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30 avril 20012
 
Animal Cognition
2012;15(4):721-724
Auditory contagious yawning in domestic dogs
(Canis familiaris):
first evidence for social modulation
 
Silva K, Bessa J, de Sousa L.
 
Departamento de Ciências do Comportamento, Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Portugal

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Abstract
 
Dogs' capacity to 'catch' human yawns has recently attracted the attention of researchers in the field of animal cognition. Following recent studies suggesting that contagion yawning in humans, and some other primates, is empathy-related, some authors have considered the possibility that the same mechanism may underlie contagious yawning in dogs. To date, however, no positive evidence has been found, and more parsimonious hypotheses have been put forward. The present study explored the 'contagion-only' hypothesis by testing whether the mere sound of a human yawn can be sufficient to elicit yawning in dogs, in a way that is unaffected by social-emotional factors. Unexpectedly, results showed an interesting interplay between contagion and social effects. Not only were dogs found to catch human yawns, but they were also found to yawn more at familiar than unfamiliar yawns. Although not allowing for conclusive inferences about the mechanisms underlying contagious yawning in dogs, this study provides first data that renders plausible empathy-based, emotionally connected, contagious yawning in these animals.

-Harr AL, Gilbert VR Do dogs show contagious yawning ? Anim Cogn. 2009;12(6):833-837
-Joly-Mascheroni RM, Senju A, Sheperd AJ Dogs catch human yawns Biology letters Animal Behaviour 2008;4(5):446-448
-Lindsay SR Coping with fear and stress: licking and yawning. Handbook of applied dog behavior and training 2000 
-Madsen EA, Persson T. Contagious yawning in domestic dog puppies (Canis lupus familiaris): the effect of ontogeny and emotional closeness on low-level imitation in dogs. Anim Cogn. 2012
-O'Hara SJ, Reeve AV A test of the yawning contagion and emotional connectedness hypothesis in dogs, Canis familiaris. Animal Behaviour 2011;81:335-340
-Perkins JR Teaching Dogs to Yawn, Sneeze, and Implications for Preparedness Theory and Observational Learning. In: Kusonose, Ryo and Sato, Shusuke 39th Congress of the International Society for Applied Ethology, Kanagawa, Japan. 20-24 August, 2005
-Silva K, Bessa J, de Sousa L. Familiarity-connected or stress-biased contagious yawning in domestic dogs (canis familiaris)? some additional data . Anim Cogn. 2013

 
Introduction
 
In recent years, a renewed interest in the study of contagious yawning has been growing among researchers from various Welds of investigation (see Campbell and de Waal 2010), mostly because of a theoretical link with empathy that has been supported empirically. Platek et al. (2003) showed that humans who performed better at self-recognition and theory-of-mind, two abilities that contribute to complex empathy, performed more contagious yawning. More recently, Palagi et al. (2009) found that yawn contagion in gelada baboons is best predicted by emotional closeness to the yawner&emdash;which is consistent with the observation that empathic tendencies are strongest or most likely to arise, as a function of familiarity (Preston and de Waal 2002; de Waal 2008)&emdash;and Campbell and de Waal (2011) demonstrated an ingroup&endash;outgroup bias in contagious yawning in chimpanzees.
 
Apart from primate species [(humans (Provine 1986, 1989; Anderson and Meno 2003; Senju et al. 2007), chimpanzees (Anderson et al. 2004), stump-tail macaques (Paukner and Anderson 2006), and gelada baboons (Palagi et al. 2009)], contagious yawning has, to date, only been demonstrated in dogs. In 2008, Joly-Mascheroni et al. published a study in which twenty-one out of twenty-nine dogs yawned after seeing a human experimenter acting full yawning movements with vocalizations while none yawned after seeing that same experimenter displaying non-yawning mouth opening actions without vocalizations. Even though, in more recent studies, Harr et al. (2009), and also O'Hara and Reeve (2010), found very limited evidence for contagious yawning in dogs, it has been recognized that at least some individuals do yawn contagiously at humans. Interestingly, a Wrst attempt to test the empathy-based, emotionally connected, contagious yawning in dogs found no evidence in support of the prediction that dogs should be more likely to yawn contagiously at familiar than unfamiliar humans (see O'Hara and Reeve 2010). Instead, it was suggested that if dogs 'catch' human yawns, then contagion might rely on a less cognitively stringent mechanism than empathy, such as some behavioral Wxed action pattern that is hard-wired and simply needs a releasing stimulus (Yoon and Tennie 2010). The present study aimed at further exploring this so-called 'contagion-only' hypothesis by testing whether an isolated presentation of the sound of a human yawn may be suYcient to induce yawning in domestic dogs, in an 'encapsulated way that is unmodulated by social contextual factors' [as proposed by Yoon and Tennie (2010)]. Interestingly, results were obtained that add more conXicting data to the debate on the possible mechanism underlying the phenomenon of dogs yawning contagiously at humans.
 
Discussion
 
Besides showing that the mere sound of a human yawn can elicit yawning in dogs, obtained results also highlight the eVect of a social variable (familiarity/unfamiliarity) on the level of contagion, with dogs yawning more at familiar yawns than at unfamiliar ones. Interestingly, obtained data on attention seems to rule out the possibility that attention diVerences per se may have accounted for the observed pattern of yawning responses. It could have been that the voice of the owners attracted more attention orienting and/or engagement, which prompted dogs to process familiar yawns more deeply or eVectively. Results, however, show that dogs seemed to pay similar attention to both the familiar and the unfamiliar yawn stimuli [for a similar observation in chimpanzees, see Campbell and de Waal (2011)].
 
What does the observed social bias suggest about the mechanism underlying the phenomenon of dogs yawning contagiously at humans? Social modulation of contagious yawning, as observed in primate species [gelada baboons (Palagi et al. 2009) and chimpanzees (Campbell and de Waal (2011)], has been interpreted as supporting the suggesting that catching another's yawn may be an empathic response. The idea that dogs, as a domestic species living in close contact with humans, may be capable of some level of empathy toward people is not new. According to Joly-Mascheroni et al. (2008), it is conceivable that these animals have developed the capacity to represent humans' actions and to modulate their own behavioral and autonomic responses accordingly, and that this underlies contagious yawning [see also Topál et al. (2009) and Silva and Sousa (2011) for an extensive theoretical discussion on dogs' potential to empathize with humans].
 
If empathy is the mechanism underlying contagious yawning also in dogs, then, how can we explain the conXicting results presented by O'Hara and Reeve (2010), which showed no evidence for empathy-based, emotionally connected yawning contagion in dogs? According to Campbell et al. (2009), the Wrst challenge in discussing results across studies on contagious yawning relates to the methodological details that diVer between studies and to the fact that these details have not been studied for their eVect on contagious yawning. To test for social modulation of contagious yawning, O'Hara and Reeve (2010) exposed dogs to familiar and unfamiliar yawns, presented by a live model or in an LCD screen, and compared the number of elicited yawns between conditions that diVered only in familiarity/ unfamiliarity. It is important to note, as it contrasts with the procedure follow in the present study, that, during experimental trials, dogs tested by these authors were encouraged to focus on these visual stimuli, meaning that there was some human&endash;dog interaction that may have diverted the animals' attention.
 
But what if there is no unitary underlying releasing mechanism across all species capable of yawning contagiously and the phenomenon of dogs yawning contagiously at humans is indeed not empathy-related [as suggested by the results pointed out in O'Hara and Reeve's study (2010)]? It is known that dogs can actively generate an internal representation of the owner's face when they hear the owner's voice (Adachi et al. 2007). Therefore, if one considers that it may be the perceptual image of yawn that triggers yawning (see Sarnecki 2008), then the explanation for the social bias observed here could be diVerences in the capacity to form mental representations from familiar and unfamiliar auditory input. That is, the perceptual image generated from hearing unfamiliar yawns would then be more obscure and less deWned than that generated from hearing familiar stimuli, thus eliciting less yawning.
 
Clearly, there is a need for future research to focus on the key variables in the presentation of yawns, as this will facilitate comparisons across studies (see Campbell and de Waal 2010) and will allow Wrm conclusions to be drawn as to whether or not contagious yawning in dogs is empathyrelated. If it emerges that it is, then giving the growing range of roles being played by dogs in human society (as service and therapy dogs, for example), it could turn out a useful complementary tool for selecting the most appropriate dogs (in terms of empathic processing) for speciWc tasks. Finally, it would also be important that future studies explore the potential eVects of a vast range of individual traits (from basic life history to temperament and degree of attachment to humans) on dogs' susceptibility to contagion. Following Sarnecki's view (2004), a theory of yawning contagion should explain not merely why human yawns are contagious to dogs, but also why, for some individuals, they are not.