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Applied Animal Behaviour Science 138 (2012) 170– 181

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Applied Animal Behaviour Science

journa l h o me pag e: www.elsev ier .com/ locate /applan im

Social dimension of emotions and its implication for animal welfare

Marek Spinka ∗

Department of Ethology, Institute of Animal Science, Prátelství 815, 104 00 Prague – Uhríneves, Czech Republic

a r t i c l e i n f o

Article history:Available online 2 March 2012

Keywords:EmotionsAnimal welfareSynchronizationCommunicationAffiliative bonds

a b s t r a c t

Animal emotions are central to the concept of animal welfare. So far, emotions have beeninvestigated in animal welfare science as within-individual phenomena, i.e. coordinatingmechanisms that guide the animal to take appropriate action. However, emotions includean important social dimension. The social side of emotions is being intensely investigatedin humans, but surprisingly little quantitative data exist for animals. Transfers of emo-tions among humans, sometimes labelled as different types of empathy, take differentforms, varying in their cognitive complexity, in the match between the observed and theinduced emotion, and in their time-scale. Sharing of emotions in humans is closely linkedto behavioural resonance, i.e. to strong involuntary propensity to automatically synchro-nize with and imitate behavioural actions of other individuals, and this resonance resultsin a shift towards positive emotions and closer affiliation. Not all forms of empathy-typeinteractions may exist in animals, but there is ample evidence that animals often do trans-fer emotions among themselves, either through inadvertent cues or through specificallyevolved signals. One simple and widespread form of emotional transfer among animals isdiscussed in more detail, namely, the process called emotional contagion that causes ani-mals to shift, upon perceiving animals in an emotional state, their own affective state in thesame direction. Because this process can multiply both negative and positive emotions inanimal groups, it can be of importance for welfare in domestic and captive animals. Othertypes of empathy-like phenomena, such as strengthening of affiliative bonds through emo-tional and behavioural entrainment may also influence welfare of social animals. Payingattention to the social dimension of animal emotions will promote our understanding ofanimal welfare and may open new ways to affect it positively, but much empirical researchinto the specific forms of social animal emotionality is needed before these prospects willbe turned into practicable knowledge.

© 2012 Elsevier B.V. All rights reserved.

1. The feeling side of emotions is central to animalwelfare

Emotions are multifaceted phenomena with neuronal,physiological, behavioural, cognitive and subjective (affec-tive) aspects (Desiré et al., 2002). Emotions coordinatethe bodily and psychological workings of the individualtowards the specific task that needs to be performed withhighest priority (Spoor and Kelly, 2004). Some prominent

∗ Tel.: +420 267 009 596.E-mail address: spinka.marek@vuzv.cz

scientists (LeDoux, 1998) maintain that emotions are pri-marily brain states and bodily responses and consider theconscious feelings to be just “frills on the emotional cake”.Nevertheless, in this article, we will assume that affectiveexperience is by definition a constituent part of any emo-tion. Specifically, we assume that an emotion always hasa valence for the animal, i.e. it feels good or bad, pleas-ant or unpleasant, and therefore enhances or compromisesthe animal’s welfare. We base this assumption on the factthat for many people, animal welfare concerns stem mainlyfrom recognition that animals are sentient beings able toexperience emotions such as fear, pain, frustration, joy, andcontentment. Animal emotions also form the core of many

0168-1591/$ – see front matter © 2012 Elsevier B.V. All rights reserved.doi:10.1016/j.applanim.2012.02.005

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definitions of animal welfare that circulate in the scien-tific community (Dawkins, 1993; Swanson, 1995; Duncan,1996; Fraser and Duncan, 1998; Mendl and Paul, 2004;Yeates and Main, 2008).

While the affective aspect of emotions (i.e. the sentientfeeling of being afraid, sad, happy, enraged, surprised, con-tent, frustrated, etc.) is so crucial for animal welfare, it isalso the most elusive for science (Desiré et al., 2002; Paulet al., 2005) and therefore science was long hesitant toengage in it (Fraser, 2009). Nevertheless, with the adventof affective neuroscience (Panksepp, 1998), biologists arecoming to a consensus that many non-human animals(henceforth labelled simply as “animals”) and almost cer-tainly all mammals experience emotions in principallythe same way we humans do. The affective, sentient sideof animal emotional states cannot be measured but ani-mal welfare science is striving hard to assess it from theother, observable or recordable aspects of animal emotions(Mendl et al., 2010). Behavioural, neural and physiologi-cal measures, such as appetitive and avoidance behaviours,opioid and dopaminergic neurotransmission, glucocorti-coid levels or heart rate dynamics have been used asindicators of positive and negative affective states. Morerecently, the link between affective states and recordablecognitive functioning, such as “optimistic” versus “pes-simistic” appraisal of ambiguous stimuli by animals inpositive or negative mood has been examined as anotherwindow into the feeling side of animal emotions (Paul et al.,2005).

The current intense research of the relationshipbetween the affective and other aspects of animal emo-tions has brought fascinating results and is currently at theforefront of animal welfare science. However, this focuson what is happening “within” the animal risks neglect-ing that emotions have their important social aspect. Theexpression “social aspect(s) of emotion(s)” denotes the factthat when one animal is in a certain emotional state, thiscan be perceived by other individuals (primarily of thesame species) and their emotional state can change in reac-tion to this perception. Research of the social dimension ofemotions has a strong record in human psychology duringthe last two decades. For instance, Reddy and Trevarthen(2004) stress that “emotions do not exist to be locked awayinside an individual” and even state that “the nature andfunction of emotions are to stir sympathetic responses inothers”. In contrast, the social aspect of emotions has beenrarely addressed in non-human animal studies, where themain focus was on how emotions work within the animaland how they prepare it for its individual action. Humanpsychology research could provide a vital inspiration forthe question of social animal emotions. Therefore I will firstgive an excursion to the human research before turning tothe much sparser literature on social emotions in animals.

2. The social dimension of emotions in humanresearch

2.1. The variety of emotional transfers among humans

In human psychology literature, the terms empathy,sympathy, emotional contagion, affective resonance,

vicarious emotion, emotional transfer, cognitive empathyand emotional empathy, among others, have been usedto describe the situation or process when one person isemotionally moved by perceiving the emotional state ofanother person (Preston and de Waal, 2002; Batson, 2009).These terms cover a variety of phenomena that we label,for the purpose of this article, with the umbrella term“emotional transfer”. Emotional transfer is not identicalwith behavioural transfer because often non-emotionalprocesses underlie the transfer of behaviour betweenindividuals, e.g., when a motor pattern is copied (Hannaand Meltzoff, 1993). We discuss the relationship betweenbehavioural mimicry and emotional transfer in the nextsection of this paper.

Human emotional transfers can be, for the purpose ofthis article, organized along three axes: the level of com-plexity of its cognitive aspect, the fact whether the sameor a different emotion is incited in the reacting individual,and the time scale in which the transfer is operating.

Firstly, evidence from cognitive and behavioural neuro-biology, developmental psychology and social psychologyshows that human empathy is composed of both affectiveand cognitive processes; that is, the feeling aspect of empa-thy is always supported by a mental ability to acquire andevaluate information about the state of the other humanperson (Decety, 2011; Shamay-Tsoory, 2011). The cognitiveaspects may be of varying degrees of complexity. Humanchildren gradually acquire several levels of “empathy” dur-ing the first four years of age (Rochat, 2002; Koski andSterck, 2010). Already at birth, babies are capable of auto-matic emotional contagion (e.g., being distressed whenhearing other babies’ distress calls, Geangu et al., 2010); attwo months, they actively reciprocate emotions (e.g., socialsmiling) in a dialogical manner (Trevarthen and Aitken,2001; Reddy and Trevarthen, 2004); and at nine months ofage, dyads of children are engaging in “shared intentional-ity” (Tomasello and Carpenter, 2007), i.e. they perceive thatbetween them, there is a shared emotional stance towardsobjects and events. Between 14 and 48 months, childrendevelop “projective empathy that encompasses the abil-ity to distinguish between self and others, self-consciousemotions such as embarrassment, and ability to theorizeabout the others’ mind (Rochat, 2002). During later life, thecognitive aspects of empathy develop further with experi-ence and knowledge acquisition while the affective aspectcritical for the immediate assessment of significance ofstimuli retains its importance (Kleiman, 1977). In adulthumans, all the different levels of empathy remain present,starting from the simple emotional contagion in families(Larson and Almeida, 1999) and in teams (Barsade, 2002),through automatically occurring dialogic exchange of emo-tions, both positive and negative, between family members(Larson and Almeida, 1999; ten Brummelhuis et al., 2010)and between strangers (Hess and Bourgeois, 2010) up toempathetic responses based on inference and represen-tation of mental states of self and others (Lamm et al.,2011).

The second important classification of empathy-typephenomena distinguishes whether the affective responseis isomorphic, i.e. “with” the object (e.g., response is withdistress to distress or with joy to joy), or anisomorphic, i.e.

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“to” the object (instrumental responses as fear or anxietyto anger or consolation to distress, Larson and Gillman,1999; Preston and de Waal, 2002). Van Kleef (2009) andVan Kleef et al. (2010) noted in their analysis of interper-sonal human emotions that in cooperative situations, orwhen time pressure was high, the “with” response, i.e.contagion of the same emotion, is usually prevalent. Inmore competitive settings, or under low time pressure,people are less inclined to resonate immediately with thesame emotion and rather utilize the other’s emotional cuesand signals to strategically infer about the other’s stateand then possibly engage in a different emotion or in noemotional reaction. When people expect the situation to bedownright competitive, their reaction to the other person’semotion may be even counterempathetic, e.g., they mayreact with pleasure to displays of distress (Lanzetta andEnglis, 1989), or with displeasure to smiling (Weyers et al.,2009). Obviously, these two types of emotion-to-emotionresponses can have different social dynamics. Whereasthe contagion with same-type emotion can spread ingroups through chain- or avalanche-type reactions, thiscannot happen if the emotion incited in the receiver(s) isqualitatively different from the emotion of the sender ofthe affective signals (Spoor and Kelly, 2004).

Thirdly, emotional transfer in humans occurs at timescales ranging from tenths of seconds to years. At thefastest, emotional grimaces are mirrored by on-lookinghumans with latencies as short as 0.4 s (Dimberg andThunberg, 1998), contagious crying by human infants haslatencies in tens of seconds (Geangu et al., 2010), valenceand intensity of emotion of the first speaker ripple acrossnegotiating groups in the time scale of minutes (Barsade,2002), family members transmit their emotions to eachother on a daily basis (Song et al., 2008; Song et al., 2011),spouses mutually influence their happiness from year toyear (Powdthavee, 2009) and persons with whom we havesocial contact “infect” us with their degree of (un)happinessover periods of several years (Hill et al., 2010).

Across all these three dimensions, the emotional trans-fers are considered practically extremely important bysocial psychologists as they crucially affect vital social pro-cesses like social fear learning (Olsson and Phelps, 2007),negotiation (Van Kleef and De Dreu, 2010; Thompson et al.,2010), cooperation (Barsade, 2002), family life (Song et al.,2011) and ethnic or religious strife (Hatfield and Rapson,2004).

In the “animal” part of this paper (Sections 3 and 4), Ishall mainly focus on cognitively undemanding, isomor-phic and short-term emotional transfers as this is thesubclass of social transfers that is best investigated in ani-mals.

2.2. Human motor mimicry, affective resonance andsocial behaviour

Psychologists agree that emotional transfer betweenhumans, especially in its common, everyday form, is nota purely observational and mental process. Rather, it hasa surprisingly strong bodily dimension since the affectiveresonance is closely linked to somatic or motoric reso-nance.

When people interact with each other, they tend toautomatically and continuously mimic and synchronizetheir facial expression, body postures and movements,vocal expression and instrumental behaviour with that ofothers (McDougall, 1908; Vallacher et al., 2005; Carter et al.,2009; Heyes, 2011). People’s facial expressions tend toreflect the very minute changes in the affective expressionsof those they observe. This facial mimicry is instanta-neous and can be either overt or so subtle that it is hardto catch by observation but can be reliably measured byelectromyography (EMG) (Lundqvist and Dimberg, 1995).People have also been found to mimic each other’s speechrate, utterance duration, latencies of response and funda-mental frequencies (Cappella and Planalp, 1981; Gregoryet al., 1997) as well as microsynchronize their posturesand movements (LaFrance and Ickes, 1981; Lakens andStel, 2011). The mimicry normally occurs without us beingaware of it (Chartrand and Bargh, 1999).

There is considerable evidence that this facial, vocal,postural and movement mimicry has a direct feedback onthe people’s moment-to-moment emotional experience.Researchers have utilized various experimental strategiesto trick people to adopt or unconsciously mimic facialemotional expressions (Wiswede et al., 2009; Dimbergand Soderkvist, 2011), affectively loaded sound patterns(Hatfield et al., 1995) or emotionally coined postures andmovements (Duclos et al., 1989; Price and Harmon-Jones,2010) and consistently found that the emotional expe-riences of the subjects were affected in the predicteddirection. This influence seems to be quite specific: peo-ple are more likely to feel, not just any emotion of thesame valence (e.g., any negative emotion), but indeed theemotion of the same quality, e.g., sad but not angry feel-ing after making a sad facial expression (Adelmann andZajonc, 1989). Conversely, when the muscles responsiblefor a distinct facial expression are temporarily paralysed,the processing of this specific emotion is hindered (Havaset al., 2010).

Given this evidence, there is little doubt that trans-fers of emotions between people are partly mediated bybehavioural mimicry and synchronization. How importantthis mechanism is for the total amount and variety of affec-tive resonance between people is not yet clear (Bastiaansenet al., 2009).

The somatic resonance not only mediates humanaffective resonance, but it also makes individuals morepositively attuned towards each other and generatescooperation (Van Baaren et al., 2009). Thus, people likemimickers more than non-mimickers, and this was provenboth for real human partners (Chartrand and Bargh, 1999)and for digital avatars that just indiscriminately mimickeda participant’s head movements at a 4-s delay (Bailensonand Yee, 2005). When people are being imitated, they aremore likely to help others and to give more generously(Van Baaren et al., 2004). Being imitated compared to notbeing imitated activates brain areas associated with emo-tion and reward processing (Kuhn et al., 2010). People whohave performed rhythmic synchronous movements showmore compassionate and altruistic behaviour (Valdesoloand Desteno, 2011). The relationship between mimicry andsocial attitudes is bidirectional because the magnitude of

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the mimicry/automatic imitation is increased by pro-socialas compared with anti-social priming (Connor et al., 2006).Once more, in all these studies, the participants did notnotice how mimicking by others affected their stance andjudgement. Because of all these powerful effects, the ten-dency to automatically imitate the behaviour of others (the“chameleon effect”) has been proclaimed a “social glue” bysome social psychologists (Lakin et al., 2003).

3. Transfer of emotions in animals

3.1. Historical time lag in the research of animal socialemotions

What we know scientifically about emotions in (non-human) animals is much less extensive, less deep, andless certain than what science has revealed about humanemotions. There are several reasons for this discrepancy.First, the research on emotions in humans can build uponthe communication of “insider” information: people havethe introspective power of being aware of their emotions,and there is the language communication that enablesdirect questions and answers about emotional experienceof others. We lack these two crucial channels of referenceswhen we investigate animal emotions and have to resort toindirectly assessing the subjective feeling component forphysiological, behavioural and cognitive changes (Desiréet al., 2002; Paul et al., 2005). Second, “humans” are onespecies, so results from different studies can directly com-plement each other. Research on “animals” is spread acrossmany species that may share some features of their emo-tionality but differ in many other aspects which makesgeneral conclusions more difficult. Third, the researcheffort on emotions in animals has been, and will certainlycontinue to be, only a tiny fraction of the investigations intohuman emotionality.

The difference is currently even more profound in theknowledge about the social aspect of emotions. In humanpsychology, research on emotions was also initially con-centrated on a within-person view but for the last twodecades, research on reciprocal interpersonal influence ofemotions has flourished (Hareli and Rafaeli, 2008). Theresearch on animal emotions has a long tradition (Darwin,1872; Panksepp, 1998) and has been revived during thelast 20 years through the desire of animal welfare scienceto understand the nature of sentient emotions (Dawkins,1990; Desiré et al., 2002). At the same time, social cogni-tive processes, such as social learning, also have a history ofmore than hundred years of research in animals (see Heyes,1994; Galef and Giraldeau, 2001 for reviews). Curiously, itis only very recently that these two approaches have beencombined into consistent research programmes address-ing the social side of animal emotions (Panksepp andLahvis, 2011), although the notion has been around sinceMcDougall (1908). The only exception to this omission isthe tradition of social fear research driven by the search foranimal models of human psychopathology. Research pro-grammes of animal empathy-type phenomena are now infull swing and encounter methodological problems that aresimilar to those previously confronted by human empathyresearch (Panksepp and Lahvis, 2011).

In the next two sections, I will review: (i) argumentsfor evolutionary common roots and continuity of socialaffective processes and (ii) available evidence showing thatanimals signal their emotions, that these emotional sig-nals are perceived by other individuals and affect theirbehaviour and that emotional contagion built on these twocapabilities exists in many species.

3.2. Evolutionary origins and continuity of socialaffective processes

In spite of current paucity of hard data, there are manyreasons to assume an evolutionary continuity of socialemotionality. The pronounced human inclination to shareand communicate emotions must have evolved for goodadaptive reasons. Spoor and Kelly (2004) hypothesize thataffect in groups serves several mutually supporting func-tions. First, group living animals need to coordinate theiractions in time and space, otherwise the group will disin-tegrate (Krause and Ruxton, 2002). Since emotions primethe individuals to act in certain ways, efficient coordi-nation is facilitated by similarity in affective states asdocumented by Vallacher et al. (2005) in a formal dynamicmodel of synchronization of both overt behaviour andinternal states in social relationships. Transfer of emotionsalso alerts the group to positive or negative aspects ofthe environment that have been noted by one or moregroup members. Finally, sharing emotions in the groupfosters inter-individual bonds and group loyalty (Lakinet al., 2003). All these adaptive functions would apply toany cohesive group of animals, not just human groups.Therefore, it appears that once emotions arose as adap-tations that motivate individuals to respond quickly andappropriately to environmental changes, the combinedpotential benefits of easier group coordination, more effi-cient information transfer and stronger interindividualbonding would press group living species to acquire shar-ing and synchronization of similar emotional states amonggroup members. On the other hand, in the more competi-tive aspects of group living, the evolution of anisomorphicemotional induction is to be expected, such as fear reac-tions to rage or contentment to fearful submission.

Besides the plausibility of common selection pressureson any group-living animals endowed with emotions,there are indications that empathy-type phenomena, atleast in mammals, employ a common basic psychologicaland neuronal substrate. Many students of emotionaltransfer accept that the basic mechanism behind it may bethe “perception-action” (or, more fittingly, the perception-representation-action) link as proposed by Preston and deWaal (2002). The model proposes that when the subjectperceives the object’s emotional state (through the subtleand overt cues and signals, see next section), this automat-ically activates the subject’s representations of the state,and that activation of these representations automaticallyprimes or generates the associated autonomic and somaticresponses. Thus, self-generated and vicariously inducedemotions activate the same neural and bodily actions, andthis gives the subject animal an access to the subjectivestate of the other (de Waal, 2008). Moreover, empa-thetic reactions may have common neuronal substrate

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in different mammalian species. For instance, anteriorcingulate cortex is activated during direct fear acquisitionthrough observing a conspecific in pain in both humansand mice (Jeon et al., 2010). Carter et al. (2009) propose thatthe mammalian nervous system evolved unique neuralcircuits with an ability to signal and to detect vocalizationsreflecting states such as pain, distress and joy, to detect andproduce facial expression and that these circuits becameintegrated with brain stem nuclei and the myelinatedvagus, thus creating a closely knit face–voice–heart con-nection capable of expressing and perceiving emotions.The fact that mammals have extensive maternal care mayhave made it advantageous for mammalian mothers tobe sensitive to their babies’ affective states (Panksepp,1998; Hild et al., 2011) which may have contributed tothe evolution of more general affective resonance abilitiesin mammals. Thus the evolution of emotion transfer mayhave been driven, in addition to the group-based advan-tages, by its role as a proximate mechanism for directedaltruism towards kin, especially progeny (de Waal, 2008).

3.3. Emotional cues, signals and perception in animalemotional transfer

There is no doubt that emotions (inner affective states)are often reflected in outer physical appearance and inbehaviour of animals. For instance, when an animal entersa fear state, it either freezes or flees to avoid the danger,its eyes open widely to see the threat sharply, breath-ing becomes shallower to avoid detection, muscle toneand heart rate increases to prepare for fast action. On theother hand, when the animal is resting in a content mood,the muscle tone relaxes, the eyes close down partiallyand ears flop to reduce the information flow to the brain,and breathing slows down to save energy. These emotion-accompanying physiological and behavioural changes helpthe animal to adjust to the situation individually. Althoughtheir main function is not communicative, other animalscan note these changes as cues indicating the affectivestate. In addition, specific behavioural patterns evolved inmany species whose main function seems to be to conveyinformation about the emotional state. Classical visual sig-nals of fear and rage were described by Darwin (1872) andLorenz (1963) for dogs and by Leyhausen (1979) for catswhile fear pheromones were described later (Fanselow,1985; Arakawa et al., 2011; Bredy and Barad, 2009). Self-directed (“displacement”) behaviour such as preening orself-scratching often reflect the individual’s emotionalstrain, e.g., after an agonistic encounter (Maestripieri et al.,1992; Wascher et al., 2010). In primates, facial expres-sions display emotions (Steiner et al., 2001; Palagi andMancini, 2011), and in our closest relative, the chimpanzee(Pan troglodytes), several facial movements involved inemotion communication system are homologous to thosein humans (Parr et al., 2007). A prominent channel foremotional signals in mammals is their vocal expression(Seyfarth and Cheney, 2003). For instance, laboratory rats(Rattus norvegicus) emit both 50-kHz and 22-kHz ultra-sonic calls in social situations (Brudzynski, 2009). Thesetwo categories of vocalizations have distinct and mostlynon-overlapping acoustic structures. The 50-kHz calls are

emitted almost exclusively in positive situations and aredriven by the ascending dopaminergic system, while the22-kHz calls are induced by the ascending cholinergic sys-tem and occur in negative situations. In pigs, too, screamingcalls are associated with negative situations and can beinduced by acetylcholine injections to amygdala or by cen-trally injected anxiogenic peptides such as corticotropinreleasing hormone (Manteuffel et al., 2004, 2007). Düpjanet al. (2008) demonstrated that pigs exposed to differenttypes of stressors (unexpected pain, expected pain, fearof upcoming pain) emit distress calls that differ in acous-tic qualities. These calls thus not only reflect the generalnegative valence of the emotion, but can also serve asdifferentiated indicators of the specific type of emotion,i.e. pain or fear. Thus in individual species, emotional sig-nals can contain fine-tuned information about very specificmotivational/emotional states. On the other hand, acrossa wide range of mammalian lineages, certain rules of theso-called motivation-structural code seem to be gener-ally upheld for acoustic communication of emotions. Forinstance, high pitched tonal calls are usually produced infear states whereas rage is associated with low pitchedharsh calls (Owings and Morton, 1998).

Experimental evidence has proven not only that ani-mals emit emotional signals but also that their conspecificsdetect these emotions and are affected by them. Boissy et al.(1998) documented that urine from stressed conspecificsinduces fear in heifers in either feeding or exploration sit-uations. Burman et al. (2007) found that rats exposed toplayback of the 22 kHz vocalizations were less likely andslower to emerge from a closed box to open arena andspent less total time in the open arena than rats exposed tothe 50 kHz calls or background noise. The authors ascribethese behavioural differences to a negative emotional stateof increased anxiety induced by the 22 kHz calls. Similarly,Kim et al. (2010) observed increased freezing in rats pairedwith fear-conditioned conspecifics in reaction to their22 kHz calls and Chen et al. (2009) obtained similar resultsin mice. Socially living primates, such as rhesus monkeys(Macaca mulatta), distinguish facial expression of emotionsthrough a combination of features such as mouth openingand lip retraction (Parr and Heintz, 2009). Physiologically,too, animals react to emotionally loaded visual or acous-tic stimuli from conspecifics, for instance, through changesin heart rate (Marchant-Forde et al., 2002; Wascher et al.,2008) or through changes in local brain temperature(Parr and Hopkins, 2000). The motivational-structural codedescribed above has been explained through communica-tive functions of the calls. Owren and Rendall (2001)hypothesized that certain basic types of call (such assqueaks, shrieks, and screams) have direct and highly con-served effects on attention and arousal through engagingsubcortical brain structures like the brainstem, thalamusand limbic system and that is why they are used exten-sively by dependent progeny to increase the probability ofresponse in their mothers (Owren and Rendall, 2001).

On the whole, the published research provides ampleevidence that many mammals combine their ability toemit cues and signals about inner emotional state, andthe ability to be affected by these stimuli into the simplerforms of empathy such as emotional contagion or dialogic

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communication of emotions (Panksepp and Lahvis, 2011).Orangutans (Pongo pygmaeus) use open-mouth facial(OMF) displays during social play. Ross et al. (2008)showed that within playing dyads, orangutans mimickOMFs of their playmates very rapidly (within 1 s) thusrevealing evidence of so called rapid involuntary facialmimicry that has been previously described only in humansand that is thought to be a fundamental building blockof positive emotional contagion and empathy. Newbornrhesus monkeys (Ferrari et al., 2009) and chimpanzees(Bard, 2007) are capable of imitating facial expression ofadult humans. Contagious yawning, which seems to bean empathy-related mimicking response in humans, hasbeen so far observed in chimpanzees (Campbell and deWaal, 2011), stump-tail macaques (Macaca arctoides) andgelada baboons (Theropithecus gelada) (Palagi et al., 2009)and in domestic dogs (Joly-Mascheroni et al., 2008)—butsee O’Hara and Reeve (2011). Adult female geladas evenmatch precisely the type of yawning they have seen intheir companion (Palagi et al., 2009), thus suggestinganother building block for full-blown empathy, namely amirroring mechanism that activates shared representationof the seen and the performed emotional signal.

In summary, the available evidence indicates that emo-tional transfers, at least those of simple kind, may becommon to all mammals, and possibly to other group-living species.

4. The social dimension of emotions and animalwelfare

Although the research on social dimension of emotionsis still in its beginnings, there are many indications thattransfers of emotions play an important role in shapingthe behaviour and the inner experience of socially livingmammals, the class of animals that make up the bulk ofdomesticated animal species. What are the welfare impli-cations of this, until recently largely overlooked, fact? Asexplained in the beginning of this article, any emotionalstate is, through its negative or positive valence, rele-vant for welfare of the animal experiencing it. Therefore,a mechanism such as emotional contagion that causes anemotion to jump from one animal to another is of impor-tance for welfare of group housed animals since it amplifiesthe number of individuals affected by the emotion. Sec-ondly, initial evidence is emerging that in non-humananimals, as in humans, emotional and behavioural reso-nance may lead to stronger inter-individual bonds, thusenhancing the resilience of the individuals and perhaps ofthe group, against future challenges and stressors. In thefollowing sections, I will review two major alleys throughwhich the social side of emotions can profoundly affectanimal welfare: firstly, the social spread and amplifica-tion of good or bad feelings in groups of animals andsecondly, the building (or not) of social bonds throughshared emotions and associated behavioural entrainment.These two aspects reflect the presumed evolutionary func-tions of social affect discussed above (Spoor and Kelly,2004).

4.1. Contagion of negative emotions

The spread of negative emotions seems to be a strongerand more ubiquitous phenomenon than the contagion ofpositive emotions (Spoor and Kelly, 2004; Greiveldingeret al., 2011; Panksepp and Lahvis, 2011), probably becauseit is more urgent to react quickly to signs of incomingdanger than to indications of a positive event. The mostextensively investigated case of emotional contagion inanimals is social transmission of fear (Mineka and Cook,1993; Boissy et al., 1998; Masuda and Aou, 2009; Kimet al., 2010). Social spread of fear, and prevention of fearby the presence of companions that do not show fearresponses, is among the very few examples of emotionalcontagion that have been explicitly noted for its animalwelfare significance (Nicol, 1995). Two forms of how fearfulreaction/signalling in one animal can influence fear lev-els in another animal have been distinguished: direct fearcontagion and social fear learning. In direct fear contagion,the behavioural (including olfactory) cues or signals fromthe fearful animal act as unconditional fear stimuli, i.e. the“receiver” animal attains fear directly from the smelling,seeing and/or hearing the fearful behaviour of the “emit-ter” animal. For instance, rhesus monkeys react by fearwhen they watch facial fear expression in a companioneven if they do not see the external stimulus (model snake)that causes the fear in the model monkey (Mineka andCook, 1993). Rats react fearfully to playback of the 22 kHzvocalizations of other rats (Burman et al., 2007). Rats,mice, pigs and cattle behave more fearfully during feed-ing and exploration when exposed to olfactory cues fromstressed conspecifics (Kikusui et al., 2001; Vieuillethomasand Signoret, 1992; Boissy et al., 1998; Bredy and Barad,2009). Social fear learning is a more complicated processwhen the cues/signals from the fearful animal serve asconditioning stimuli. That is, an observer animal learnsto fear another species, an object or a situation throughthe observation of fearful reactions of a conspecific tothe object/situation (Olsson and Phelps, 2007). Social fearlearning has been extensively studied in rodents and pri-mates as a model for human anxiety disorders and phobias(Bruchey et al., 2010; Panksepp and Lahvis, 2011).

Another recently documented social transfer of a neg-ative emotion is social pain modulation. Langford et al.(2006) showed that when mice are exposed to noxiousstimuli in dyads, their pain behaviour (such as writhing inreaction to abdominal pain and licking in reaction to pawpain) were either enhanced or diminished, depending onwhether the “partner in pain” was experiencing a higheror a lower level of pain than the focal individual. More-over, the pain behaviours were synchronized in time in thedyads and observation of the conspecific in pain increasedthe observer’s pain sensitivity to another pain modality,namely radiant heat stimulus, thus indicating that the pairindeed mutually entrains their general pain sensitivity.

Although this research on the spread of negativeemotions in domestic (mostly laboratory) animals wasmotivated by the search for experimental models of humanpsychosocial impairments, the animal welfare implicationsof these findings are obvious—inflicting pain or fear on oneor a few animals may negatively affect also the welfare of

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their group mates. Nevertheless, the effects need not tobe always negative. Both in the social fear transfer and inthe social pain modification studies, evidence exists thata less- or non-fearful animal, or an animal in lesser or nopain, may attenuate the perceived level of fear or pain in itsmates (Davitz and Mason, 1955; Mineka and Cook, 1986;Munksgaard et al., 2001; Langford et al., 2006; Guzmánet al., 2009; Kiyokawa et al., 2009).

4.2. Contagion of positive emotions

Traditionally, most animal welfare research work con-cerned with emotions focused on negatively valencedaffective states such as pain, fear, anxiety, sadness, help-lessness, frustration, anger or boredom and their relation-ship to animal suffering (Dawkins, 1990; Wemelsfelder,1993; Janczak et al., 2003; Greiveldinger et al., 2011).However, during the last decade, intense research hasdeveloped into the animal welfare role of positive emo-tions such as those incited during play, expectation ofpositive events, contentment from achieving a consum-matory behaviour, successful problem solving or positivesocial interactions (e.g., Dudink et al., 2006; Boissy et al.,2007; Yeates and Main, 2008; Manteuffel et al., 2009; Heldand Spinka, 2011; Spinka and Wemelsfelder, 2011). Thesocial aspect of positive emotions in animals has receiveda very limited research attention so far. The only instanceof focused research of socially transferred positive emo-tions is social play. It has been repeatedly noted that playbehaviour is highly contagious (Fagen, 1981; Bekoff, 2001)and quantitative investigations, although still rare, indeeddocument the effects of playfulness of one partner onplay behaviour of the other (Pellis and McKenna, 1992;Varlinskaya et al., 1999). There is both behavioural andneurobiological evidence that play behaviour is rewarding(reviewed by Held and Spinka, 2011) and therefore withplay contagion a pleasurable affect is being transferred. Aswith many other causes of emotional contagion, it has notbeen settled yet whether the behaviour is first transferredthen driving the change in the recipient’s emotional stateor the emotion jumps first and then incites the recipientto play, but this distinction is not critical for the welfarerelevance of the phenomenon. Other possible instances ofshared positive emotions include the case of generalizedreciprocity in rats (Rutte and Taborsky, 2007), where ratsthat had been helped by other rats to an oat treat, would,in turn, help an unfamiliar conspecific to the treat, butwhether a shared positive affect is involved in this phe-nomenon is currently purely speculative. A similar casewould be that of adolescent mice who become ‘pseudosen-sitized’ to the locomotor-activating effect of morphine byobserving other mice that had been treated with the drug(Hodgson et al., 2010).

4.3. Behavioural resonance, affective resonance andsocial bonds in animals

In the transfer of emotions between humans, thereis a positive feedback between behavioural resonanceand affective resonance, on the one hand, and themutual attractiveness, strength of relationships, and

positive mood, on the other. That is, people are moreinclined to share/copy/imitate the behaviour and/ormood of people who are close to them and also ifthey are in a prosocial mood (Leighton et al., 2010)and vice versa, if people’s behaviour and emotions areshared/synchronized/imitated, then this brings theminto a more positive and prosocial mood, thus enhancingthe chance of strengthening inter-personal relationships(Valdesolo and Desteno, 2011). Spoor and Kelly (2004)hypothesize that coordination of mood and activity withina group, and fostering group member bonds, are two mutu-ally reinforcing functions of affective states in groups. Ifsharing of emotion and the accompanying behavioural syn-chrony indeed contribute to positive social relationships ingroups of domestic animals, a considerable welfare benefitwould result because positive social relationships havemany beneficial effects for the animals’ physical and men-tal well-being (Newberry and Swanson, 2001; Hild et al.,2011; Galindo et al., 2011; Sachser et al., 1998; Hennessyet al., 2006; Kikusui et al., 2006; Hennessy et al., 2009).

Currently the evidence for the positive feedback is verylimited in animals, but this is due to paucity of researchrather than due to negative findings. Recently, animals suchas budgerigars (Melopsittacus undulatus) and dogs havebeen shown to possess the tendency to automatically imi-tate seen movements (Mui et al., 2008; Range et al., 2011)which is one of the building blocks of the positive feed-back in humans (Chartrand and Van Baaren, 2009; Heyes,2011). Paukner et al. (2009) demonstrated that capuchinmonkeys (Cebus apella) prefer humans that imitate theirball-manipulating behaviour to those that perform non-matching actions thus proved for the first time thatimitation increases affiliation in a non-human primate.The other arm of the loop, i.e. closer resonance betweencloser affiliates, has support in wild living mammals such asbottlenose dolphins (Tursiops truncatus), Indo-Pacific bot-tlenose dolphins (Tursiops aduncus) and African elephants(Loxodonta africana) (Connor et al., 2006; Perelberg andSchuster, 2008; Sakai et al., 2010; Soltis et al., 2005) as wellas in laboratory rats (Schuster and Perelberg, 2004) anddairy cows (Gygax et al., 2010). The role of shared positiveemotions in this loop has not been documented yet for anyspecies except humans. Nevertheless, some researcherspropose that the positive hedonic aspect of acting in syn-chrony is a bridge that immediately rewards the build-upof closer social links; the links that, in turn, will bring fitnesspay-offs much later in life (Schuster and Perelberg, 2004;Perelberg and Schuster, 2008). Group-housed domesticanimals often synchronize their behaviour spontaneously(Webster and Hurnik, 1994; Spinka et al., 2004; Blanc andTheriez, 1998; Collins and Sumpter, 2007; Sárová et al.,2007; Gibbons et al., 2010). It is plausible to assume thatachieving this synchrony is rewarding when it brings asense of security (Pays et al., 2007; Sirot and Touzalin, 2009)or cohesion during coordinated group movements (Sárováet al., 2007; Ramseyer et al., 2009). This logic is proba-bly behind the notion that synchronicity may be one ofthe most promising indicators of positive welfare for cattle(Napolitano et al., 2009). On the other hand, behaviouralsynchronization need not be always positively motivated;for instance, it is unclear whether the well-known social

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facilitation of feeding (Collins and Sumpter, 2007; Hoppittand Laland, 2008) is not sometimes competitively moti-vated and therefore negatively valenced.

4.4. Variability in emotional transfer

The spread of emotions, either the negative or the pos-itive ones, does not occur automatically between any twoindividuals of the same species in any situation. Accord-ing to various investigations, fear contagion, social fearlearning or social modification of nociception only occur ifsome pre-conditions are met (see Table 1 in Panksepp andLahvis, 2011, for an overview). Several studies found thatthe emotional transfer takes place more strongly, or evenexclusively, when the animal displaying the emotionalbehaviour is familiar to the perceiving animal (Langfordet al., 2006; Palagi et al., 2009; Jeon et al., 2010) althoughmany other studies did not find unfamiliarity to hinderthe effect. In other cases, the animal has to have its ownprevious experience with the aversive situation (e.g., painthrough electric foot shock) to be liable to social emotiontransfer (Bredy and Barad, 2009; Kiyokawa et al., 2009;Knapska et al., 2010; Kim et al., 2010). Within-speciesgenetic variability can also contribute to the variation inemotional transfer as documented by the fact that the moregregarious C57BL/6J mouse strain is vulnerable to sociallyconditioned fear while the less social BALB/cJ strain is not(Chen et al., 2009). The propensity to a specific type ofemotional transfer can also change during ontogeny, e.g.,be present in adolescent but not in adult mice (Hodgsonet al., 2010) and be sex specific, e.g., occur only in females(Langford et al., 2010).

While our knowledge about the short-term, isomorphicand cognitively undemanding transfer of affective states,as reviewed in the current article, is still very poor, infor-mation about animal empathy-type phenomena that areat work over longer periods of time, induce anisomorphicaffective states and/or employ higher levels of cognitionis even more patchy. The experiments on cognitive biasessuggest that animals do experience longer-term affectivestates or “moods” which may serve as cumulative Bayesianproxy indicators of probabilities of reward and punishment(Mendl et al., 2010). For instance, rats seem to be more“depressed” when living in a poor versus in an enrichedcaptive environment (Burman et al., 2008a,b). However,whether these states are socially shared to the same extentas short-term emotions, remains to be established. Theinduction of anisomorphic affective states, e.g., in relationto communication of dominance status in a group, hasbeen quantitatively investigated in humans (Lovaglia andHouser, 1996) but not yet in animals. And cases of socialemotionality that includes higher levels of cognition, suchas distinguishing between self and others and active help-ing based on the perception of conspecific distress (Prestonand de Waal, 2002; de Waal, 2008; Langford et al., 2010;Silva and De Sousa, 2011) are still hotly debated due totheir difficult interpretation and contradictory results (Silket al., 2005; Jensen et al., 2006; Melis et al., 2011). In con-crete cases, these phenomena definitely exist in mammals,such as the long-term depression-like states after the lossof mother, progeny or close companion in apes and dogs

(de Waal, 1996); the induction of fear through the ragebehaviour of a dominant group member; and the helpingbehaviour of mammalian mothers in response to distressbehaviour of their progeny (Hild et al., 2011). The question,once more, is how widespread and how strong are thesephenomena in groups of individual mammalian species.

Great variability, both within and between species,is also to be expected in the positive loop betweenbehavioural and emotional resonance, on the one side,and the strength of social bonds, on the other. In theultra-social species of Homo sapiens, this loop is demon-strably very strong. Most of the main domesticated speciesare also social (i.e. group-living) but the importance ofindividualized bonds definitely differs from species tospecies because of their social organization and life his-tory (Newberry and Swanson, 2001; Hennessy et al., 2009;Raussi et al., 2010; Hild et al., 2011).

Because of the paucity of empirical data, we do not knowhow ubiquitous and how important emotional transfers arefor specific domesticated and captive species. One warn-ing sign against any precocious sweeping generalizationsis the fact that several studies did not confirm the expectedor previously reported transfers of emotions. For instance,Düpjan et al. (2011) specifically investigated the possibilityof acoustic fear transfer in pigs. The pigs were put in iso-lation and exposed to playbacks of either high-pitched pigdistress calls (recorded from unfamiliar and unrelated pigs)or much lower artificial 500 Hz sounds. No behavioural orheart rate indications of increased fear in the pigs hear-ing the distress calls were found. Another example is thereported contagion of yawning by dogs (Joly-Mascheroniet al., 2008) that could not be replicated by later two studies(Harr et al., 2009; O’Hara and Reeve, 2011).

Our uncertainty about the real extent of emotionaltransfer in animals stems also from outstanding method-ological difficulties. The most significant challenge is toconvincingly demonstrate that the resonance that has beenobserved between two or more animals is not “just” abehavioural transfer, i.e. that the transferred behaviourshave emotional valence. The quality of such evidence variesfrom study to study. While most of the animal studies citedin this article did not go beyond behavioural evidence, somebrought in heart rate data (Düpjan et al., 2011) or investi-gated the involvement of different brain centres (Jeon et al.,2010). Optimally, a combination of behavioural, physio-logical, neurobiological and cognitive processing evidenceshould be used in future studies to make the case of emo-tional transfer more persuasive.

These negative findings, the dependence of other casesof emotional transfer on specific conditions, and the sheerlack of empirical data underline the importance of furtherintensive research about specific forms of emotional trans-fer in the main human-held species. For animal welfareresearch, it is not so important what types of emotionaltransfer are principally possible in animals. Rather, inves-tigations should focus on whether, when and how intenselythe concrete negative and positive affective states areindeed socially transferred and modified. Preston and deWaal (2002) stress in their review that for empathy-typephenomena to occur, the observer animal has to attend tothe cues/signals from the object animal and this attention

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could be blocked by factors like unfamiliarity, lack of expe-rience, different dominant position or a stressor that makesan individually based emotion prevalent. The researchtherefore should be shaped by hypotheses derived frompresumed adaptive functions of the emotional transfer, i.e.should start from the question “when does it pay-off for theanimal to attend to the emotional state of the other”?

5. Conclusion

The research on social aspects of animal emotions is stillin its infancy but is quickly revealing that different forms ofemotional transfer are important for group living animals.There are multiple potential animal welfare implications ofthe social emotionality in domestic and captive mammals,and possibly in other vertebrates. The real scope of theseimplications needs to be assessed in the years to come.

Conflict of interest

None.

Acknowledgements

This study was supported by the grant P505/10/1411from the Czech Grant Agency and the grantMZE0002701404 from the Czech Ministry of Agriculture.

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