (Atsak et al., 2011; Chen et al., 2009; Ueno et al., 2020) exposure to familiar or unrelated conspecifics receiving foot-shocks or to videos of foot-shocked cagemates elicited freezing responses in observer rodents. However, another series of studies provided positive evidence of this phenomenon. Mice (Mus musculus), degus (Octodon degus) and rats displayed freezing behavior in response to the sight of a familiar or unrelated demonstrator receiving electrical shocks (e.g., Allsop et al., 2018; Atsak et al., 2011; Carrillo et al., 2015; Gonzalez-Liencres et al., 2014; Han et al., 2020; Jeon et al., 2010; Jeon & Shin, 2011; Keum et al., 2016; Keum et al., 2018; Lidhar et al., 2017; Pisansky, Hanson, et al., 2017; Pisansky, Young, et al., 2017; Sanders et al., 2013; Twining et al., 2017; Ueno et al., 2020; Yusufishaq & Rosenkranz, 2013). Besides, in rats, the demonstrators' behavior was modulated by the behavior of the observers: they froze more if witnesses froze more (Atsak et al., 2011; Han et al., 2020). Interestingly, genetic background modulated some of the mice's responses. For example, only mice from a gregarious genetic strain displayed a heart rate deceleration in response to the playback of vocalizations of conspecifics receiving shocks (Chen et al., 2009). That response has been related to empathic concern in humans (Zahn-Waxler et al., 1995). Also, this social breed and four more inbred mouse strains showed a significant increase in freezing behavior while observing a demonstrator being repeatedly shocked compared to five other strains (Keum et al., 2016). Overall, the results of some of these studies showed that exposure to a conspecific experiencing an aversive event influenced the behavior of observer rodents. More precisely, observers displayed similar behavioral responses to those of the demonstrators, being freezing the most prominent response. However, a recent study has questioned whether this freezing behavior is an indicator of emotional contagion or it is rather a tendency to imitate the movements of others (Ueno et al., 2020). Ueno and collaborators reported that observer mice ate the same amount of chocolate chips in the presence of a foot-shocked cagemate than in the presence of an undisturbed mouse, whereas demonstrators ate no chocolate while receiving the shocks. According to the authors, this outcome indicates that observers were more strongly motivated by food than by the emotional responses of their mate, suggesting that freezing behavior does not reflect empathy-like behavior. Furthermore, in support of this hypothesis, this study also showed that observers' freezing behavior did not correlate with the degree of pain experimented by demonstrators. 2. In the second group of studies on emotional contagion of fear, demonstrators are first fear-conditioned and then subjected to a fear-memory retrieval task in which only the conditioned stimulus is presented (e.g., a tone). During the fear-memory retrieval, the observers' reactions to a frightened demonstrator are registered. In these studies, the display of freezing behavior by the observer is also interpreted as evidence of the social transfer of fear among rodents. Overall, prairie voles (Microtus ochrogaster) and rats with previous experience with the aversive event but not with the conditioned stimulus, displayed significant freezing in response to the reactions of the frightened individual (e.g., Burkett et al., 2016; Kim et al., 2010; Pereira et al., 2012). Furthermore, some of the observer's responses occurred concurrently with those of the demonstrator (Burkett et al., 2016). A more controversial issue is which of the demonstrator's responses triggered the observed freezing behavior. It has been proposed that fear-induced 22-kHz ultrasonic vocalizations (USVs) may play a role in this “fear transmission” in rats (Kim et al., 2010). This hypothesis is supported by the fact that observers' freezing was blocked by specific lesions in the thalamus, which prevented auditory information flow to the forebrain (Kim et al., 2010). However, some studies (Jones & Monfils, 2016; Pereira et al., 2012) showed that most of the demonstrators did not emit PÉREZ-MANRIQUE AND GOMILA 3of26 distress calls at all during the fear-memory retrieval task, and yet observers displayed freezing behavior. This result casts doubt on the role of USVs in this process. An alternative explanation is that other auditory cues could be involved in this process. In fact, Pereira et al. (2012) reported that freezing of the demonstrator could be detected through the lack of movement-evoked sound. They showed that the sudden cessation of locomotion sounds triggered freezing only in experienced observers, even when the test was performed in the dark. Vicarious fear learning: Social interaction with a frightened, distressed or emotionally aroused conspecific has been found to result in long-lasting changes in behavior modulating learning and memory (Meyza et al., 2016). Vicarious fear learning and social acquisition of defensive, avoidance or conditioned fear responses have been interpreted as a proof of emotional contagion. In these studies, observer rodents are usually first exposed to a demonstrator reacting to a conditioned stimulus either during the conditioning procedure (e.g., paired with an unconditioned stimulus like shocks) or during a fear memory retrieval (without unconditioned stimulus). Then, observers are tested to examine their responses towards the conditioned stimulus. In this way, it is possible to assess whether observers learned from the demonstrator's emotional responses to fear certain cues. This social transfer of information and subsequent learning from emotional cues have been observed in rats, mice deer mice (Peromyscus maniculatus) and degus (e.g., Allsop et al., 2018; Bredy & Barad, 2009; Bruchey et al., 2010; Chen et al., 2009; Ito et al., 2015; Jeon et al., 2010; Jones et al., 2014; Jones & Monfils, 2016; Kavaliers et al., 2003; Kavaliers et al., 2005; Knapska et al., 2010; Lidhar et al., 2017; Nowak et al., 2013; Panksepp & Lahvis, 2016; Twining et al., 2017; Yusufishaq & Rosenkranz, 2013). However, the use of this type of measurements to assess emotional contagion is controversial. It has been claimed that these paradigms do not measure emotional contagion, instead, they use it as a tool to study the cognitive impacts of observing distress in others (Hernandez-Lallement et al., 2020). That is, as changes in memory and learning do not involve an emotional observable response, they are considered as secondary processes related to emotional contagion (Hernandez-Lallement et al., 2020). Furthermore, observational learning can occur in these tasks without implying the sharing of emotions (Keum et al., 2018). 3. In the third group of experiments, observer rodents were exposed to a distressed conspecific which had undergone an aversive event (e.g., fear conditioning episode). In this case, the demonstrator was still stressed due to the previous aversive and/or painful event. Thus, this protocol serves to evaluate the observer's responses to demonstrator's distress cues. These studies used different indicators to assess the occurrence of emotional contagion: behavioral reactions (e.g., percentage of freezing time), and physiological and neural responses. Again, the existing evidence is mixed: On the one hand, rats, mice and voles showed several signs of distress and fear when exposed to a distressed conspecific. Rats displayed an increased arousal/vigilance state (Knapska et al., 2006; Knapska et al., 2010), and fear responses (increased freezing and self-grooming) (Rogers-Carter et al., 2018). Besides, after the exposure, only female rats presented an amygdalar activation similar to that of demonstrators, being the amygdala a part of the limbic system involved in fear processing and emotional reactions (Knapska et al., 2006; Mikosz et al., 2015). Similarly, mice also spent significantly more time immobile when exposed to a fear-conditioned cage mate than when exposed to an unaltered partner (Ueno et al., 2020). And, only a gregarious strain of mice displayed increased activation in the prefrontal cortex and the amygdala (Meyza et al., 2015). In turn, prairie voles mimicked the anxiety and fear like behaviors (self-grooming and freezing) of a stressed familiar vole (Burkett et al., 2016). Furthermore, when voles could not interact physically with their distressed partner, they presented significantly elevated plasma corticosterone which correlated with that of the demonstrator. Therefore, the behavioral and physiological responses displayed by observers and demonstrators were alike, suggesting an emotional state-matching between them. On the other hand, rats' responses did not differ when interacting with distressed or control rats (Mikosz et al., 2015). And, when visual but not auditory or odor cues emitted by the distressed partner were blocked, no significant differences in observer mice' freezing were observed (Ueno et al., 2020). 4. The fourth category encompasses studies assessing social modulation of pain by registering changes in pain sensitivity or pain thresholds in individuals exposed to a conspecific in pain (see reviews Hernandez-Lallement et al., 2020; Martin et al., 2014; Mogil, 2015). To do so, a noxious stimulus is administered to observers and demonstrators and then, they are tested in dyads or isolation. In mice, modulation of pain sensitivity (hyperalgesia) was observed in familiar (cagemates) but not in stranger dyads or individuals tested alone (e.g., Langford et al., 2006; Laviola et al., 2017; Martin et al., 2015). Furthermore, observers presented altered pain sensitivity in a different modality and displayed pain behaviors (writhing) that were influenced and co-occurred with those of the cagemate. These pain behaviors were dependent on visual information (Langford et al., 2006). However, this protocol in which both, observer and demonstrator are in pain, does not allow to distinguish between the effects of vicariously felt pain and 4of26 PÉREZ-MANRIQUE AND GOMILA physical pain (Yu et al., 2019). A series of studies have tried to overcome this impediment by first exposing mice and rats to an individual in pain (cagemate or stranger), and then isolating them and examining their pain responses (Du et al., 2020; Li et al., 2014; Li, Yu, et al., 2018; Lü et al., 2017; Yu et al., 2019). Again, only observers which interacted with familiar individuals showed enhanced pain-related behaviors, increased mechanical but not thermal pain sensitivity, and enhanced nociceptive neuronal activity. Furthermore, these responses seemed to be mediated by the medial prefrontal cortex and the locus coeruleus (Li et al., 2014; Lü et al., 2017), brain structures related to empathy for pain in humans (Singer et al., 2004; Yu et al., 2019). 5. Finally, a series of studies used social defeat as a social stressor to assess the effects on the physiological, cognitive and behavioral responses of observer rats and mice (see Carnevali et al., 2020 for a review). After several days of viewing aggressive encounters between conspecifics, observers displayed different responses including increased anxiety and depression-like behaviors strikingly similar to that of defeated conspecifics. Both, witnesses and demonstrators, also displayed increased levels of serum corticosterone (a glucocorticoid involved in stress responses), deficits in body weight and increases in mean arterial pressure and heart rate (Carnevali et al., 2017; Finnell et al., 2017, 2018; Iñiguez et al., 2018; Miao et al., 2018; Patki et al., 2014; Patki et al., 2015; Sial et al., 2016; Warren et al., 2013, 2014)(Warren et al., 2013). Studies on emotional contagion of positive emotions There is an important lack of studies investigating emotional contagion of positive emotions in rodents (HernandezLallement et al., 2020). One of the few available studies is that of Saito et al. (2016). They tested whether rats display positive or negative emotional contagion after hearing conspecific USVs (50 kHz USVs emitted in positive contexts and 22 kHz USVs emitted in negative contexts) via a cognitive bias task. This task serves to measure affective states via operant conditioning. Rats were first conditioned to respond differently to two sounds, each of which signaling either a positive or a negative outcome. Then, they were exposed to an ambiguous cue (frequency falling between the two conditioned stimuli). After being exposed to positive vocalizations rats responded to ambiguous cues as positive (optimistic bias), and negative after being exposed to negative vocalizations (pessimistic bias). Suggesting that rats were indeed influenced by the emotional cues of conspecifics. Another experiment showed that observation of reward delivery to another rat modulated the emission of USVs in observers and the release of dopamine (neurotransmitter involved, among other things, in reward processes and reinforcement learning) (Kashtelyan et al., 2014). Interestingly, rats seemed to experience a mixture of affective states while observing their conspecific receiving the treat but not when the reward was delivered to an empty box. On the first trial of conspecific observation, a strong release of dopamine and the highest rate and amplitude of positive calls (50 kHz) were registered. When the rat obtained the reward for itself, a release of dopamine was also observed, suggesting a positive emotional state matching between rats. However, during the following trials, dopamine release was reduced and the rate of negative calls (22 kHz) increased. Moreover, during these trials, observers rapidly oriented away from the rewarded rat. The authors suggested that these data could be indicative of a negative affective state (e.g., frustration) in the observer when watching another individual eating. Factors influencing emotional contagion responses Certain variables seemed to influence rodent responses in these studies: previous experience, familiarity, genetic background, rearing conditions, gender, stress levels and repeated exposure to the stimulus. For example, observer mice and rats displayed fear behaviors only if they previously had a shock experience similar to that of demonstrators (Atsak et al., 2011; Carrillo et al., 2015; Sanders et al., 2013). Specific genetic variations and the rearing conditions also influenced emotional contagion of fear and distress in rats and mice. Distinct mouse strains responded differently to the sight (S. Keum et al., 2016) and sound (Chen et al., 2009) of conspecifics receiving shocks. Besides, isolation-reared rats showed significantly less freezing behavior observing a demonstrator receiving foot-shocks compared to pairhoused rats (Yusufishaq & Rosenkranz, 2013). However, when it comes to familiarity the results are not so clear cut. On the one hand, a familiarity bias was reported in mice and degus fear responses: observers showed more freezing behavior when they were socially related to demonstrators (e.g., Gonzalez-Liencres et al., 2014; Jeon et al., 2010; Jeon & Shin, 2011; Lidhar et al., 2017; Pisansky, Young, et al., 2017). On the other hand, Sanders et al. (2013) did not find any familiarity bias in the freezing levels of observer mice, and the administration of oxytocin render male mice sensitive to the distress of strangers (Pisansky, Young, et al., 2017). Elevated stress levels could be responsible for the absence of emotional contagion in stranger dyads (Martin et al., 2015). In fact, blockade of glucocorticoid synthesis or receptors for adrenal stress hormones elicited the same pain behaviors among stranger and familiar pairs of mice and humans. PÉREZ-MANRIQUE AND GOMILA 5of26 Moreover, the induction of stress impaired the previously observed behavioral responses in familiar dyads (Martin et al., 2015). A recent meta-analysis (Hernandez-Lallement et al., 2020) found that, indeed, some of those factors had a significant modulatory effect on rodents' emotional contagion responses: breed (mice), prior experience with the stimulus (rats), social testing conditions, age or the sensory modality of the demonstrator cues. Conversely, they found no effect of sex and familiarity on emotional contagion of pain or fear. However, the authors remained cautious about these last results. In the case of sex, they relied on few data points and in the case of familiarity, the negative results could be due to important between-study differences in familiarity length (e.g., number of days rodents were together before the test). Furthermore, further analysis revealed a familiarity effect on pain contagion in mice, but only when demonstrators were subjected to abdominal pain. 2.1.2 |Nonhuman primates Several anecdotal reports have described possible cases of emotional contagion in nonhuman primates, especially in chimpanzees: mothers briefly whimpering when they heard their offspring whimper (de Waal, 2008); chimpanzees becoming excited upon seeing another individual become aroused (O'Connell, 1995); or the scaling up of group arousal through the emission of excited vocalizations (Fritz & Koelsch, 2013). The empirical study of emotional contagion in nonhuman primates started mainly in the ‘60s, with several experiments with rhesus macaques (Macaca mulatta). These monkeys received electric shocks while a conspecific observed their reactions (Masserman et al., 1964). The sight of a distressed individual affected the behavior of the observer up to the point that most of the macaques would suffer hunger rather than obtain food at the expense of shocking a partner. In their turn, Miller and colleagues carried out a set of experiments in which two macaques engaged in a cooperativeconditioning paradigm. In these studies, the demonstrator had access to the conditioned stimulus that was paired with noxious stimuli and the responder had access to a lever that, if operated, avoided aversive stimulation for both macaques. Importantly, the responder could see the face of the demonstrator during the testing sessions. The experiments showed that (1) macaques do react to the emotional expressions of other individuals (Miller et al., 1963; Mirsky et al., 1958); (2) observers did not respond when a monkey puppet or a rat received the shock (Miller et al., 1959); and that (3) macaques exhibited the same heart rate (HR) response when experiencing distress and when perceiving distress in others (Miller, 1967). Several studies have more recently assessed the behavioral and physiological responses of chimpanzees to the sight and sound of emotional expressions of conspecifics. Berntson et al. (1989) exposed infant chimpanzees to conspecifics' emotional vocalizations and recorded changes in HR and behavior. Conspecific laughter had an acceleratory influence in HR and evoked vocalizations similar to adult threat-barks. Conversely, screams evoked decelerating HR responses. These findings indicate that cardiac responses of infant chimpanzees differentiate between scream and laughter stimuli. However, infants' reactions to laughter were more reminiscent of a defensive reaction than of a positive emotional state. In another study (Parr & Hopkins, 2000), chimpanzees' tympanic membrane temperature (Tty) was measured while they watched three types of emotional videos: positive, neutral or negative. Tty is an index of brain temperature changes that, in turn, indicates variations in physiological arousal (Hopkins & Fowler, 1998). Right Tty increased significantly in response to the negative emotional videos and left Tty increased in response to the positive videos, but not significantly. This outcome might suggest lateralization of emotional processing in chimpanzees. Moreover, during negative videos chimpanzees responded with strong visual orientation, piloerection, pant-hooting vocalizations and bluff-displays, indicators of a high arousal state. In a similar experiment (Parr, 2001), chimpanzees watched three categories of negative emotional videos. A decrease in peripheral skin temperature (an indicator of negative arousal) was recorded when chimpanzees viewed videos of individuals injected with needles or videos showing needles but not when watching videos of a conspecific chasing the veterinarian. There were no significant differences in the responses to the sight of conspecific injected and the sight of needles themselves. Thus, it was not clear that the physiological changes were triggered by the perception of another's distress rather than by the sight of an aversive stimulus like needles. Furthermore, two studies have used infrared thermography to examine changes in skin temperature in wild and captive chimpanzees exposed to different types of emotional stimuli (Dezecache et al., 2017; Kano et al., 2016). Kano et al. (2016) registered nasal temperature, cortisol level, HR and behavioral responses of chimpanzees exposed to playback sounds or videos of conspecifics fighting. Chimpanzees showed changes in excitement behavior and HR-variability 6of26 PÉREZ-MANRIQUE AND GOMILA in response to these stimuli but not in salivary cortisol. Furthermore, chimpanzees' nasal temperature decreased in response to the playbacks and videos of conspecific agonistic interactions. In turn, Dezecache et al. (2017) assessed changes in surface body temperature of wild chimpanzees upon hearing different conspecific vocalizations. Overall, they found that aversive vocalizations induced larger decreases in temperature in the nasal area compared to neutral vocalizations, data that match that obtained with captive individuals (Kano et al., 2016). In turn, neutral calls produced larger increases in temperature in the ear region than aversive ones. Moreover, the vocalizations that were associated with more dramatic temperature changes were the aggressive barks, vocalizations that have been proposed to be highly emotional (Dezecache et al., 2017). Overall, it has been reported a link between a decrease in nasal temperature and negative emotional states (Adriaense et al., 2020). Therefore, these findings suggest the occurrence of contagion of negative emotions in chimpanzees. However, there are still discrepancies and inconsistencies in the data on facial temperature and its relationship with emotional states, thus, more research is needed to extract solid conclusions based on thermal results. Furthermore, the use of aggressive vocalizations as stimuli might not be the best to assess emotional contagion since they can trigger fear responses in the listener without involving the sharing of emotions. In turn, tufted capuchin monkeys (Sapajus apella) appropriately associated the emotional valence of conspecifics' expressions with a container, preferring to reach the one that elicited positive expressions in the demonstrator (Morimoto & Fujita, 2011, 2012). However, no clear responses indicative of emotional contagion between observers and demonstrators were registered, despite demonstrators displaying overt emotions during the experiment (Morimoto & Fujita, 2012). Finally, a study assessed the occurrence of visual contagion of grooming, affiliative behavior associated with positive and relaxed states, in a group of semi-free-ranging female Barbary macaques (Macaca sylvanus) (Berthier & Semple, 2018). In this group, observing conspecifics groom produced a reduction of behavioral indicators of anxiety and an increase in the number of different affiliative behaviors. These results suggest that both being groomed and observing others grooming, induce, in fact, a positive state in macaques and that this state can be transferred to bystanders. However, this study does not allow to differentiate whether these outcomes were the result of emotional or behavioral contagion. 2.1.3 |Swine and bovids Interest in whether emotional contagion is found in swine and bovids has been related to animal welfare in farms. Some evidence of emotional state matching has been found, but experimental control in this area needs improvement. Some interesting research has been done on the reactions of farm animals to distressed conspecifics. Anil et al. (1997;1996), for example, investigated the stress responses of pigs (Sus scrofa domestica) and sheep (Ovis aries) witnessing the process of slaughtering of conspecifics. They did not find any specific stress-related changes in pigs or sheep when witnessing stunning or slaughter, although the levels of stress-related hormones and HR tended to be high during the process due to human contact and handling. Both studies lacked rigorous controls, so they were not able to distinguish between effects due to the experience of the observers and those triggered by the slaughter. Reimert et al. (2013) assessed the responses of naive pigs (observers) to the emotional responses of a trained pen mate (demonstrator). The demonstrator had had experience with the auditory and visual cues that signaled rewarding and aversive events, and the naive pig observed its reactions during the anticipation and experience of the events. The behavior of both pigs matched, displaying behaviors indicative of positive emotions (e.g., play) during the rewarding events and behavioral indicators of negative emotions (e.g., tail low, increased level of defecation and urination, lowpitched vocalizations, etc.) during the aversive events. Salivary cortisol measurements supported these behavioral observations, indicating that both pigs were aroused by the events. The authors ruled out the possibility that naive pigs were just copying the behaviors from the demonstrators since, during the events, observers could not see the demonstrators only hear them. In two follow-up studies, Reimert et al. (2015, 2017) used the same paradigm to examine the influence of intranasal doses of oxytocin (neurohormone that has been related to empathic processes) on observer pigs' behavior, and whether the emotional responses of the demonstrator had long-term effects on observers' emotional state. Oxytocin did not significantly affect observers' behavior, except by increasing the number of negative vocalizations (Reimert et al., 2015). Surprisingly, it affected the behavior of the demonstrators which had not received oxytocin. Thus, the authors concluded that oxytocin may play a role in pig auditory or olfactory communication. In turn, the emotional state of a pig subjected to either a positive or negative treatment affected (positively and negatively, respectively) the state of PÉREZ-MANRIQUE AND GOMILA 7of26 observers in the period after the treatment (Reimert et al., 2017). However, the positive emotional state elicited in the observer pigs could also be due to the exposure to traces of peat and chocolate raisins present on the demonstrator body after the treatment, rather than triggered by emotional contagion. Another study (Goumon & Špinka, 2016) showed that piglets responded to the sight of a frightened pen mate with greater attention and more indicators of fear than to the sight of an unaltered mate. Furthermore, experienced observers reacted more strongly than naïve ones. The authors stated that these responses could be indicative of emotional contagion of fear between piglets. Baciadonna et al. (2019), using a habituation–dishabituation–rehabituation playback paradigm, showed that goats (Capra hircus) seem to distinguish the valence of conspecific calls. Goats were exposed to conspecific calls of the same type (contact call) but differing in their valence (positive and negative). First, they were habituated to listen to a positive or negative call. Then, in the dishabituation phase, the valence of the call was reversed and was followed by a final call from the habituation phase as control. When the valence of the call was reversed, goats look more towards the speaker. Furthermore, whereas the valence of the call did not affect goats' HR, in the habituation/rehabituation phases HR variability tended to be higher when goats were exposed to positive vocalizations than when exposed to negative ones. 2.1.4 |Canids Dogs are a very interesting animal model to study inter-species emotional contagion due to their close bond with humans. It has been reported that during positive interactions there is a physiological and hormonal synchronization (Odendaal & Meintjes, 2003) and a positive correlation of HR variability changes (Katayama et al., 2019) between dogs and their owners. Moreover, dogs seem to discriminate human emotions (Deputte & Doll, 2011) and emotional expressions of human faces (Müller et al., 2015). Even human odors excreted during emotional situations of different valence could distinctly affect dogs' behavioral and cardiac responses (D'Aniello et al., 2018). Using different paradigms, several studies have evaluated the occurrence of emotional contagion between dogs and humans. In one of them, dogs were exposed to 4 conditions: two in which their owner or a stranger pretended to cry and two in which they hummed a song (Custance & Mayer, 2012). Dogs oriented significantly more often towards their owner or the stranger during the crying condition. Furthermore, most of the dogs approached the person in a submissive way and two dogs produced mild distress vocalizations. When the stranger was pretending to cry, dogs sniffed, nuzzled and licked him instead of seeking out their owner for comfort. Thus, the authors suggested that dogs' reactions were driven rather by emotional contagion than by personal distress (a self-focused, aversive emotional response triggered by the perception of another's distress [Batson, 1991]). Sümegi et al. (2014) examined whether the owner's stress level could be contagious to the dog using as an indicator the registered changes in dogs' performance in a spatial working memory task (remember the location of a ball). This paradigm is supported by data showing a significant effect of perceived stress on subjects' cognitive performance in memory tasks (McEwen & Sapolsky, 1995). Task completion was indeed affected by dog owners' anxiety state: dogs showed better performance in the task after interacting with their stressed owner. A stressful period in which dogs were separated from their owners also improved dogs' performance in the test. Yong and Ruffman (2014) assessed whether humans and dogs showed signs of emotional contagion responses to three auditory stimuli: a human infant crying, a human infant babbling and ‘white noise’. They found that, only after the crying condition, cortisol levels increased significantly from the baseline in both species. Moreover, dogs behave in a submissive and alert manner in response to crying. Similarly, Huber et al. (2017) exposed dogs to positive and negative sounds of humans or conspecifics and nonemotional sounds and measured their behavioral responses. Dogs displayed significantly more indicators of arousal and negative emotional states (e.g., more time freezing) when hearing negative sounds compared to positive ones, irrespectively of the species producing the sound. These results suggest an inter and intra-specific contagion of emotional valence. To date, three studies have assessed prosocial rescue behavior in dogs and whether this behavior relies on emotional contagion (Carballo et al., 2020; Sanford, 2017; Van Bourg et al., 2020). In these experiments, dogs had the opportunity to free their seemingly trapped owner from a compartment. Dogs were tested in one condition in which the owner displayed signs of distress and in different control conditions (e.g., the owner hummed or read inside the box). In general, dogs released their owner more often in the distress condition compared to the control conditions. However, only one of the studies provided clear evidence that dogs were affected by the distress cues emitted by their owners (Van Bourg 8of26 PÉREZ-MANRIQUE AND GOMILA et al., 2020): dogs displayed significantly more behavioral stress responses in the stress condition than in the control ones. Finally, a study tested whether dogs experience emotional contagion and direct empathy-like behaviors towards familiar individuals (dogs that lived together) after hearing conspecifics' distress whines (Quervel-Chaumette et al., 2016). Each dog participated in three conditions in which they were first exposed to the playback of three stimuli: either familiar whines (from their partner), stranger whines or control sounds. Then, they were reunited with their partners. Whereas dogs displayed higher alertness and more stress-related behaviors in the whine conditions compared with the control condition, none of these responses was influenced by familiarity. That is, dogs did not respond differently to whines according to the identity of the caller. Unlike the study of Yong and Ruffman (2014), no increase in salivary cortisol levels was found. Dogs spent more time near their partner and engaged in more affiliative behaviors after the whine conditions than after the control condition. 2.1.5 |Elephants Elephants have complex social behavior and share close bonds with family members, features which make them a very interesting study species for emotional contagion research (Plotnik & de Waal, 2014). However, there are not many empirical studies with well-defined controls assessing emotional contagion, and most of the available data come from anecdotal reports. The available evidence suggests that when a member of a group experiences distress, the others react emotionally. Although anecdotal reports have been called into question for several reasons (see Bates & Byrne, 2007), they can provide valuable data. For example, Douglas-Hamilton et al. (2006) carried out a rigorous observational report using long-term associations records, GPS tracking data and direct observations of a group of African elephants (Loxodonta africana). They reported the behavioral responses of different elephants towards a dying and deceased matriarch. For example, when the injured matriarch fell to the ground showing signs of distress such as temporal gland secretion (related to stress, excitement or fear in elephants [Gorman, 1986]), an unrelated matriarch rapidly approached her displaying signs of excitement too, as tail raised, emission of vocalizations and temporal gland secretion. This female also tried to lift her. Sikes, in 1971 (Schulte, 2000) described a similar case in which an elephant was mortally wounded and could not rise. The other group members tried to lift it, but they failed, so they started circling the injured individual (an indicator of stress in elephants [Ranaweerage et al., 2015]). Similar observations were made in Asian elephants (Elephas maximus). Sharma et al. (2020) registered the responses of an adult female to an injured and dying calf. This female tried to lift the calf and emitted a series of vocalizations (trumpets) that could be indicative of her distress. Jointly, these studies indicate that elephants are affected by the sight of a suffering individual. During those situations, they displayed both behavioral and physiological signals of distress that, sometimes, appeared to match those of the distressed individual suggesting the occurrence of an emotional state-matching. Regarding empirical evidence of emotional contagion in elephants, we can only mention the study of Plotnik and de Waal (2014). They investigated affiliative tendencies between Asian elephants living in an elephant camp after distressing events (e.g., conspecific intimidation or aggression, group separation, environmental threat). The behavioral and emotional state of observer elephants matched those of individuals that had undergone a distressful event. More specifically, bystanders adopted the agitated behavior of the distressed individual (e.g., ears presented forward, erected tail, vocalizations, urination and defecation). Following a distress display, observers engaged in significantly more reassuring responses towards the distressed individual and directed more contacts to other elephants than during control periods with no distress displays. However, this study lacked well-defined controls to distinguish between the observer's behaviors triggered by the perception of distress in others from the behaviors elicited by the distressing event itself. 2.1.6 |Horses In recent years, research on emotional processes of domestic horses (Equus caballus) has experienced great advances. These animals recognize and remember human emotional facial expressions (Nakamura et al., 2018; Trösch et al., 2019), and use those memories to adapt their behavior in subsequent interactions with humans (Proops et al., 2018). Furthermore, human anxiety might be contagious to horses. A study reported that when a person PÉREZ-MANRIQUE AND GOMILA 9of26 TABLE 1 (Continued) Measures Behavioral changes Physiological and hormonal changes Cognitive performance Others Stimulus* HR Temperature changes Hormonal changes (cortisol, corticosterone) Changes in memory/ Learning Cognitive bias Changes in pain sensitivity Chickens (Edgar et al., 2011; Edgar et al., 2012; Edgar et al., 2013; Edgar & Nicol, 2018) Pigs and Sheep (Anil et al., 1996; Anil et al., 1997) Degus (Lidhar et al., 2017) Pigs and Sheep (Anil et al., 1996; Anil et al., 1997) Conspecific in pain Rats (Li et al., 2014) Rats (Li et al., 2014) Rats (Du et al., 2020; Li et al., 2018; Li et al., 2014; Lü et al., 2017) Mice (Langford et al., 2006; Martin et al., 2015) Mice (Du et al., 2020; Langford et al., 2006; Martin et al., 2015) Fearful demonstrator Rhesus macaques (Miller et al., 1959) (pictures) Mice (Bredy & Barad, 2009; Nowak et al., 2013; Panksepp & Lahvis, 2016) Rats (Jones et al., 2014; Jones & Monfils, 2016; Kim et al., 2010; Knapska et al., 2010; Pereira et al., 2012) Rats (Bruchey et al., 2010; Jones et al., 2014; Jones & Monfils, 2016; Knapska et al., 2010) Prairie voles (Burkett et al., 2016) 16 of 26 PÉREZ-MANRIQUE AND GOMILA TABLE 1 (Continued) Measures Behavioral changes Physiological and hormonal changes Cognitive performance Others Stimulus* HR Temperature changes Hormonal changes (cortisol, corticosterone) Changes in memory/ Learning Cognitive bias Changes in pain sensitivity Agonistic interactions of conspecifics Chimpanzees (Kano et al., 2016) (video, playback) Chimpanzees (Kano et al., 2016) (video,playback) Chimpanzees (Parr & Hopkins, 2000) (video) (Kano et al., 2016) (video,playback) Chimpanzees (Kano et al., 2016) video, playback Rats (Patki et al., 2014) Rats (Carnevali et al., 2017; Finnell et al., 2017, 2018, Patki et al., 2014, 2015) Rats (Carnevali et al., 2017; Finnell et al., 2017, 2018) Rats (Carnevali et al., 2017; Finnell et al., 2017, 2018, Patki et al., 2014, 2015) Mice (Iñiguez et al., 2018; Li, Xu, & Wang, 2018; Miao et al., 2018; Warren et al., 2013, 2014) Greylag geese (Wascher et al., 2010) Mice (Iñiguez et al., 2018; Warren et al., 2013, 2014) Aggressive vocalizations of conspecifics Chimpanzees (Dezecache et al., 2017) Conspecific experiencing a negative event Tufted capuchin monkeys (Morimoto & Fujita, 2012) Horses (Trösch et al., 2020) Pigs (Reimert et al., 2013, 2015) Ravens (Adriaense et al., 2019) Pigs (Reimert et al., 2013, 2015) Horses (Trösch et al., 2020) (Continues) PÉREZ-MANRIQUE AND GOMILA 17 of 26 TABLE 1 (Continued) Measures Behavioral changes Physiological and hormonal changes Cognitive performance Others Stimulus* HR Temperature changes Hormonal changes (cortisol, corticosterone) Changes in memory/ Learning Cognitive bias Changes in pain sensitivity Conspecific experiencing a positive event Tufted capuchin monkeys (Morimoto & Fujita, 2012) Horses (Trösch et al., 2020) Pigs (Reimert et al., 2013, 2015) Ravens (Adriaense et al., 2019) Pigs (Reimert et al., 2013, 2015) Rats (Kashtelyan et al., 2014) Horses (Trösch et al., 2020) Positive interactions of conspecifics Barbary macaques (Berthier & Semple, 2018) Chimpanzees (Parr & Hopkins, 2000) (video) Ravens (Osvath & Sima, 2014) Positive vocalizations of conspecifics Horses (Briefer et al., 2017) Chimpanzees (Berntson et al., 1989) Chimpanzees (Dezecache et al., 2017) Rats (Saito et al., 2016) Keas (Schwing et al., 2017) Horses (Briefer et al., 2017) Horses (Briefer et al., 2017) a Stimulus:Stressed conspecific/human: exposure to a human or a conspecific which is under stress; Stressed conspecific (only auditory cues): exposure to the sounds emitted by a conspecific under stress; conspecific experiencing negative stimulation: exposure to a conspecific which, in that moment, is receiving painful stimulation (the aversive stimulus is present); conspecific in pain: exposure to a conspecific that has been subjected to a treatment inducing pain (e.g., injection of venom) (the aversive stimulus is not present); fearful demonstrator: exposure to a conspecific which is frightened due to a previous treatment; agonistic interactions of conspecifics: exposure to two or more conspecifics interacting in an agonistic manner (e.g., fights); aggressive vocalizations of conspecifics: exposure to aggressive vocalizations of conspecifics; conspecific experiencing a negative event: exposure to a conspecific being subjected to an unpleasant event, without causing harm or fear in the individual (e.g., frustration); conspecific experiencing a positive event: exposure to a conspecific enjoying a pleasant situation; positive interactions of conspecifics: exposure to two or more conspecifics interacting in a positive way (e.g., play); positive vocalizations of conspecifics: exposure to vocalizations emitted by conspecifics during positive situations (e.g., play). 18 of 26 PÉREZ-MANRIQUE AND GOMILA advantages, the contagion of negative emotions such as fear could be widespread among animals and be displayed in several contexts; while the contagion of positive emotions could be restricted to a reduced number of social species. This is a question for further research. 3.3 |Assessment of contagion processes even though evidence has been found suggesting possible cases of emotional state-matching in chimpanzees, elephants, birds, rodents or pigs (Burkett et al., 2016; Douglas-Hamilton et al., 2006; Langford et al., 2006; Parr & Hopkins, 2000; Perez et al., 2015; Reimert et al., 2013, 2017; Warren et al., 2013) the number of studies specifically assessing an emotional match between individuals is still small. Moreover, many of the reviewed studies did not register the responses of both individuals (observers and demonstrators) to assess the occurrence of an emotional convergence. Although emotional contagion is broadly defined as the emotional state-matching of an individual with another, even in humans it is not well established whether the emotional response triggered by the perception of another's emotional state is isomorphic or not to the perceived affective state (de Vignemont & Singer, 2006). The transmission of certain emotions might not imply a perfect emotional match. There may be differences in arousal or a mismatch between the behaviors or the physiological states of observers and demonstrators even if an emotional transfer has taken place. For example, in the case of distress contagion, likely, the observer's emotional response triggered by the perception of a conspecific in distress differ in magnitude from that of the demonstrator. Therefore, more research is needed to clarify this issue. Furthermore, the evidence is not always powerful enough to rule out an alternative interpretation of individuals' emotional convergence in terms of distress, instead of contagion. Studies need to exclude the possibility that the emotional-state matching is due to the observer responding to environmental aversive cues rather than the demonstrator emotional state. Thus, the demonstrator's emotional cues must be the main source of emotion induction in the observer. A good way to do so is to control that the observer cannot perceive the stimulus which triggers demonstrator's emotional response, as proposed by Adriaense et al. (2020). In experimental paradigms, therefore, it is crucial the election of the appropriate emotional stimulus to induce contagion in the observer: 1) this stimulus must be the emotional state of the demonstrator and 2) this state should trigger a similar emotional state in the observer. Not all emotions may be equally effective in triggering the same emotional state in both individuals. For example, inducing frustration or anger in the demonstrator may induce different emotional states of the same negative valence in the observer. That is, demonstrator's frustration or aggressive displays could trigger distress or fear responses in the observer due to the probability of becoming the target of redirected aggression. Based on the results of the reviewed studies, emotions such as fear or positive emotions are good candidates to assess emotional contagion because they seem to induce similar emotional states in both individuals. 4|CONCLUSION The reviewed studies show that certain animals seem to be affected by the emotional displays of others, suggesting that the sharing of emotions could be widespread among social species capable of emotions. Emotional contagion seems to be related to the ecological circumstances and socio-behavioral traits of the species and thus present a great variability across the animal kingdom. Therefore, depending on the species, it could be triggered by a great variety of stimuli, modulated by different factors and be based on distinct mechanisms. This phenomenon thus could be far more complex and flexible than previously thought, and we should be cautious when generalizing about its functions and mechanisms between species. From this point of view, while it seems clear that emotional contagion involves some perceptionaction mediating systems (as suggested by Preston & de Waal, 2002), its workings look much more flexible and contextdependent than expected if it were an automatic response –what suggests an interaction of several components (as suggested by Yamamoto, 2017). Overall, more research is needed to expand our understanding of the mechanisms and functions of emotional contagion and the extent to which this process is present in a wide variety of animal species. Simultaneously registering the different responses of observers and demonstrators would allow us to reliably establish the occurrence of an emotional state-matching between individuals. Furthermore, future studies should provide more evidence on the link between these processes, prosociality and complex empathic behaviors. The use of systematized paradigms including both behavioral and physiological measures and reliable controls to test different species are much needed in this endeavor. PÉREZ-MANRIQUE AND GOMILA 19 of 26 ACKNOWLEDGMENTS This research has received the support of the Spanish Government through project FFI2017-86351-R (AEI, FEDER, EU). Ana Pérez-Manrique was supported by an FPU PhD scholarship from the Spanish Ministry of Education, Culture and Sport (AP2012-3501). This research has received the support of the Ministerio de Ciencia, Innovaci on y Universidades (MCIU), the Agencia Estatal de Investigaci on (AEI) and the European Regional Development Funds (ERDF, EU) to the project FFI2017-86351-R. CONFLICT OF INTEREST The authors have declared no conflicts of interest for this article. AUTHOR CONTRIBUTIONS Ana Pérez-Manrique: Data curation; methodology; writing-original draft; writing-review & editing. Antoni Gomila: Conceptualization; funding acquisition; methodology; supervision; writing-review & editing. DATA AVAILABILITY STATEMENT Data sharing is not applicable to this article as no new data were created or analyzed in this study. ORCID Antoni Gomila https://orcid.org/0000-0001-7325-961X RELATED WIREs ARTICLES Combinatoriality in the vocal systems of nonhuman animals Theory of mind in animals: Current and future directions Self-control in crows, parrots and nonhuman primates REFERENCES Adriaense, J. E. C., Koski, S. E., Huber, L., & Lamm, C. (2020). Challenges in the comparative study of empathy and related phenomena in animals. Neuroscience & Biobehavioral Reviews,112,62–82. http://doi.org/10.1016/j.neubiorev.2020.01.021 Adriaense, J. E. C., Martin, J. S., Schiestl, M., Lamm, C., & Bugnyar, T. (2019). Negative emotional contagion and cognitive bias in common ravens (Corvus corax). Proceedings of the National Academy of Sciences of the United States of America,166(23), 11547–11552. http://doi. org/10.1073/pnas.1817066116 Allsop, S. A., Wichmann, R., Mills, F., Burgos-Robles, A., Chang, C. J., Felix-Ortiz, A. C., …Tye, K. M. (2018). Corticoamygdala transfer of socially derived information gates observational learning. Cell,173(6), 1329–1342.e18. http://doi.org/10.1016/j.cell.2018.04.004 Anil, M., McKinstry, J., Field, M., & Rodway, R. (1997). Lack of evidence for stress being caused to pigs by witnessing the slaughter of conspecifics. Animal Welfare,6(1), 3–8. Retrieved from http://www.ingentaconnect.com/content/ufaw/aw/1997/00000006/00000001/ art00001 Anil, M., Preston, J., & McKinstry, J. (1996). An assessment of stress caused in sheep by watching slaughter of other sheep. Animal Welfare, 5(4), 435–441. Retrieved from http://www.ingentaconnect.com/content/ufaw/aw/1996/00000005/00000004/art00007 Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., …Keysers, C. (2011). Experience modulates vicarious freezing in rats: a model for empathy. PLoS One,6(7), e21855. http://doi.org/10.1371/journal.pone.0021855 Baciadonna, L., Briefer, E. F., Favaro, L., & Mcelligott, A. G. (2019). Goats distinguish between positive and negative emotion-linked vocalisations. Frontiers i n Zoology,16, 25. http://doi.org/10.1186/s12983-019-0323-z Bates, L. A., & Byrne, R. W. (2007). Creative or created: using anecdotes to investigate animal cognition. Methods (San Diego, Calif.),42(1), 12–21. http://doi.org/10.1016/j.ymeth.2006.11.006 Batson, C. D. (1991). The altruism question: Toward a social-psychological answer (1st ed.). Lawrence Erlbaum Associates, Inc. Berntson, G. G., Boysen, S. T., Bauer, H. R., & Torello, M. S. (1989). Conspecific screams and laughter: Cardiac and behavioral reactions of infant chimpanzees. Developmental Psychobiology,22(8), 771–787. http://doi.org/10.1002/dev.420220803 Berthier, J. M., & Semple, S. (2018). Observing grooming promotes affiliation in Barbary macaques. Proceedings of the Royal Society B: Biological Sciences,285(1893), 20181964. http://doi.org/10.1098/rspb.2018.1964 Boesch, C. (2020). Identifying animal complex cognition requires natural complexity. iScience,24, 102195. Bredy, T. W., & Barad, M. (2009). Social modulation of associative fear learning by pheromone communication. Learning & Memory (Cold Spring Harbor, N.Y.),16(1), 12–18. http://doi.org/10.1101/lm.1226009 Briefer, E. F. (2018). Vocal contagion of emotions in non-human animals. Proceedings of the Royal Society B: Biological Sciences,285(1873), 20172783. http://doi.org/10.1098/rspb.2017.2783 Briefer, E. F., Mandel, R., Maigrot, A. L., Briefer Freymond, S., Bachmann, I., & Hillmann, E. (2017). Perception of emotional valence in horse whinnies. Frontiers in Zoology,14(1), 8. http://doi.org/10.1186/s12983-017-0193-1 20 of 26 PÉREZ-MANRIQUE AND GOMILA Bruchey, A. K., Jones, C. E., & Monfils, M.-H. (2010). Fear conditioning by-proxy: Social transmission of fear during memory retrieval. Behavioural Brain Research,214(1), 80–84. http://doi.org/10.1016/j.bbr.2010.04.047 Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B. M., & Young, L. J. (2016). Oxytocin-dependent consolation behavior in rodents. Science,351(6271), 375–378. http://doi.org/10.1126/science.aac4785 Campbell, M. W., & de Waal, F. B. M. (2011). Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy. PLoS ONE,6(4), e18283. https://doi.org/10.1371/journal.pone.0018283 Carballo, F., Dzik, V., Freidin, E., Dami an, J. P., Casanave, E. B., & Bentosela, M. (2020). Do dogs rescue their owners from a stressful situation? A behavioral and physiological assessment. Animal Cognition,23(2), 389–403. http://doi.org/10.1007/s10071-019-01343-5 Carnevali, L., Montano, N., Statello, R., Coudé, G., Vacondio, F., Rivara, S., …Sgoifo, A. (2017). Social stress contagion in rats: Behavioural, autonomic and neuroendocrine correlates. Psychoneuroendocrinology,82, 155–163. http://doi.org/10.1016/j.psyneuen.2017.05.017 Carnevali, L., Montano, N., Tobaldini, E., Thayer, J. F., & Sgoifo, A. (2020). The contagion of social defeat stress: Insights from rodent studies. Neuroscience and Biobehavioral Reviews,111,12–18. http://doi.org/10.1016/j.neubiorev.2020.01.011 Carrillo, M., Migliorati, F., Bruls, R., Han, Y., Heinemans, M., Pruis, I., …Keysers, C. (2015). Repeated witnessing of conspecifics in pain: Effects on emotional contagion. PLoS One,10(9), e0136979. http://doi.org/10.1371/journal.pone.0136979 Chartrand, T. L., & Lakin, J. L. (2013). The antecedents and consequences of human behavioral mimicry. Annual Review of Psychology,64, 285–308. https://doi.org/10.1146/annurev-psych-113011-143754 Chen, Q., Panksepp, J. B., & Lahvis, G. P. (2009). Empathy is moderated by genetic background in mice. PLoS One,4(2), e4387. http://doi. org/10.1371/journal.pone.0004387 Church, R. M. (1959). Emotional reactions of rats to the pain of others. Journal of Comparative and Physiological Psychology,52(2), 132–134. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/13654562 Custance, D., & Mayer, J. (2012). Empathic-like responding by domestic dogs (Canis familiaris) to distress in humans: an exploratory study. Animal Cognition,15(5), 851–859. http://doi.org/10.1007/s10071-012-0510-1 D'Aniello, B., Semin, G. R., Alterisio, A., Aria, M., & Scandurra, A. (2018). Interspecies transmission of emotional information via chemosignals: from humans to dogs (Canis lupus familiaris). Animal Cognition,21(1), 67–78. http://doi.org/10.1007/s10071-017-1139-x Darwin, C. (1897). The expression of the emotions in man and animals. D. Appleton and Company. Davila-Ross, M., Menzler, S., & Zimmermann, E. (2008). Rapid facial mimicry in orangutan play. Biological Letters,4,27–30. http://doi.org/ 10.1098/rsbl.2007.0535 de Vignemont, F., & Singer, T. (2006). The empathic brain: how, when and why? Trends in Cognitive Sciences,10(10), 435–441. http://doi. org/10.1016/j.tics.2006.08.008 de Waal, F. B. M. (2007). The “Russian doll”model of empathy and imitation. In S. Bråten (Ed.), On being moved: From mirror neurons to empathy (pp. 49–69). John Benjamins Publishing Company. http://doi.org/10.1075/aicr.68.06waa de Waal, F. B. M. (2008). Putting the altruism back into altruism: the evolution of empathy. Annual Review of Psychology,59, 279–300. http:// doi.org/10.1146/annurev.psych.59.103006.093625 de Waal, F., & Preston, S. (2017). Mammalian empathy: Behavioural manifestations and neural basis. Nature Reviews Neuroscience,18, 498– 509. https://doi.org/10.1038/nrn.2017.72 Decety, J., Norman, G. J., Berntson, G. G., & Cacioppo, J. T. (2012). A neurobehavioral evolutionary perspective on the mechanisms underlying empathy. Progress in Neurobiology,98(1), 38–48. http://doi.org/10.1016/j.pneurobio.2012.05.001 Deputte, B. L., & Doll, A. (2011). Do dogs understand human facial expressions? Journal of Veterinary Behavior: Clinical Applications and Research,6(1), 78–79. http://doi.org/10.1016/j.jveb.2010.09.013 Dezecache, G., Zuberbühler, K., Davila-Ross, M., & Dahl, C. D. (2017). Skin temperature changes in wild chimpanzees upon hearing vocalizations of conspecifics. Royal Society Open Science,4(1), 160816. http://doi.org/10.1098/rsos.160816 Douglas-Hamilton, I., Bhalla, S., Wittemyer, G., & Vollrath, F. (2006). Behavioural reactions of elephants towards a dying and deceased matriarch. Applied Animal Behaviour Science,100(1–2), 87–102. http://doi.org/10.1016/j.applanim.2006.04.014 Du, R., Luo, W. J., Geng, K. W., Li, C. L., Yu, Y., Wei, N., & Chen, J. (2020). Empathic contagious pain and consolation in laboratory rodents: Species and sex comparisons. Neuroscience Bulletin,36, 649–653. http://doi.org/10.1007/s12264-020-00465-y Duffy, & Chartrand, T. L. (2015). Mimicry: Causes and consequences. Current Opinion in the Behavioral Sciences,3, 112–116. https://doi.org/ 10.1016/j.cobeha.2015.03.002 Edgar, J. L., Lowe, J. C., Paul, E. S., & Nicol, C. J. (2011). Avian maternal response to chick distress. Proceedings of the Royal Society B: Biological Sciences,278(1721), 3129–3134. http://doi.org/10.1098/rspb.2010.2701 Edgar, J. L., & Nicol, C. J. (2018). Socially-mediated arousal and contagion within domestic chick broods. Scientific Reports,8(1), 1–10. http:// doi.org/10.1038/s41598-018-28923-8 Edgar, J. L., Paul, E. S., Harris, L., Penturn, S., & Nicol, C. J. (2012). No evidence for emotional empathy in chickens observing familiar adult conspecifics. PLoS One,7(2), e31542. http://doi.org/10.1371/journal.pone.0031542 Edgar, J. L., Paul, E. S., & Nicol, C. J. (2013). Protective mother hens: Cognitive influences on the avian maternal response. Animal Behaviour,86(2), 223–229. http://doi.org/10.1016/j.anbehav.2013.05.004 Estes, W. K., & Skinner, B. F. (1941). Some quantitative properties of anxiety. Journal of Experimental Psychology,29(5), 390–400. https://doi. org/10.1037/h0062283 Fernandes da Silva, P., Garcia de Leaniz, C., & Luchiari, A. C. (2019). Fear contagion in zebrafish: a behaviour affected by familiarity. Animal Behavior,153,95–103. https://doi.org/10.1016/j.anbehav.2019.05.004 PÉREZ-MANRIQUE AND GOMILA 21 of 26 Finnell, J. E., Lombard, C. M., Padi, A. R., Moffitt, C. M., Wilson, L. B., Wood, C. S., & Wood, S. K. (2017). Physical versus psychological social stress in male rats reveals distinct cardiovascular, inflammatory and behavioral consequences. PLoS One,12(2), e0172868. http:// doi.org/10.1371/journal.pone.0172868 Finnell, J. E., Muniz, B. L., Padi, A. R., Lombard, C. M., Moffitt, C. M., Wood, C. S., …Wood, S. K. (2018). Essential role of ovarian hormones in susceptibility to the consequences of witnessing social defeat in female rats. Biological Psychiatry,84(5), 372–382. http://doi.org/10. 1016/j.biopsych.2018.01.013 Fritz, T., & Koelsch, S. (2013). Acoustically mediated emotional contagion as an across-species homology underlying music processing. In E. Altenmüller, S. Schmidt, & E. Zimmermann (Eds.), Evolution of emotional communication (pp. 300–312). Oxford University Press. http:// doi.org/10.1093/acprof:oso/9780199583560.003.0018 Gonzalez-Liencres, C., Juckel, G., Tas, C., Friebe, A., & Brüne, M. (2014). Emotional contagion in mice: the role of familiarity. Behavioural Brain Research,263,16–21. http://doi.org/10.1016/j.bbr.2014.01.020 Gorman, M. L. (1986). The secretion of the temporal gland of the African elephant Loxodonta africana as an elephant repellent. Journal of Tropical Ecology,2(2), 187–190. https://doi.org/10.1017/S0266467400000766 Goumon, S., & Špinka, M. (2016). Emotional contagion of distress in young pigs is potentiated by previous exposure to the same stressor. Animal Cognition,19(3), 501–511. http://doi.org/10.1007/s10071-015-0950-5 Han, Y., Sichterman, B., Maria, C., Gazzola, V., & Keysers, C. (2020). Similar levels of emotional contagion in male and female rats. Scientific Reports,10(1), 1–12. http://doi.org/10.1038/s41598-020-59680-2 Hatfield, E., Cacioppo, J., & Rapson, R. (1994). Emotional contagion. Cambridge University Press. Hauser, M. D. (2000). The evolution of communication. A Bradford book. The MIT Press. Hernandez-Lallement, J., G omez-Sotres, P., & Carrillo, M. (2020). Towards a unified theory of emotional contagion in rodents—A meta-analysis. Neuroscience & Biobehavioral Reviews. http://doi.org/10.1016/j.neubiorev.2020.09.010 Hopkins, W. D., & Fowler, L. A. (1998). Lateralized changes in tympanic membrane temperature in relation to different cognitive tasks in chimpanzees (Pan troglodytes). Behavioral Neuroscience,112(1), 83–88. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/9517817 Huber, A., Barber, A. L. A., Farag o, T., Müller, C. A., & Huber, L. (2017). Investigating emotional contagion in dogs (Canis familiaris)to emotional sounds of humans and conspecifics. Animal Cognition,20(4), 703–715. http://doi.org/10.1007/s10071-017-1092-8 Iñiguez, S. D., Flores-Ramirez, F. J., Riggs, L. M., Alipio, J. B., Garcia-Carachure, I., Hernandez, M. A., …Castillo, S. A. (2018). Vicarious social defeat stress induces depression-related outcomes in female mice. Biological Psychiatry,83(1), 9–17. http://doi.org/10.1016/j. biopsych.2017.07.014 Isern-Mas, C., & Gomila, A. (2019). Making Sense of Emotional Contagion. Mente Journal of Philosophical Studies,35,71–100. Retrieved from http://www.humanamente.eu/index.php/HM/article/view/209 Ito, W., Erisir, A., & Morozov, A. (2015). Observation of distressed conspecific as a model of emotional trauma generates silent synapses in the prefrontal-amygdala pathway and enhances fear learning, but Ketamine abolishes those effects. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology,40(11), 2536–2545. http://doi.org/10.1038/npp.2015.100 Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H. E., Lin, S.-Y., …Shin, H.-S. (2010). Observational fear learning involves affective pain system and Cav1.2 Ca 2+ channels in ACC. Nature Neuroscience,13(4), 482–488. http://doi.org/10.1038/nn.2504 Jeon, D., & Shin, H. S. (2011). A mouse model for observational fear learning and the empathetic response. Current Protocols in Neuroscience, 57/1, 8.27.1–8.27.9. http://doi.org/10.1002/0471142301.ns0827s57 Jones, C. E., & Monfils, M.-H. (2016). Dominance status predicts social fear transmission in laboratory rats. Animal Cognition,19(6), 1051–1069. http://doi.org/10.1007/s10071-016-1013-2 Jones, C. E., Riha, P. D., Gore, A. C., & Monfils, M.-H. (2014). Social transmission of Pavlovian fear: Fear-conditioning by-proxy in related female rats. Animal Cognition,17(3), 827–834. http://doi.org/10.1007/s10071-013-0711-2 Kano, F., Hirata, S., Deschner, T., Behringer, V., & Call, J. (2016). Nasal temperature drop in response to a playback of conspecific fights in chimpanzees: A thermo-imaging study. Physiology and Behavior,155,83–94. http://doi.org/10.1016/j.physbeh.2015.11.029 Kashtelyan, V., Lichtenberg, N. T., Chen, M. L., Cheer, J. F., & Roesch, M. R. (2014). Observation of reward delivery to a conspecific modulates dopamine release in ventral striatum. Current Biology,24(21), 2564–2568. http://doi.org/10.1016/j.cub.2014.09.016 Katayama, M., Kubo, T., Yamakawa, T., Fujiwara, K., Nomoto, K., Ikeda, K., …Kikusui, T. (2019). Emotional contagion from humans to dogs is facilitated by duration of ownership. Frontiers in Psychology,10, 1678. http://doi.org/10.3389/fpsyg.2019.01678 Kavaliers, M., Colwell, D. D., & Choleris, E. (2003). Learning to fear and cope with a natural stressor: individually and socially acquired corticosterone and avoidance responses to biting flies. Hormones and Behavior,43(1), 99–107. http://doi.org/10.1016/S0018-506X(02)00021-1 Kavaliers, M., Colwell, D. D., & Choleris, E. (2005). Kinship, familiarity and social status modulate social learning about “micropredators” (biting flies) in deer mice. Behavioral Ecology and Sociobiology,58(1), 60–71. http://doi.org/10.1007/s00265-004-0896-0 Keeling, L. J., Jonare, L., & Lanneborn, L. (2009). Investigating horse–human interactions: The effect of a nervous human. Veterinary Journal,181(1), 70–71. http://doi.org/10.1016/j.tvjl.2009.03.013 Keum, S., Kim, A., Shin, J. J., Kim, J. H., Park, J., & Shin, H. S. (2018). A missense variant at the Nrxn3 locus enhances empathy fear in the mouse. Neuron,98(3), 588–601.e5. http://doi.org/10.1016/j.neuron.2018.03.041 Keum, S., Park, J., Kim, A., Park, J., Kim, K. K., Jeong, J., & Shin, H.-S. (2016). Variability in empathic fear response among 11 inbred strains of mice. Genes, Brain and Behavior,15(2), 231–242. http://doi.org/10.1111/gbb.12278 Keum, S., & Shin, H. (2016). Rodent models for studying empathy. Neurobiology of Learning and Memory,135,22–26. http://doi.org/10.1016/ j.nlm.2016.07.022 22 of 26 PÉREZ-MANRIQUE AND GOMILA Kim, A., Keum, S., & Shin, H.-S. (2019). Observational fear behavior in rodents as a model for empathy. Genes, Brain and Behavior,18(1), e12521. http://doi.org/10.1111/gbb.12521 Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J. (2010). Social transmission of fear in rats: The role of 22-kHz ultrasonic distress vocalization. PLoS One,5(12), e15077. http://doi.org/10.1371/journal.pone.0015077 Knapska, E., Mikosz, M., Werka, T., & Maren, S. (2010). Social modulation of learning in rats. Learning & Memory,17(1), 35–42. http://doi. org/10.1101/lm.1670910 Knapska, E., Nikolaev, E., Boguszewski, P., Walasek, G., Blaszczyk, J., Kaczmarek, L., & Werka, T. (2006). Between-subject transfer of emotional information evokes specific pattern of amygdala activation. Proceedings of the National Academy of Sciences of the United States of America,103(10), 3858–3862. http://doi.org/10.1073/pnas.0511302103 Langford, D. J., Crager, S. E., Shehzad, Z., Smith, S. B., Sotocinal, S. G., Levenstadt, J. S., …Mogil, J. S. (2006). Social modulation of pain as evidence for empathy in mice. Science (New York, N.Y.),312(5782), 1967–1970. http://doi.org/10.1126/science.1128322 Laviola, G., Zoratto, F., Ingiosi, D., Carito, V., Huzard, D., Fiore, M., & Macrì, S. (2017). Low empathy-like behaviour in male mice associates with impaired sociability, emotional memory, physiological stress reactivity and variations in neurobiological regulations. PLoS One,12 (12), e0188907. http://doi.org/10.1371/journal.pone.0188907 Li, C.-L., Yu, Y., He, T., Wang, R.-R., Geng, K.-W., Du, R., …Chen, J. (2018). Validating rat model of empathy for pain: effects of pain expressions in social partners. Frontiers in Behavioral Neuroscience,12, 242. http://doi.org/10.3389/fnbeh.2018.00242 Li, M., Xu, H., & Wang, W. (2018). An Improved model of physical and emotional social defeat: Different effects on social behavior and body weight of adolescent mice by interaction with social support. Frontiers in Psychiatry,9, 688. http://doi.org/10.3389/fpsyt.2018.00688 Li, Z., Lu, Y. F., Li, C. L., Wang, Y., Sun, W., He, T., …Chen, J. (2014). Social interaction with a cagemate in pain facilitates subsequent spinal nociception via activation of the medial prefrontal cortex in rats. Pain,155(7), 1253–1261. http://doi.org/10.1016/j.pain.2014.03.019 Lidhar, N. K., Insel, N., Dong, J. Y., & Takehara-Nishiuchi, K. (2017). Observational fear learning in degus is correlated with temporal vocalization patterns. Behavioural Brain Research,332, 362–371. http://doi.org/10.1016/j.bbr.2017.06.011 Liévin-Bazin, A., Pineaux, M., Clerc, O., Gahr, M., von Bayern, A. M. P., & Bovet, D. (2018). Emotional responses to conspecific distress calls are modulated by affiliation in cockatiels (Nymphicus hollandicus). PLoS One,13(10), e0205314. http://doi.org/10.1371/journal.pone.0205314 Lü, Y. F., Yang, Y., Li, C. L., Wang, Y., Li, Z., & Chen, J. (2017). The locus coeruleus–norepinephrine system mediates empathy for pain through selective up-regulation of P2X3 receptor in dorsal root ganglia in rats. Frontiers in Neural Circuits,11, 66. http://doi.org/10.3389/ fncir.2017.00066 Martin, L. J., Hathaway, G., Isbester, K., Mirali, S., Acland, E. L., Niederstrasser, N., …Mogil, J. S. (2015). Reducing social stress elicits emotional contagion of pain in mouse and human strangers. Current Biology,25(3), 326–332. http://doi.org/10.1016/j.cub.2014.11.028 Martin, L. J., Tuttle, A. H., & Mogil, J. S. (2014). The interaction between pain and social behavior in humans and rodents. Current Topics in Behavioral Neurosciences,20, 233–250. http://doi.org/10.1007/7854_2014_287 Masserman, J. H., Wechkin, S., & Terris, W. (1964). “Altruistic”behavior in rhesus monkeys. The American Journal of Psychiatry,121(1), 584–585. http://doi.org/10.1176/appi.ajp.121.6.584 McEwen, B. S., & Sapolsky, R. M. (1995). Stress and cognitive function. Current Opinion in Neurobiology,5(2), 205–216. http://doi.org/10. 1016/0959-4388(95)80028-X Meyza, K., & Knapska, E. (2018). What can rodents teach us about empathy? Current Opinion in Psychology.24,15–20. http://doi.org/10. 1016/J.COPSYC.2018.03.002 Meyza, K., Nikolaev, T., Kondrakiewicz, K., Blanchard, D. C., Blanchard, R. J., & Knapska, E. (2015). Neuronal correlates of asocial behavior in a BTBR T (+) Itpr3(tf)/J mouse model of autism. Frontiers in Behavioral Neuroscience,9, 199. http://doi.org/10.3389/fnbeh.2015.00199 Meyza, K. Z., Bartal, I. B. A., Monfils, M. H., Panksepp, J. B., & Knapska, E. (2017). The roots of empathy: Through the lens of rodent models. Neuroscience and Biobehavioral Reviews,76, 216–234. http://doi.org/10.1016/j.neubiorev.2016.10.028 Miao, Z., Mao, F., Liang, J., Szyf, M., Wang, Y., & Sun, Z. S. (2018). Anxiety-related behaviours associated with microRNA-206-3p and BDNF expression in pregnant female mice following psychological social stress. Molecular Neurobiology,55(2), 1097–1111. http://doi.org/10. 1007/s12035-016-0378-1 Mikosz, M., Nowak, A., Werka, T., & Knapska, E. (2015). Sex differences in social modulation of learning in rats. Scientific Reports,5, 18114. http://doi.org/10.1038/srep18114 Miller, R. (1967). Experimental approaches to the physiological and behavioral concomitants of affective communication in rhesus monkeys. In S. Altmann (Ed.), Social communication among primates (pp. 125–147). The University of Chicago Press. Miller, R. E., Banks, J. H., & Kuwahara, H. (1966). The communication of affects in monkeys: cooperative reward conditioning. The Journal of Genetic Psychology,108(1), 121–134. http://doi.org/10.1080/00221325.1966.9914438 Miller, R. E., Banks, J. H., & Ogawa, N. (1963). Role of facial expression in “cooperative-avoidance conditioning”; in monkeys. Journal of Abnormal and Social,67(1), 24–30. http://doi.org/10.1037/h0044018 Miller, R. E., Murphy, J. V., & Mirsky, I. A. (1959). Non-verbal communication of affect. Journal of Clinical Psychology,15(2), 155–158. http://doi.org/10.1002/1097-4679(195904)15:2<155::AID-JCLP2270150211>3.0.CO;2-P Mirsky, I. A., Miller, R. E., & Murphy, J. V. (1958). The communication of affect in Rhesus monkeys. I An experimental method. Journal of the American Psychoanalytic Association,6(3), 433–441. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/13575267 Mogil, J. S. (2012). The surprising empathic abilities of rodents. Trends in Cognitive Sciences,16(3), 143–144. http://doi.org/10.1016/j.tics. 2011.12.012 PÉREZ-MANRIQUE AND GOMILA 23 of 26 Mogil, J. S. (2015). Social modulation of and by pain in humans and rodents. Pain,156(4), S35–S41. http://doi.org/10.1097/01.j.pain. 0000460341.62094.77 Morimoto, Y., & Fujita, K. (2011). Capuchin monkeys (Cebus apella) modify their own behaviors according to a conspecific's emotional expressions. Primates,52(3), 279–286. http://doi.org/10.1007/s10329-011-0249-3 Morimoto, Y., & Fujita, K. (2012). Capuchin monkeys (Cebus apella) use conspecifics' emotional expressions to evaluate emotional valence of objects. Animal Cognition,15(3), 341–347. http://doi.org/10.1007/s10071-011-0458-6 Müller, C. A., Schmitt, K., Barber, A. L. A., & Huber, L. (2015). Dogs can discriminate emotional expressions of human faces. Current Biology, 25(5), 601–605. http://doi.org/10.1016/j.cub.2014.12.055 Nakamura, K., Takimoto-Inose, A., & Hasegawa, T. (2018). Cross-modal perception of human emotion in domestic horses (Equus caballus). Scientific Reports,8(1), 8660. http://doi.org/10.1038/s41598-018-26892-6 Niedenthal, P. (2007). Embodying emotion. Science,316(5827), 1002–1005. https://doi.org/10.1126/science.1136930 Nicol, C. J., Caplen, G., Edgar, J., & Browne, W. J. (2009). Associations between welfare indicators and environmental choice in laying hens. Animal Behaviour,78(2), 413–424. http://doi.org/10.1016/j.anbehav.2009.05.016 Norscia, I., & Palagi, E. (2011). Yawn contagion and empathy in homo sapiens. PLoS ONE,6(12), e28472. https://doi.org/10.1371/journal. pone.0028472 Nowak, A., Werka, T., & Knapska, E. (2013). Social modulation in extinction of aversive memories. Behavioural Brain Research,238(1), 200– 205. http://doi.org/10.1016/j.bbr.2012.10.031 O'Connell, S. M. (1995). Empathy in chimpanzees: Evidence for theory of mind? Primates,36(3), 397–410. http://doi.org/10.1007/ BF02382862 Odendaal, J. S. J., & Meintjes, R. A. (2003). Neurophysiological correlates of affiliative behaviour between humans and dogs. The Veterinary Journal,165(3), 296–301. http://doi.org/10.1016/S1090-0233(02)00237-X Oliveira, T. A., Idalencio, R., Kalichak, F., dos Santos Rosa, J. G., Koakoski, G., de Abreu, M. S., …Barcellos, L. J. G. (2017). Stress responses to conspecific visual cues of predation risk in zebrafish. PeerJ,5, e3739. http://doi.org/10.7717/peerj.3739 Osvath, M., & Sima, M. (2014). Sub-adult Ravens synchronize their play: A case of emotional contagion? Animal Behavior and Cognition,2 (2), 197. http://doi.org/10.12966/abc.05.09.2014 Palagi, E., Celeghin, A., Tamietto, M., Winkielman, P., & Norscia, I. (2020). The neuroethology of spontaneous mimicry and emotional contagion in human and non-human animals. Neuroscience & Biobehavioral Reviews,111, 149–165. https://doi.org/10.1016/j.neubiorev.2020.01.020 Palagi, E., Leone, A., Mancini, G., & Ferrari, P. F. (2009). Contagious yawning in gelada baboons as a possible expression of empathy. Proceedings of the National Academy of Sciences of the United States,106(46), 19262–19267. https://doi.org/10.1073/pnas.0910891106 Palagi, E., Marchi, E., Cavicchio, P., et al. (2019). Sharing playful mood: Rapid facial mimicry in Suricata suricatta. Animal Cognition,22, 719–732. https://doi.org/10.1007/s10071-019-01269-y Palagi, E., Norscia, I., & Cordoni, G. (2018). Facial mimicry and play: A comparative study in chimpanzees and gorillas. Emotion,19(4), 665– 681. https://doi.org/10.1037/emo0000476 Panksepp, J. B., & Lahvis, G. P. (2011). Rodent empathy and affective neuroscience. Neuroscience and Biobehavioral Reviews,35, 1864–1875. http://doi.org/10.1016/j.neubiorev.2011.05.013 Panksepp, J. B., & Lahvis, G. P. (2016). Differential influence of social versus isolate housing on vicarious fear learning in adolescent mice. Behavioral Neuroscience,130(2), 206–211. http://doi.org/10.1037/bne0000133 Parr, L. A. (2001). Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes). Animal Cognition,4(3–4), 223–229. http://doi.org/10.1007/s100710100085 Parr, L. A., & Hopkins, W. D. (2000). Brain temperature asymmetries and emotional perception in chimpanzees, Pan troglodytes.Physiology and Behavior,71(3–4), 363–371. http://doi.org/10.1016/S0031-9384(00)00349-8 Patki, G., Salvi, A., Liu, H., & Salim, S. (2015). Witnessing traumatic events and post-traumatic stress disorder: Insights from an animal model. Neuroscience Letters,600,28–32. http://doi.org/10.1016/j.neulet.2015.05.060 Patki, G., Solanki, N., & Salim, S. (2014). Witnessing traumatic events causes severe behavioral impairments in rats. International Journal of Neuropsychopharmacology,755(12), 2017–2029. http://doi.org/10.1017/S1461145714000923 Paul, E. S., Harding, E. J., & Mendl, M. (2005). Measuring emotional processes in animals: The utility of a cognitive approach. Neuroscience and Biobehavioral Reviews,29(3), 469–491. http://doi.org/10.1016/j.neubiorev.2005.01.002 Pereira, A. G., Cruz, A., Lima, S. Q., & Moita, M. A. (2012). Silence resulting from the cessation of movement signals danger. Current Biology, 22(16), R627–R628. http://doi.org/10.1016/j.cub.2012.06.015 Perez, E. C., Elie, J. E., Boucaud, I. C. A., Crouchet, T., Soulage, C. O., Soula, H. A., …Vignal, C. (2015). Physiological resonance between mates through calls as possible evidence of empathic processes in songbirds. Hormones and Behavior,75, 130–141. http://doi.org/10. 1016/j.yhbeh.2015.09.002 Pérez-Manrique, A., & Gomila, A. (2018). The comparative study of empathy: sympathetic concern and empathic perspective-taking in nonhuman animals. Biological Reviews,93(1), 248–269. http://doi.org/10.1111/brv.12342 Pisansky, M. T., Hanson, L. R., Gottesman, I. I., & Gewirtz, J. C. (2017). Oxytocin enhances observational fear in mice. Nature Communications,8(1), 1–11. http://doi.org/10.1038/s41467-017-02279-5 Pisansky, M. T., Young, A. E., O'Connor, M. B., Gottesman, I. I., Bagchi, A., & Gewirtz, J. C. (2017). Mice lacking the chromodomain helicase DNA-binding 5 chromatin remodeler display autism-like characteristics. Translational Psychiatry,7(6), e1152. http://doi.org/10.1038/tp. 2017.111 24 of 26 PÉREZ-MANRIQUE AND GOMILA Plotnik, J. M., & de Waal, F. B. M. (2014). Asian elephants ( Elephas maximus ) reassure others in distress. PeerJ,2, e278. http://doi.org/10. 7717/peerj.278 Preston, S. D., & de Waal, F. B. M. (2002). Empathy: Its ultimate and proximate bases. The Behavioral and Brain Sciences,25(1), 1–20. http:// doi.org/10.1017/S0140525X02000018 Proops, L., Grounds, K., Smith, A. V., & McComb, K. (2018). Animals remember previous facial expressions that specific humans have exhibited. Current Biology,28(9), 1428–1432.e4. http://doi.org/10.1016/j.cub.2018.03.035 Quervel-Chaumette, M., Faerber, V., Farag o, T., Marshall-Pescini, S., & Range, F. (2016). Investigating empathy-like responding to conspecifics' distress in pet dogs. PLoS One,11(4), e0152920. http://doi.org/10.1371/journal.pone.0152920 Ranaweerage, E., Ranjeewa, A. D. G., & Sugimoto, K. (2015). Tourism-induced disturbance of wildlife in protected areas: A case study of free ranging elephants in Sri Lanka. Global Ecology and Conservation,4, 625–631. http://doi.org/10.1016/j.gecco.2015.10.013 Reimert, I., Bolhuis, J. E., Kemp, B., & Rodenburg, T. B. (2013). Indicators of positive and negative emotions and emotional contagion in pigs. Physiology & Behavior,109,42–50. http://doi.org/10.1016/j.physbeh.2012.11.002 Reimert, I., Bolhuis, J. E., Kemp, B., & Rodenburg, T. B. (2015). Emotions on the loose: emotional contagion and the role of oxytocin in pigs. Animal Cognition,18(2), 517–532. http://doi.org/10.1007/s10071-014-0820-6 Reimert, I., Fong, S., Rodenburg, T. B., & Bolhuis, J. E. (2017). Emotional states and emotional contagion in pigs after exposure to a positive and negative treatment. Applied Animal Behaviour Science,193,37–42. http://doi.org/10.1016/j.applanim.2017.03.009 Rice, G. E. J. (1964). Aiding behavior vs. fear in the albino rat. The Psychological Record,14(2), 165–170. Rogers-Carter, M. M., Djerdjaj, A., Culp, A. R., Elbaz, J. A., & Christianson, J. P. (2018). Familiarity modulates social approach toward stressed conspecifics in female rats. PLoS One,13(10), e0200971. http://doi.org/10.1371/journal.pone.0200971 Saito, Y., Yuki, S., Seki, Y., Kagawa, H., & Okanoya, K. (2016). Cognitive bias in rats evoked by ultrasonic vocalizations suggests emotional contagion. Behavioural Processes,132,5–11. http://doi.org/10.1016/j.beproc.2016.08.005 Sanders, J., Mayford, M., & Jeste, D. (2013). Empathic fear responses in mice are triggered by recognition of a shared experience. PLoS One,8 (9), e74609. http://doi.org/10.1371/journal.pone.0074609 Sanford, E. M. (2017). Timmy's in the well:Empathy and prosocial helping in dogs. Retrieved from http://digitalcommons.macalester.edu/ psychology_honors Schulte, B. A. (2000). Social structure and helping behavior in captive elephants. Zoo Biology,19(5), 447–459.https://doi.org/10.1002/10982361(2000)19:5<447::AID-ZOO12>3.0.CO;2-# Schwing, R., Nelson, X. J., Wein, A., Parsons, S., & Huber, L. (2017). Positive emotional contagion in a New Zealand parrot. Current Biology, 27(6), R213–R214. http://doi.org/10.1016/j.cub.2017.02.020 Shamay-Tsoory, S. G. (2011). The neural bases for empathy. The Neuroscientist: A Review. Journal Bringing Neurobiology, Neurology and Psychiatry,17(1), 18–24. http://doi.org/10.1177/1073858410379268 Sharma, N., Pokharel, S. S., Kohshima, S., & Sukumar, R. (2020). Behavioural responses of free-ranging Asian elephants (Elephas maximus) towards dying and dead conspecifics. Primates,61(1), 129–138. http://doi.org/10.1007/s10329-019-00739-8 Sial, O. K., Warren, B. L., Alcantara, L. F., Parise, E. M., & Bolaños-Guzm an, C. A. (2016). Vicarious social defeat stress: Bridging the gap between physical and emotional stress. Journal of Neuroscience Methods,258,94–103. http://doi.org/10.1016/j.jneumeth.2015.10.012 Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science,303(5661), 1157–1162. http://doi.org/10.1126/science.1093535 Sivaselvachandran, S., Acland, E. L., Abdallah, S., & Martin, L. J. (2016). Behavioral and mechanistic insight into rodent empathy. Neuroscience and Biobehavioral Reviews,91, 130–137. http://doi.org/10.1016/j.neubiorev.2016.06.007 Sümegi, Z., Ol ah, K., & Top al, J. (2014). Emotional contagion in dogs as measured by change in cognitive task performance. Applied Animal Behaviour Science,160, 106–115. http://doi.org/10.1016/j.applanim.2014.09.001 Trösch, M., Cuzol, F., Parias, C., Calandreau, L., Nowak, R., & Lansade, L. (2019). Horses categorize human emotions cross-modally based on facial expression and non-verbal vocalizations. Animals,9(11), 862. http://doi.org/10.3390/ani9110862 Trösch, M., Pellon, S., Cuzol, F., Parias, C., Nowak, R., Calandreau, L., & Lansade, L. (2020). Horses feel emotions when they watch positive and negative horse–human interactions in a video and transpose what they saw to real life. Animal Cognition,23(4), 643–653. http://doi. org/10.1007/s10071-020-01369-0 Twining, R. C., Vantrease, J. E., Love, S., Padival, M., & Rosenkranz, J. A. (2017). An intra-amygdala circuit specifically regulates social fear learning. Nature Neuroscience,20(3), 459–469. http://doi.org/10.1038/nn.4481 Uchino, B. N., Cacioppo, J. T., & Kiecolt-Glaser, J. K. (1996). The relationship between social support and physiological processes: A review with emphasis on underlying mechanisms and implications for health. Psychological Bulletin,119(3), 488–531. http://doi.org/10.1037/ 0033-2909.119.3.488 Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Takahashi, Y., …Ishihara, T. (2020). Conformity-like behaviour in mice observing the freezing of other mice: A model of empathy. BMC Neuroscience,21(1), 19. http://doi.org/10.1186/s12868-020-00566-4 Van Bourg, J., Patterson, J. E., & Wynne, C. D. L. (2020). Pet dogs (Canis lupus familiaris) release their trapped and distressed owners: Individual variation and evidence of emotional contagion. PLoS One,15(4), e0231742. http://doi.org/10.1371/journal.pone.0231742 Warren, B. L., Sial, O. K., Alcantara, L. F., Greenwood, M. A., Brewer, J. S., Rozofsky, J. P., …Bolaños-Guzm an, C. A. (2014). Altered gene expression and spine density in nucleus accumbens of adolescent and adult male mice exposed to emotional and physical stress. Developmental Neuroscience,36(3–4), 250–260. http://doi.org/10.1159/000362875 PÉREZ-MANRIQUE AND GOMILA 25 of 26