Applied Animal Behaviour Science 223 (2020) 104916

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Applied Animal Behaviour Science

journal homepage: www.elsevier.com/locate/applanim

The effect of oxytocin on yawning by dogs (Canis familiaris) exposed to T

human yawns
Anna Kis*, Katinka Tóth, Orsolya Kanizsár, József Topál
Research Centre for Natural Sciences, Institute of Cognitive Neuroscience and Psychology, Hungarian Academy of Sciences, Magyar Tudósok krt. 2, 1117, Budapest,
Hungary

A R T I C LE I N FO A B S T R A C T

Keywords: Previous studies have found that human yawning is contagious to dogs, but the results are still controversial. It is
Dog also debated whether contagious yawning is a sign of empathy, and the physiological mechanisms behind this
Contagious yawning phenomenon are also unknown. Our goal was to further investigate if human yawning is contagious to dogs, and
Empathy how it is affected by intranasally administered oxytocin. We also tested if contagious yawning was related to
Oxytocin
dogsʼ empathetic skills measured via an owner-completed questionnaire. Dogs (N = 33) were presented with
human yawns (yawning condition – YC) or mouth openings (gaping condition – GC) on two test occasions after
intranasal administration of 12 IU oxytocin or placebo. Contagious yawning (defined as a significant increase in
the number of yawns in YC as compared to GC) was not found in either of the treatment groups and the number
of yawns was not related to the owner-reported emotion contagion of the dogs. However, oxytocin pre-treatment
significantly decreased the number of yawns in dogs (in general, but more particularly during the phase when
human yawns and gaping were presented). Furthermore, there was a positive relation between signs of stress and
anxiety (mouth licking) and the number of yawns (in general, but more particularly during the post phase when
human yawns and gaping were not any more presented). We conclude that dogs’ yawning observed in this
situation may largely be due to situational stress. Thus the difference between the oxytocin and the placebo
group is possibly caused by the decreased social stress and not by oxytocin’s hypothesised effect on empathy.

1. Introduction response to the experimenterʼs yawning in contrast to the control con-

Due to their special domestication history (Hare et al., 2002) as well
as their prolonged and intensive contact with humans (Wynne et al.,
2008) dogs have been shown to be an ideal model species for studying
different aspects of human social behaviour (Hare and Tomasello, 2005;
Miklósi and Topál, 2013) as well as its neural (Bunford et al., 2017),
hormonal (Kis et al., 2017a) and genetic (Parker and Ostrander, 2005;
Hejjas et al., 2007) background. Although even such easily measurable
markers of social competence as dogs’ infant-like ability to follow
human pointing (Lakatos et al., 2009) are surrounded by vivid debates
(Riedel et al., 2008; Udell and Wynne, 2010; Elgier et al., 2012;
Pongrácz et al., 2013), it is increasingly assumed that dogs develop a
relatively deep understanding of nuances of interspecific (dog-human)
social interactions. One of the presumed hallmarks of dogs’ social
competence is empathy, that makes it possible for human yawning to be
contagious to dogs (Joly-Mascheroni et al., 2008), although research in
this field is still controversial (O’Hara and Reeve, 2011). Joly-
Mascheroni et al. (2008) found that 72 % of the dogs yawned in
dition when none of them did. This performance is comparable to or
even exceeds the level of yawn contagion in adult humans (Provine,
1986). In contrast, Harr et al. (2009) reported that human yawns pre-
sented on videos were not contagious to dogs, while others (O’Hara and
Reeve, 2011) found that if contagious yawning does exist in dogs at all,
it is only present to a much lesser degree than originally proposed.
Another study (Silva et al., 2012), however, has confirmed that human
yawning is contagious to dogs, moreover according to their results the
mere sound of yawning was enough to elicit the phenomenon. This
inconsistency of findings may largely be due to methodological differ-
ences. The experimental arrangement of the “original” study (Joly-
Mascheroni et al., 2008), for example, has received lot of criticism
because it was done in an unnatural setting; dogs had to sit facing the
experimenter during the presentation of the yawns, thus the behaviour
labelled contagious yawning may not be related to ‘empathic response’
but might stem, at least partly, from situational stress (Silva and de
Sousa, 2011).
While yawn contagion is often labelled as a complex capacity

⁎
Corresponding author.
E-mail address: vargane.kis.anna@ttk.mta.hu (A. Kis).

https://doi.org/10.1016/j.applanim.2019.104916
Received 3 June 2019; Received in revised form 15 November 2019; Accepted 17 November 2019
Available online 26 November 2019
0168-1591/ © 2019 Elsevier B.V. All rights reserved.
A. Kis, et al.
related to empathy, yawning in itself is a wide-spread and common
behavioural event that consists of a long inspiratory phase, a brief acme
and a rapid expiration (Daquin et al., 2001). The function of yawning,
however, is not yet well understood (Guggisberg et al., 2007). In hu-
mans it is known that this semi-voluntary event increases vigilance and
aims to alert when sleepiness occurs, as well as probably has an im-
portant role for social communication, e.g. to synchronize group be-
haviour. Yawning has been found in all the major vertebrate classes,
including several mammalian orders (e.g., primates, carnivores, and
rodents), birds, reptiles, amphibians and fish (Baenninger and Greco,
1991). Despite the ubiquitous nature of yawning, several evolutionary
hypotheses have been proposed suggesting that yawning has a specific
function in humans, mostly because of its contagiousness (Smith,
1999).
Another widely studied and highly controversial topic is the role
oxytocin plays in the regulation of human-specific socio-cognitive
capabilities. It is well known that in humans oxytocin, among others,
plays a pivotal role in social bonding (Donaldson and Young, 2008), as
well as in socio-cognitive skills (Savaskan et al., 2008). The oxytocin
system is also related to psychiatric conditions such as autism, de-
pression and social anxiety disorders (Hollander et al., 2007). Fur-
thermore polymorphisms in the oxytocin receptor (OXTR) gene influ-
ence such complex human social behaviours as attachment (Gillath
et al., 2008; Chen et al., 2011) or empathy (Rodrigues et al., 2009). The
latter result ‒ the relationship between the oxytocin system and human
empathy ‒ is especially important for the present study. We have to
note, however, that empathy is a complex umbrella term, and its re-
lation to the oxytocin system is not straightforward. It has been shown
for example that intranasally administered oxytocin does not affect the
activity of brain regions (anterior insula) responsible for empathic
distress (self-centred feelings of discomfort and anxiety in response to
the perceived physical or emotional pain of another person – Singer
et al., 2008). On the other hand empathic concern (other-oriented
feelings of sympathy and compassion) are related to the oxytocin
system as it has been shown (Barraza and Zak, 2009) that after viewing
a video of a young boy suffering from cancer there was a positive re-
lationship between the increase in peripheral oxytocin levels and feel-
ings of empathic concern, but not empathic distress. Furthermore the
magnitude of the change in participants’ blood oxytocin level was re-
lated to their baseline empathy measured via questionnaire. However,
there are some more recent results (Tabak et al., 2015) arguing that
empathic concern is related to the vasopressin, but not to the oxytocin
system. Results regarding the relationship between the oxytocin system
and the third component of empathy, cognitive empathy (the capacity
to understand an otherʼs mental state without feeling in the same way)
are also controversial. Some (Domes et al., 2007) have shown that in-
tranasally administered oxytocin increases adult participant’s perfor-
mance in a “mind-reading” task where they have to attribute emotions
to photographs representing a pair of eyes. Another study (Rodrigues
et al., 2009) has found an association between performance in the same
task and single nucleotide polymorphisms in the OXTR gene. But there
are results (Hurlemann et al., 2010) suggesting that intranasally ad-
ministered oxytocin is only related to empathic concern and not to
cognitive empathy. Although the effect of oxytocin on contagious
yawning has not yet been investigated in humans either, there is an
indirect relationship as autistic children have lower plasma oxytocin
levels (Modahl et al., 1998) and show diminished susceptibility to
contagious yawning (Senju et al., 2007; Helt et al., 2010).
In case of dogs it has already been shown that the oxytocin system is
related to human-directed social behaviour (for a summary of the most
recent results see Kis et al., 2019). The classic findings include evidence
for an increase in peripheral oxytocin levels not only after positive
social interactions (Odendaal and Meintjes, 2003; Handlin et al., 2011;
Mitsui et al., 2011; Hritcu et al., 2019), but also following intranasal
oxytocin treatment (Temesi et al., 2017). Such intranasal oxytocin
treatments have also been found to influence various forms of dogs’
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Applied Animal Behaviour Science 223 (2020) 104916
social behaviour including affiliative versus agonistic responses
(Romero et al., 2014; Hernádi et al., 2015), the use of human com-
municative signals (Oliva et al., 2015; Oláh et al., 2017) and gaze in-
itiation towards humans (Nagasawa et al., 2015; Kis et al., 2017b).
These results are generally and mostly in line with findings from human
studies, although important null-results have also been reported e.g. on
dogs’ attachment to humans (Thielke et al., 2017, but see: Kovács et al.,
2018). Moreover, similarly to humans (e.g. Bartz et al., 2011), con-
siderable individual as well as group-level differences have been re-
vealed in terms of dogs’ oxytocin-responsiveness (e.g. breed: Kis et al.,
2014a; Kovács et al., 2016b; sex: Cimarelli et al., 2016; Kovács et al.,
2016a). The effect of oxytocin on empathy and contagious yawning,
however, has not yet been investigated in dogs.
The purpose of the present study is threefold: 1) to assess the
yawning-inducing effect of human yawns and the association between
yawning and overt signs of stress such as mouth licking in dogs; 2) to
test if yawn contagion is related to dogsʼ baseline empathy (measured
via an owner-completed questionnaire); and 3) to investigate the effect
of intranasally administered oxytocin on the contagiousness of human
yawning to dogs. One possible prediction is that contagious yawning, as
a form of empathetic behaviour, would increase after oxytocin treat-
ment, and would be unrelated to stress indicators. On the contrary, it
can also be predicted that dogs’ yawning in response to human yawns is
related to stress signs (unrelated to empathy), and would thus decrease
after oxytocin treatment.
2. Methods
2.1. Ethical statement
Research was done in accordance with the Hungarian regulations on
animal experimentation and the Guidelines for the use of animals in
research described by the Association for the Study Animal Behaviour
(ASAB). Ethical approval was obtained from the National Animal
Experimentation Ethics Committee (Ref No. XIV-I-001/531-4-2012).
2.2. Subjects
33 adult pet dogs (mean age ± SD: 4.68 ± 2.58 years) and their
owners were recruited on a voluntary basis. All dogs were older than
1 year of age, as similarly to humans a developmental effect has been
observed in the contagiousness of yawning in dogs (Harr et al., 2009;
O’Hara and Reeve, 2011). Subjects in our study were both mixed
(n = 14) and purebred (n = 19), intact (n = 11) and neutered
(n = 22), male (n = 19), and female (n = 14), single dog (n = 16) and
from multiple-dog households (n = 17). Subjects were randomly as-
signed to test conditions and the two conditions did not differ in subject
properties.
2.3. Procedure
The experiment took place in a room (3.9 m × 4.1 m) at the Family
Dog Project laboratory, Eötvös University, Budapest. Subjects partici-
pated in two test occasions with a minimum of 1 and a maximum of 13
days in-between (mean ± SD: 5.43 ± 3.60 days) receiving oxytocin
and placebo treatment (see later) in a counterbalanced order. Both the
owner and the experimenter were blind to the treatment and owners
were unable to guess if their dogs had received oxytocin or placebo on
either the first (Binomial test; p = 0.608) or the second (p = 1.000)
occasions. Subjects were randomly assigned to either the Yawning
(N = 15) or the Gaping (control; N = 18) condition (see later), parti-
cipating in this condition after both the oxytocin and the placebo pre-
treatment. Test occasions in both conditions (and for both pre-treat-
ments) consisted of first a test phase (during which the human ex-
perimenter presented yawns or gaping) and then a post phase of quiet
waiting without any yawns or gaping presented.
A. Kis, et al.
2.3.1. Oxytocin and placebo treatment, waiting period
The pretreatment was performed following a protocol previously
validated by showing the effect of oxytocin on heart rate and heart rate
variability (Kis et al., 2014b). Dogs were administered 3 puffs of pla-
cebo (0.7 % NaCl solution), or 3 puffs of oxytocin (12 IU, Syntocinon,
Novartis) intranasally to alternating nostrils. This was followed by a
40 min waiting period necessary for the central oxytocin levels to reach
plateau (Born et al., 2002). During this time dogs spent the first 30 min
with an on-leash walk with their owner and the experimenter at the
university campus. The experimenter ensured that neither the owner
nor other people or dogs made any social contact (e.g. eye-contact, dog-
directed talk) with the dog as this could have affected oxytocin levels
(Nagasawa et al., 2015).
For the remaining 10 min dogs and owners were left alone in the
behavioural laboratory. Dogs were off the leash and free to move in the
room, while owners were sitting on a chair and instructed not to look at
or interact with their dogs. Owners were informed that they would be
video recorded from that moment on and they were asked to fill in a
canine empathy questionnaire ‒ a child empathy questionnaire (Rieffe
et al., 2010) adapted for dogs ‒ during the waiting period. Owners were
instructed to answer all questions to their best knowledge, even if some
of the items are anthropomorphic and/or they cannot recall the exact
same situation. The questionnaire consisted of 20 items and the owners
had to rate how often the given behaviour occurred in their dog (1:
never ‒ 5: always). The items belonged to three scales: Emotion Con-
tagion, Attention to Others’ Feelings, and Prosocial Actions. For the
current analysis solely the Emotion Contagion scale was used, this
consisted of the following seven items: “when another dog cries, my dog
gets upset too” “when other dogs fight, my dog gets upset”, “my dog
also needs to be comforted when another dog is in pain” “when another
dog makes a bad fall, shortly after my dog pretends to fall too” “when
another dog gets frightened, my dog freezes or starts to cry” “when
another dog cries, my dog looks away” “when another dog is upset, my
dog needs to be comforted too”.
2.3.2. Behavioural test
The experimental procedure was based on that used by Madsen and
Persson (2013) thus in an effort to make the situation as natural as
possible, dogs were free to move in the experimental room while both
the owner and a female experimenter were seated on the floor. Subjects
on both occasions (once after oxytocin and once after placebo pre-
treatment, in a random order) participated in the same test condition:
they could see the experimenter either yawning or gaping. The tests
were carried out by three female experimenters, with an even dis-
tribution among the two conditions. Each subject had the same ex-
perimenter on both occasions.
Yawning. During the 5 min of the test phase the experimenter re-
peatedly yawned for at least 15 times. Experimenters yawned as
naturally as possible, with yawning defined as opening the mouth fully,
drawing in air, tilting the head and body backwards, closing the eyes,
and producing a vocalisation during exhalation, for a total duration of
5–10 s. As the mere sound of human yawning has also been shown to be
contagious to dogs (Silva et al., 2012), subjects were not forced to look
at the experimenter and make eye-contact during the demonstrations, it
was sufficient for the experimenter to be in the dogsʼ peripheral vision.
The test phase was followed by a 5-min-long post phase during which
no yawns were produced, the experimenter and the owner were just
talking to each other.
Coding of the video recordings after the test revealed that dogs in
the placebo group witnessed (defined as orienting towards the experi-
menter) on average ( ± SD) 18 ± 7 yawns during the demonstration
accounting for the 59 ± 17 % of the yawns performed. Subjects in the
oxytocin group witnessed on average ( ± SD) 15 ± 5 yawns during the
demonstration accounting for the 53 ± 18 % of the yawns performed.
This number was similar to those in previous experiments (e.g. 16 ± 2
in Madsen and Persson, 2013).
3
Applied Animal Behaviour Science 223 (2020) 104916
Gaping. The test phase of the gaping condition differed from the
yawning in that in this case instead of yawning the experimenter re-
peatedly opened the mouth wide saying a prolonged [a:] sound of
5–10 s duration, and then closed her mouth. The test phase was also
followed by a 5-minute-long post phase without gaping.
Coding of the video recordings after the test revealed that dogs in
the gaping condition witnessed (defined as orienting towards the ex-
perimenter) a similar number of demonstrations as in the yawning
condition: average ( ± SD) 19 ± 3.6 gapings accounting for the
60.3 ± 7.3 % of the gapings performed in the placebo groups and an
average ( ± SD) 18 ± 2 gapings accounting for the 61 ± 9.2 % of the
gapings performed in the oxytocin group.
2.4. Data analysis
The number of elicited yawns was coded from the video recordings
during both the test and the post phases as the main outcome measure.
The number of mouth licks was also coded from the videos. Coding was
blind to subject details and oxytocin / placebo treatment. From the
questionnaire data the Emotion contagion factor was extracted ac-
cording to the guidelines of Rieffe et al. (2010). Data analysis was
carried out with Generalized Linear Mixed Model (with dog ID as
random factor) using the number of yawns as the target variable and
condition (yawning versus gaping), phase (test versus post), pre-treat-
ment (oxytocin versus placebo) as well as the number of mouth licks
and questionnaire measured emotion contagion as predicting variables.
Main effects and all possible two-way interactions were examined,
using backward elimination to step-by-step eliminate the least sig-
nificant factors from the model. All analyses were carried out with SPSS
version 22.
3. Results
Contagious yawning was not convincingly observable in our sub-
jects, as there was only a non-significant tendency in the placebo group
for more yawns in the yawning compared to the gaping condition
(condition × pre-treatment: F(1,121) = 2.815, p = 0.096; condition
main effect: F(1,121) = 0.144, p = 0.705; Fig. 1). It was found that
oxytocin pre-treatment significantly decreased the number of yawns,
especially during the test phase (pre-treatment × phase:
F(1,121) = 4.499, p = 0.036; pre-treatment main effect: F(1,121) = 4.459,
p = 0.037).
In addition the number of yawns was strongly related to the number
of mouth licks, especially during the post phase (mouth licks × phase:
Fig. 1. The number of elicited yawns (median, quartiles, whiskers, outliers) for
the different phases, conditions and pre-treatments.
A. Kis, et al.
Fig. 2. Relationship between the number of elicited yawns and mouth licks for
the differentphases, conditions and pre-treatments.
F(1,121) = 8.234, p = 0.005; mouth licks main effects: F(1,121) = 14.100,
p < 0.001; Fig. 2). The main effect of phase was not significant
(F(1,121) = 1.038, p = 0.310).
The effect of questionnaire measured emotion contagion (empathy)
was not significant neither as a main effect, nor in interaction with any
other variables (all p > 0.1).
4. Discussion
The present study provides mixed results regarding the effect of
oxytocin on dogs’ yawn contagion. The lack of contagious yawning in
the placebo group contradicts previous findings (Joly-Mascheroni et al.,
2008), although some (Harr et al., 2009) have found similar negative
results. Our findings are also in line with the fact that yawn contagion
in humans emerges only in preschool-age children reaching adult levels
at around the age of 12 years (Anderson and Meno, 2003; Millen and
Anderson, 2011), while dogs’ socio-cognitive capacities are generally
comparable to that of considerably younger children (Lakatos et al.,
2009; Péter et al., 2014). Emotion contagion, however, has been found
in dogs both in response to positively and negatively valenced sound
playbacks (Huber et al., 2017) as well as in the form of rapid mimicry
(Palagi et al., 2015). Thus we would not argue for the lack of emotion
contagion in dogs, in fact the tendency we found in the placebo groups
hints for a weak yawn contagion in our subjects as well. However,
based on several of our current findings we might argue that yawning in
this contagious yawning test situation is not a form of empathic re-
sponse.
The lack of association between dogsʼ owner-reported emotion
contagion and the number of elicited yawns suggests dissociation be-
tween these two measures. The relationship between empathy and
contagious yawning is also debated in case of humans. Some (Chartrand
and Bargh, 1999) argue that more empathetic people are more prone to
all form of social mimicry and thus might be more susceptible to yawn
contagion (Platek et al., 2003). Others (Deputte, 1994) differentiate two
types of yawns in primates, the so-called rest yawns, and the social
yawns; with only this latter belonging to social mimicries. Similar
theories ‒ yawning as social mimicry (Yoon and Tennie, 2010) ‒ have
also been proposed for dogs, as it has been found that dogs living in a
rescue shelter yawned more at mostly unfamiliar human models com-
pared to pet dogs (O’Hara and Reeve, 2011). This might be explained by
contact-deprived dogs recognizing the potential for new social affilia-
tion and thus responding by returning non-consciously mimicking ac-
tions. Measuring dogs’ empathy with an owner-completed ques-
tionnaire is also a controversial issue, although such surveys still seem
to be the most reliable, as behavioural tests are usually not sufficiently
4
Applied Animal Behaviour Science 223 (2020) 104916
realistic to evoke empathic-like behaviour (Szánthó et al., 2017).
It has also been raised (Silva et al., 2011) that yawning in the canine
contagious yawning paradigms might be an artefact resulting from the
stress of the experimental situation. Others (Romero et al., 2013),
however, found no indication of elevated stress during the contagious
yawning test based on heart rate measures. Future studies might
overcome these controversies by directly comparing subtly different
paradigms for both contagious yawning as well as stress indicators. In
the present study we also found that, especially during the post phase of
both conditions, the number of yawns was positively related to the
number of mouth licks, a commonly observed sign of stress and anxiety
(e.g. Pastore et al., 2011). Since mouth licks were not presented by the
experimenter in either of the conditions (and as their number was re-
lated to the number of dogs’ yawns) it is plausible to assume that
yawning was mostly also a manifestation of stress. Our results about the
effect of oxytocin point to the same direction, as it was found that,
especially during the test phase, oxytocin pre-treated dogs yawned
considerably less, a finding consistent with oxytocin’s stress relieving
effect (Neumann, 2002). If, on the other hand, oxytocin would have
induced a more empathetic response as hypothesised, the opposite ef-
fect should have been found (an increase in the number of yawns,
specifically in the yawning condition).
In sum our results provide evidence for the stress relieving effect of
oxytocin in a social situation, as well as shed further light on the con-
troversies of the commonly used contagious yawning paradigm.
Declaration of Competing Interest
We wish to confirm that there are no known conflicts of interest
associated with this publication and there has been no significant fi-
nancial support for this work that could have influenced its outcome.
We confirm that the manuscript has been read and approved by all
named authors and that there are no other persons who satisfied the
criteria for authorship but are not listed. We further confirm that the
order of authors listed in the manuscript has been approved by all of us.
We confirm that we have given due consideration to the protection
of intellectual property associated with this work and that there are no
impediments to publication, including the timing of publication, with
respect to intellectual property. In so doing we confirm that we have
followed the regulations of our institutions concerning intellectual
property.
We further confirm that any aspect of the work covered in this
manuscript that has involved either experimental animals or human
patients has been conducted with the ethical approval of all relevant
bodies and that such approvals are acknowledged within the manu-
script.
Acknowledgements
We thank the Family Dog Project (led by Ádám Miklósi) for pro-
viding laboratory space and materials. Financial support was provided
by the Hungarian Scientific Research Fund (OTKA FK128242 &
K128448), the BIAL Foundation (grant no 169/16) and the János Bolyai
Research Scholarship of the Hungarian Academy of Sciences.
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