You are on page 1of 4

Anim Cogn (2013) 16:1007–1009

DOI 10.1007/s10071-013-0669-0

SHORT COMMUNICATION

Familiarity-connected or stress-based contagious yawning


in domestic dogs (Canis familiaris)? Some additional data
Karine Silva • Joana Bessa • Liliana de Sousa

Received: 5 March 2013 / Revised: 16 July 2013 / Accepted: 6 August 2013 / Published online: 28 August 2013
Ó Springer-Verlag Berlin Heidelberg 2013

Abstract The present short note aimed at further Introduction


exploring data from a recent study showing socially mod-
ulated auditory contagious yawning in domestic dogs The recent interest in the phenomenon of dogs yawning
(Canis familiaris). Two independent observers further contagiously at humans has raised several challenges as
extended the analysis of all video recordings made in the conflicting results from different studies have left a number
previous study and coded both the number of yawns per- of unresolved issues (for detailed discussions on the topic
formed by the dogs and the frequencies or durations of see Campbell and de Waal 2010; Silva et al. 2012). In
stress-related behaviors exhibited throughout the presen- particular, the question of whether contagious yawning in
tation of familiar and unfamiliar yawns. By showing no dogs might have a basis in empathy has stimulated debate
significant difference between conditions in the frequencies among researchers (e.g., Joly-Mascheroni et al. 2008; Silva
or durations of the coded behaviors, nor any association et al. 2012 vs. O’Hara and Reeve 2010; Madsen and
between the number of yawns and the frequencies or Persson 2013; see also Yoon and Tennie 2010).
durations of stress-related behaviors, results raised doubt By showing that dogs are subject to auditory contagious
on the stress-induced yawn hypothesis, thus supporting yawning and that, in addition, this is modulated by famil-
social modulation. The exact mechanism underlying con- iarity with the model yawner, Silva et al. (2012) provided
tagious yawning, however, needs further research. the first direct test suggesting empathy-based emotionally
connected yawn contagion in dogs (but see the complete
Keywords Contagious yawning  Domestic dogs  paper for alternative interpretations). Such evidence,
Social modulation  Stress however, strongly contrasts with observations from a pre-
vious test on social modulation in dogs (O’Hara and Reeve
2010) and also with more recent data on puppies (Madsen
and 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
and Persson (2013) raised questions about the interpreta-
tion of the results presented in Silva et al. (2012) and
Karine Silva and Joana Bessa contributed equally to this work. brought up the possibility of a stress artifact underlying the
apparent social modulation reported in Silva et al. (2012):
K. Silva (&)  J. Bessa  L. de Sousa
‘While the study showed that the sound of familiar yawns
Departamento de Ciências do Comportamento, Instituto de
Ciências Biomédicas Abel Salazar, Universidade do Porto, elicited more contagious yawning than unfamiliar yawns,
Largo Prof. Abel Salazar, 2, 4099-003 Porto, Portugal the dogs’ increased yawning to familiar yawns may have
e-mail: cssilva@icbas.up.pt been induced by mildly heightened tension’ (Madsen and
Persson 2013). That is, according to Madsen and Persson
K. Silva  J. Bessa  L. de Sousa
Ânimas, Avenida Sidónio Pais, 392, r/c Dto., (2013), (at least) some of the yawns observed in response
4100-466 Porto, Portugal to the sound of familiar yawns as ‘natural’ contagious

123
1008 Anim Cogn (2013) 16:1007–1009

yawns might have been, in fact, ‘tension’ yawns evoked by and number of yawns performed during the presentation of
that particular experimental condition: ‘The sound of the familiar and unfamiliar yawns were also assessed.
owner’s yawns, emitted from two speakers immediately in All statistical analyses were performed using STATIS-
front of the dogs, was from a direction where the owner TICA 7.0 (StatSoft, Tulsa, Oklahoma, USA), and a sig-
was not (the owner was outside the testing room). Dogs nificance level of 0.05 was used.
sensing this discrepancy would likely experience uncer-
tainty and consequently mild stress’ (Madsen and Persson
2013). Results
The possibility of a stress-related effect underlying Silva
et al.’s (2012) findings is a valid concern and deserves Results showed 100 % agreement between the number of
serious consideration, particularly given lack of evidence of yawns coded per dog for each of the two experimental
empathy-based, emotionally connected yawning contagion conditions (presentation of familiar and unfamiliar yawns)
in dogs exposed to familiar and unfamiliar human yawns and those reported in Silva et al. 2012 for those same
presented by a live model (O’Hara and Reeve 2010). In light conditions (i.e., both new coders fully agreed with Silva
of this, the purpose of the present short study was to further et al.’s reported yawn frequencies).
explore recordings from Silva et al. (2012) so as to obtain With respect to signs of stress, only four behaviors were
new data on the potential levels of stress in the tested dogs recorded throughout the entire study: snout liking (coded as
during the presentation of familiar and unfamiliar yawns. an oral behavior), scratching and licking self (both coded
Assuming that ‘tension’ yawns, as opposed to ‘natural’ as autogrooming), and panting. No other behavior consid-
contagious yawns, tend to co-occur with a number of ered for analysis (see the ‘Methods’ section) was ever
associated signs of anxiety, then, under Madsen and Pers- observed.
son’s (2013) argument that the increase in dog yawns in Since the total duration of the observed tension-related
response to the sounds of familiar yawns might have been behaviors was not normally distributed (Shapiro–Wilk
accounted for elicitation of tension yawns, one should be goodness-of-fit tests, P [ 0.05), only nonparametric tests
able to (1) notice more frequent (or longer) stress-related (i.e., Wilcoxon matched-pairs tests) were used throughout
behaviors in that particular experimental condition and (2) to assess differences between treatments with regard to
find a correlation between the number of yawns performed apparent stress levels.
by each dog and the total frequency, or duration, of stress- Results showed no significant differences in either the
related behaviors. 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
Methods yawns was 0.14 ± 0.44; mean total frequency ± S.D. dur-
ing the presentation of unfamiliar yawns was 0.10 ± 0.41;
Two independent researchers, naive to the purpose of the N = 29, Z = 0.26, P = 0.79) or total duration (scratching,
analysis and blind to the treatment conditions, re-coded the licking self, and panting; mean total duration ± S.D. during
video recordings of all experimental sessions conducted by the presentation of familiar yawns was 0.52 – 1.57; mean
Silva et al. (2012). Both coded (1) the total number of total duration ± S.D. recorded during the presentation of
yawns performed by each dog during the presentation of unfamiliar yawns was 0.66 ± 1.88; N = 29, Z = 0.63,
familiar and unfamiliar yawns and (2) the total frequency, P = 0.53). Also, no correlations were found between total
or total duration, of the behaviors exhibited by the dogs frequency of stress-related behaviors and number of yawns
that could potentially be related to some level of tension. performed during the presentation of familiar and unfamiliar
Regarding point (2), a shorter version of the ethogram yawns (familiar yawns: Pearson’s r = 0.14, P = 0.46;
presented in Beerda et al. (1998) was considered for unfamiliar yawns: Pearson’s r = 0.09, P = 0.65). Addi-
analysis. Behaviors scored only in terms of frequency of tionally, no correlations were found between total duration
occurrence including the following: body shaking, circling, of stress-related behaviors and number of yawns (familiar
open mouth, oral behaviors, sighing, stretching, and yawns: Pearson’s r = 0.11, P = 0.58; unfamiliar yawns:
vocalizing. Behaviors scored as state and event including Pearson’s r = 0.19, P = 0.33).
the following: autogrooming, panting, and trembling.
To test whether stress could have accounted for the
results reported in Silva et al. (2012), the above-referred Discussion
behaviors were scored and compared between the two
experimental conditions. Potential associations between the According to Madsen and Persson’s (2013), a stress effect
total frequencies, or durations, of the observed behaviors related to the particular experimental procedure used by

123
Anim Cogn (2013) 16:1007–1009 1009

Silva et al. (2012)—instead of an actual social effect— due to the methodology followed by these authors, which
might have accounted for the reported pattern of yawning. implied some dog–human interaction that could have
The sounds of the familiar (i.e., owner’s) yawns were not diverted the dogs’ attention from the yawn stimuli (for
emitted from the exact same place where the owners were further details, see Silva et al. 2012). We, did, however,
hiding, which according to Madsen and Persson (2013) also highlight the possibility that the social modulation of
could have generated uncertainty and consequently mild contagious yawing evidenced by our previous results—and
stress in the tested dogs. The behavioral analysis here supported by the present analysis—could be related to
presented, however, does not support this hypothesis. differences in dogs’ capacity to form mental representa-
Tested dogs only rarely showed behavioral indicators of tions from familiar and unfamiliar auditory inputs (see
stress, and, crucially, there were no differences in stress Adachi et al. 2007).
levels between conditions. Also, no association was found Clearly, there is a need for some kind of standardization
between the number of yawns and the level of observed in the methodologies used to explore the phenomenon of
stress, thus raising doubt on the stress-induced yawn dogs yawning contagiously at humans, so that unequivocal
hypothesis. conclusions can be drawn about the particular mechanism
Importantly, we only measured stress as evidenced in at its base—be it empathy related or not. Also, particularly
stress-correlated behaviors, following Beerda et al. (1998). interesting insights could be gained from longitudinal
That is, we did not measure stress directly through physi- studies, in which the same dogs are tested throughout their
ological measurements, and we therefore cannot fully developmental process (i.e., from puppies to adults).
discard Madsen and Persson’s (2013) argument. It seems
however unlikely that the tested dogs might have been able Acknowledgments We thank Elainie Alenkaer Madsen and Tomas
Persson for calling attention on the possibility of a stress-related
to control their outward emotional responses throughout effect underlying the results presented in our previous study on
the experimental sessions, thus showing physiological contagious yawning in dogs. Also, we are grateful to Claudio Tennie
markers of tension (such as heart rate changes; Harr et al. for his valuable comments.
2009), but suppressing behavioral indicators. Also, it is
important to note that the speakers used in Silva et al.
(2012), from which the sounds of yawns were emitted, References
were positioned as close as possible (\1 m) to the owner
Adachi I, Kuwahata H, Fujita K (2007) Dogs recall their owner’s face
and that previous studies testing the ability of dogs to upon hearing the owner’s voice. Anim Cogn 10:17–21
match an auditory stimulus to a corresponding visual Beerda B, Schilder MBH, van Hooff JARAM, de Vries HW, Mol JA
stimulus were not compromised by dogs’ acute sound (1998) Behavioral, saliva, cortisol and heart rate responses to
localization. In Taylor et al. (2011), for example, the dis- different types of stimuli in dogs. Appl Anim Behav Sci
58:365–381
tance between the speakers from which sounds were Campbell MW, de Waal FBM (2010) Methodological problems in the
emitted and the associated visual stimulus was 1.5 m. study of contagious yawning. Front Neurol Neurosci 28:20–127
We conclude that stress differences per se did not Harr AL, Gilbert VR, Phillips KA (2009) Do dogs (Canis familiaris)
account for the results presented in Silva et al. (2012). show contagious yawning? Anim Cogn 12:833–837
Joly-Mascheroni RM, Senju A, Shepherd AJ (2008) Dogs catch
How, then, to interpret the contradictory evidence of human yawns. Biol Lett 4:446–448
socially modulated contagious yawning in dogs reported in Madsen EA, Persson T (2013) Contagious yawning in domestic dog
O’Hara and Reeve (2010) and Madsen and Persson (2013) puppies (Canis lupus familiaris): the effect of ontogeny and
(see the ‘Introduction’ section)? With respect to the latter, emotional closeness on low-level imitation in dogs. Anim Cogn
6:233–240
it seems to us, given the age of the tested dogs (puppies O’Hara SJ, Reeve AV (2010) A test of the yawning contagion and
ranging from 4 to 14 months of age), that the contradiction emotional connectedness hypothesis in dogs, Canis familiaris.
may be related to the testing age. Indeed, the authors Anim Behav 81:335–340
themselves refer to the possibility that, in species that Silva K, Bessa J, de Sousa L (2012) Auditory contagious yawning in
domestic dogs (Canis familiaris): first evidence for social
exhibit an empathy-based social modulatory effect on modulation. Anim Cogn 15:721–724
contagious yawning, the effect may emerge only at later Taylor AM, Reby D, McComb K (2011) Cross modal perception of
stages of development (Madsen and Persson 2013). With body size in domestic dogs (Canis familiaris). PLoS ONE
respect to the lack of evidence of familiarity-based conta- 6:e17069
Yoon JMD, Tennie C (2010) Contagious yawning: a reflection of
gious yawning reported in O’Hara and Reeve (2010), we empathy, mimicry, or contagion? Anim Behav 79:1–3
previously argued that disparate findings could have been

123
Copyright of Animal Cognition is the property of Springer Science & Business Media B.V.
and its content may not be copied or emailed to multiple sites or posted to a listserv without
the copyright holder's express written permission. However, users may print, download, or
email articles for individual use.

You might also like