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Le bâillement : phylogenèse, éthologie, nosogénie
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La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
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2 septembre 2013
 Familiarity-connected or stress-biased contagious yawning in domestic dogs (canis familiaris)? some additional data
 
Silva Karine, Bessa Joana, de Sousa Liliana
 
Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto
Departamento de Ciências do Comportamento
Largo Prof. Abel Salazar, 2
Porto, Portugal
  

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 ABSTRACT
 
The present short note aimed at further exploring data from a recent study showing socially modulated auditory contagious yawning in domestic dogs (Canis familiaris).
Two independent observers further extended the analysis of all video-recordings made in that previous study and coded both the number of yawns performed by the dogs and the frequencies or durations of stress-related behaviors exhibited throughout the presentation of familiar and unfamiliar yawns. By showing no significant different between conditions in the frequencies or durations of the coded behaviors, nor any association between the number of yawns and the frequencies or durations of stress-related behaviors, results raised doubt on the stress-induced yawn hypothesis, thus supporting social modulation. The exact mechanism underlying contagious yawning, however, needs further research.
 

-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. Auditory contagious yawning in domestic dogs (Canis familiaris): first evidence for social modulation. Anim Cogn. 2012.

 
INTRODUCTION
 
The recent interest in the phenomenon of dogs yawning contagiously at humans has raised several challenges as conflicting results from different studies have left a number of unresolved issues (for detailed discussions on the topic see Campbell & de Waal 2010 and Silva et al. 2012). In particular, the question of whether contagious yawning in dogs might have a basis in empathy has stimulated debate among researchers (e.g., Joly Mascheroni et al. 2008 and Silva et al. 2012 vs. O'Hara & Reeve 2010 and Madsen & Persson 2013; see also Yoon & Tennie 2009).
 
By showing that dogs are subject to auditory contagious yawning and that, in addition, this is modulated by familiarity with the model yawner, Silva et al. (2012) provided the first direct test suggesting empathy-based emotionally connected yawn contagion in dogs (but see the complete paper for alternative interpretations). Such evidence, however, strongly contrasts with observations from a previous test on social modulation in dogs (O'Hara & Reeve 2010) and also with more recent data on puppies (Madsen & Persson 2013). In neither of these two studies, was the strength of yawn contagion related to dogs' emotional closeness with the yawning models. Based on this, Madsen & Persson (2013) raised questions about the interpretation of the results presented in Silva et al (2012) and brought up the possibility of a stress-artifact underlying the apparent social modulation reported in Silva et al. (2012): "While the study showed that the sound of familiar yawns elicited more contagious yawning than unfamiliar yawns, the dogs' increased yawning to familiar yawns may have been induced by mildly heightened tension" (Madsen & Persson 2013). That is, according to Madsen & Persson (2013), (at least) some of the yawns observed in response to the sound of familiar yawns as 'natural' contagious yawns might have been, in fact, 'tension' yawns evoked by that particular experimental condition: "The sound of the owner's yawns, emitted from two speakers immediately in front of the dogs, was from a direction where the owner was not (the owner was outside the testing room). Dogs sensing this discrepancy would likely experience uncertainty and consequently mild stress" (Madsen & Persson 2013).
 
The possibility of a stress-related effect underlying Silva et al.s' (2012) findings is a valid concern and deserves serious consideration, particularly given lack of evidence of empathy based-emotionally connected yawning contagion in dogs exposed to familiar and unfamiliar human yawns presented by a live model (O'Hara & Reeve 2010). In light of this, the purpose of the present short study was to further explore recordings from Silva et al. (2012) so as to obtain new data on the potential levels of stress in the tested dogs during the presentation of familiar and unfamiliar yawns.
Assuming that 'tension' yawns, as opposed to 'natural' contagious yawns, tend to co-occur with a number of associated signs of anxiety, then, under Madsen & Perssons' (2013) argument that the increase in dog yawns in response to the sounds of familiar yawns might have been accounted for by elicitation of tension yawns, one should be able to i) notice more frequent (or longer) stress-related behaviors in that particular experimental condition and ii) find a correlation between the number of yawns performed by each dog and the total frequency, or duration, of stress-related behaviors.
 
METHODS
 
Two independent researchers, naive to the purpose of the analysis and blind to the treatment conditions, re-coded the video recordings of all experimental sessions conducted by Silva et al. (2012). Both coded i) the total number of yawns performed by each dog during the presentation of familiar and unfamiliar yawns and ii) the total frequency, or total duration, of the behaviors exhibited by the dogs that could potentially be related to some level of tension. Regarding point ii), a shorter version of the ethogram presented in Beerda et al. (1998) was considered for analysis. Behaviours scored only in terms of frequency of occurrence included: body shaking, circling, open mouth, oral behaviours, sighing, stretching and vocalizing. Behaviours scored as state and event included: autogrooming, panting and trembling.
To test whether stress could have accounted for the results reported in Silva et al. (2012), the above referred behaviors were scored and compared between the two experimental conditions. Potential associations between the total frequencies, or durations, of the observed behaviors and number of yawns performed during the presentation of familiar and unfamiliar yawns were also assessed.
 
All statistical analyses were performed using STATISTICA 7.0 (StatSoft, Tulsa, Oklahoma, USA), and a significance level of 0.05 was used.
 
RESULTS
 
Results showed 100% agreement between the number of yawns coded per dog for each of the two experimental conditions (presentation of familiar and unfamiliar yawns) and those reported in Silva et al. 2012 for those same conditions (i.e. both new coders fully agreed with Silva et al.'s reported yawn frequencies).
In respect to signs of stress, only four behaviours were recorded throughout the entire study: snout liking (coded as an oral behaviour), scratching and licking-self (both coded as autogrooming) and panting. No other behaviour considered for analysis (see the Methods section) was ever observed.
 
Since the total duration of the observed tension-related behaviours was not normally distributed (Shapiro-Wilk, goodness-of-fit, tests, P>0.05) only non-parametric tests (i.e., Wilcoxon matched pairs tests) were used throughout to assess differences between treatments with regard to apparent stress levels.
 
Results showed no significant differences in neither the total frequency of the observed stress related behaviors (snout liking, scratching, licking-self and panting; mean total frequency ± S.D. during the presentation of familiar yawns: 0.14 ± 0.44; mean total frequency ± S.D. during the presentation of unfamiliar yawns: 0.10 ± 0.41; N=29, Z= 0.26, P=0.79) nor in total duration (scratching, licking-self and panting; mean total duration ± S.D. during the presentation of familiar yawns: 0.52 ± 1.57; mean total duration ± S.D. recorded during the presentation of unfamiliar yawns: 0.66 ± 1.88; N=29, Z=0.63, P=0.53). Also, no correlations were found between total frequency of stress-related behaviors and number of yawns performed during the presentation of familiar and unfamiliar yawns (familiar yawns: Pearson's r =0.14, P =0.46; unfamiliar yawns: Pearson's r =0.09, P =0.65). Additionally, no correlations were found between total duration of stress-related behaviors and number of yawns (familiar yawns: Pearson's r =0.11, P =0.58; unfamiliar yawns: Pearson's r =0.19, P =0.33).
 
DISCUSSION
 
According to Madsen & Persson's (2013), a stress-effect related to the particular experimental procedure used by Silva et al. (2012) - instead of an actual social effect - might have accounted for the reported pattern of yawning. The sounds of the familiar (i.e., owner's) yawns were not emitted from the exact same place where the owners were hiding, which according to Madsen & Persson (2013) could have generated uncertainty, and consequently mild stress, in the tested dogs. The behavioral analysis here presented, however, does not to support this hypothesis. Tested dogs only rarely showed behavioral indicators of stress and, crucially, there were no differences in stress levels between conditions. Also, no association was found between the number of yawns and the level of observed stress, thus raising doubt on the stress-induced yawn hypothesis.
 
Importantly, we only measured stress as evidenced in stress-correlated behaviors, following Beerda et al. (1998). That is, we did not measure stress directly through physiological measurements, and we therefore cannot fully discard Madsen & Persson's (2013) argument. It seems however unlikely that the tested dogs might have been able to control their outwards emotional responses throughout the experimental sessions, thus showing physiological markers of tension (such as heart rate changes; Harr et al. 2010), but suppressing behavioral indicators. Also, it is important to note, that the speakers used in Silva et al. (2012), and from which the sounds of yawns were emitted, were positioned as close as possible (< 1 meter) to the owner, and that previous studies testing the ability of dogs to match an auditory stimulus to a corresponding visual stimulus were not compromised by dogs' acute sound localization. In Taylor et al. (2012), for example, the distance between the speakers from which sounds were emitted and the associated visual stimulus was 1.5 meters.
 
We conclude that stress differences per se did not account for the results presented in Silva et al. (2012). How, then, to interpret the contradictory evidence of socially modulated contagious yawning in dogs reported in O'Hara & Reeve (2010) and Madsen & Persson (2013) (see the introduction section)? With respect to the latter, it seems to us, given the age of the tested dogs (puppies ranging from 4 to 14 months of age), that the contradiction may be related to the testing age. Indeed the authors themselves refer to the possibility that, in species that exhibit an empathy-based social modulatory effect on contagious yawning, the effect may emerge only at later stages of development (Madsen & Persson 2013). With respect to the lack of evidence of familiarity biased contagious yawning reported in O'Hara & Reeve (2010), we previously argued that disparate findings could have been due to the methodology followed by these authors, which implied some dog-human interaction that could have diverted the dogs' attention from the yawn stimuli (for further details, see Silva et al. 2012). We, did, however, also highlight the possibility that the social modulation of contagious yawing evidenced by our previous results - and supported by the present analysis - could be related to differences in dogs' capacity to form mental representations from familiar and unfamiliar auditory input (see Adachi et al. 2007).
Clearly, there is a need for some kind of standardization in the methodologies used to explore the phenomenon of dogs yawning contagiously at humans, so that unequivocal conclusions can be drawn about the particular mechanism at its base - be it empathy related or not. Also, particularly interesting insights could be gained from longitudinal studies, in which the same dogs are tested throughout their developmental process (i.e., from puppies to adults).
 
ACKNOWLEDGMENTS
 
We thank Elainie Alenkær Madsen and Tomas Persson for calling attention on the possibility of a stress related effect underlying the results presented in our previous study on contagious yawning in dogs. Also we are grateful to Claudio Tennie for his valuable comments.
 
REFERENCES
 
Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner's face upon hearing the owner's voice. Anim Cogn 10: 17-21.
 
Beerda B, Schilder MBH, van Hooff JARAM, de Vries HW, Mol JA
(1998) Behavioral, saliva, cortisol and heart rate responses to different types of stimuli
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Campbell MW, de Waal FBM (2010) Methodological problems in the study of contagious yawning. Front Neurol Neurosci 28: 20-127.
 
Joly-Mascheroni RM, Senju A, Shepherd AJ (2008) Dogs catch human yawns. Biol Lett 4: 446-448.
 
Madsen EA, Persson T (2013) Contagious yawning in domestic dog puppies (Canis lupus familiaris): the effect of ontogeny and emotional closeness on low-level imitation in dogs. Anim Cogn 6: 233-240.
 
O'Hara SJ, Reeve AV (2010) A test of the yawning contagion and emotional connectedness hypothesis in dogs, Canis familiaris. Anim Behav 81: 335-340.
 
Silva K, Bessa J, de Sousa L (2012) Auditory contagious yawning in domestic dogs (Canis familiaris): first evidence for social modulation. Anim Cogn 15: 721-724.
 
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Yoon JMD, Tennie C (2010) Contagious yawning: a reflection of empathy, mimicry, or contagion? Anim Behav 79: 1-3.