In humans, the susceptibility to yawn
contagion has been theoretically and empirically
related to our capacity for empathy. Because of
its relevance to evolutionary biology, this
phenomenon has been the focus of recent
investigations in non-human species. In line
with the empathic hypothesis, contagious yawning
has been shown to correlate with the level of
social attachment in several primate species.
Domestic dogs (Canis familiaris) have also shown
the ability to yawn contagiously. To date,
however, the social modulation of dog contagious
yawning has received contradictory support and
alternative explanations (i.e., yawn as a mild
distress response) could explain positive
evidence.
The present study aims to replicate
contagious yawning in dogs and to discriminate
between the two possible mediating mechanisms
(i.e., empathic vs. distress related response).
Twenty-five dogs observed familiar (dog's owner)
and unfamiliar human models (experimenter)
acting out a yawn or control mouth movements.
Concurrent physiological measures (heart rate)
were additionally monitored for twenty-one of
the subjects. The occurrence of yawn contagion
was significantly higher during the yawning
condition than during the control mouth
movements. Furthermore, the dogs yawned more
frequently when watching the familiar model than
the unfamiliar one demonstrating that the
contagiousness of yawning in dogs correlated
with the level of emotional proximity. Moreover,
subjects' heart rate did not differ among
conditions suggesting that the phenomenon of
contagious yawning in dogs is unrelated to
stressful events. Our findings are consistent
with the view that contagious yawning is
modulated by affective components of the
behavior and may indicate that rudimentary forms
of empathy could be present in domesticated
dogs.
Introduction
Contagious yawning, or yawning after seeing
or hearing another individual yawning, is an
intriguing phenomenon, and the underlying
mechanisms and functions remain unclear
[1]. In humans, contagious yawning
affects 45-60% of healthy adults, and it has
been demonstrated experimentally by exposing
individuals to video sequences showing yawns
[2,3]. Although some authors have
suggested that contagious yawning is a response
to innate releasing mechanisms [2,4],
more recent hypotheses have focused on its
potential role in communication, social
interactions, and empathy [1,5,6].
Evidence from clinical, psychological,
behavioral and neurobiological studies has
supported this latter view. In humans, yawning
when seeing other people yawn is associated with
activations in neural networks responsible for
empathy and social skills [7-9].
Furthermore, people who performed better on
tests of self-recognition, theory of mind and
empathy were more susceptible to yawn
contagiously [1,3]. A recent
naturalistic study has also demonstrated that
the socialemotional bond between individuals,
associated with empathy [10] affects the
occurrence, frequency, and response latency of
yawn contagion in humans [11].
Additionally, the contagious effect of yawning
seems to be impaired in subjects suffering from
empathy disorders, such as autism
[12,13].
The evidence supporting the link between
contagious yawning and empathy is not specific
to humans. Chimpanzees (Pan troglodytes),
bonobos (Pan paniscus) and gelada baboons
(Theropithecus gelada) have been reported to
yawn contagiously when they observe a
conspecific yawning [14-19]. Similarly
to humans, in both species the closer the social
bond between individuals, the more likely they
would yawn when the other yawned
[16-18]. These findings are consistent
with the empathic-based hypothesis of contagious
yawning since in both humans and animals empathy
is biased toward individuals who are more
similar, familiar, or socially close
[10,20].
Outside the primate order contagious yawning
has received far less attention. It has been
demonstrated or suggested only in one species of
birds (budgerigars, Melopsittacus undulates;
[21]) and in the domestic dog (Canis
familiaris; [22-26]). Intriguingly, the
only attempts to test the empathic-based,
emotionally connected contagious yawning have
been done in dogs with contradicting
findings.
The first study investigating contagious
yawning in dogs showed that a high proportion of
the subjects (72%) yawned after observing a
human experimenter acting a yawn [22].
The authors argued that since dogs are unusually
skilled at reading human social and
communicative signals [27] there is the
potential that dogs may also have developed the
capacity for empathy towards humans, and thus
being able to catch human yawns. Following a
similar procedure, Madsen & Persson
[26] confirmed that dogs are able to
yawn contagiously but failed to demonstrate that
the emotional closeness with the model affected
the strength of contagion. Another recent study,
however, has provided data that support the
empathic-based explanation of contagious yawning
in dogs using auditory stimuli [25].
Silva et al. [25] explored dogs'
reactions to the sound of a human yawn finding
that not only dogs yawned contagiously when they
heard a human yawning, but that they yawned more
at familiar than unfamiliar yawns, thus
following the same familiarity bias as
empathy.
On the other hand, the other two studies
investigating yawn contagion in dogs have found
very limited evidence of the phenomenon itself
or of the linkage between yawn contagion and
empathy [23,24]. In these studies, dogs
did not yawn more frequently when exposed to
yawn stimuli than when exposed to control ones,
nor were their responses affected by their
social bond with the yawner. Instead, the
authors suggested that if dogs yawn contagiously
then the contagion might rely on less
cognitively stringent grounds than empathy
[24]. Although it is likely that the
different methodologies used in each study
contributed to the discrepancy between results
(e.g., the use of video vs. live presentation of
stimuli; human vs. dog models; see
[28]), the current evidence do not allow
firm conclusions to be drawn as to whether or
not dogs are able to yawn contagiously or
whether the phenomenon is empathy-related. An
additional problem when examining the current
evidence on dog contagious yawning is that none
of the previous studies allow alternative
hypotheses to be dismissed. For instance,
spontaneous yawning has been associated with
psychological tension or mild stress in several
animal species including dogs [29,30].
Thus, it could be possible that dogs yawn more
frequently during a particular condition simply
because the stimuli presented increase their
anxiety (e.g., hearing, but not seeing, their
owners). A similar interpretation was given to
apparent contagious yawning in stumptail
macaques (Macaca arctoides) since both yawning
and selfscratching, which is considered an
indicator of tension in primates [29],
increased when the monkeys were exposed to a
video of conspecifics yawning [31]. Some
attempts have been made to address this issue in
dog's experiments. In some studies the authors
visually distinguished ''tension'' yawns from
''natural'' yawns according to the yawn
intensity, or to the association with behavioral
indicators of anxiety [23,25,26].
However, none of these studies provided an
objective definition of yawn intensity that
could be replicated by other researchers, nor
did they report quantitative data on behavioral
indicators of anxiety that could be compared
across conditions. Additionally, in one study an
acoustic stethoscope was used to take heart rate
measures at three time points throughout the
experimental session [24]. However, the
use of a stethoscope to measure stress
inherently disturbs the animals, thereby
affecting their stress levels and making
accurate assessment of stress difficult. Thus,
no study that has so far reported contagious
yawning in dogs could rule out the
stress-response hypothesis.
If contagious yawning indeed is related to
the capacity for empathy, it could became a
powerful tool to explore the root of empathy in
animal evolution by studying cross-species
contagious yawning. Therefore, there is a need
for further experimentation on this issue,
especially in non-primate species. The current
study explores whether contagious yawning can be
observed in the domestic dog. In particular, we
tested whether dogs yawn when they see a human
yawning and whether this response is similar to
contagious yawning observed in humans and other
primates or is due to tension or anxiety.
Telemetric monitoring of subjects' heart rate
(HR) and heart rate variability (HRV), which has
been successfully used as a measure of autonomic
regulation of cardiac activity to assess stress
and well-being in companion animals over the
last decade [32], was used to measure
psychological changes and anxiety states in dog
throughout the experimental sessions.
Additionally, we tested the hypothetical link
between contagious yawning and empathy. We
hypothesized that if contagious yawning is
related to dog's capacity for empathy, then
contagious yawning should follow the same
familiarity bias as empathy, with dogs yawning
more often at familiar than unfamiliar
yawns.
Discussion
The present study demonstrates that the
presentation of human yawning is able to elicit
yawns in domestic dogs and that the social bond,
associated with empathy [10], mediates
its occurrence. Interestingly, the physiological
measures (i.e., HR and HRV) recorded
continuously during the experimental sessions
rule out the possibility that anxiety per se may
have accounted for the observed pattern of
yawning responses. Although this finding
conflicts with previous studies on dog
contagious yawning [23,24], it
corroborates the evidence reported by
Joly-Mascheroni et al. [22], Silva et
al. [25], and Madsen & Persson
[26]. The discrepancy between results on
dog contagious yawning is likely explained by
the use of different methods of experimentation.
For example, while studies using live models
have been able to elicit contagious yawns in
dogs [22,26]; Harr et al. [23]
and O'Hara & Reeve [24] failed to
find such effect when they used video clips or a
combination of both. Although some studies have
successfully applied video or LCD playbacks to
present stimuli to dogs [42], it is
possible that videos are less ecologically
relevant to dogs, and thus they attend
differently to the videos and the live models.
Another important methodological difference
between studies is the type of sensory modality
presented to the subjects. A yawn may include
different sensory modalities (i.e. visual or
auditory) and some studies have used only
auditory cues (e.g. [25]), only visual
(e.g. [23]) or a combination of both
(e.g. [22], this study) with different
results. However, before any conclusion could be
drawn on which sensory modality elicited more
contagious yawns in dogs; further investigations
should explore the prevalence of each modality
as well as the degree of individual variability
to the sensibility to each.
It is also noteworthy that the expressions
selected as control differ among studies, from
silent mouth movements [22,23,26] to the
sound of a yawn [24]. There is no
consensus about what makes for the ideal
control, and several facial expressions (e.g.,
smiles, silence mouth movements,
species-specific expressions) seem to turn up
baseline levels of yawning [28].
However, it has been documented that the mere
sound of a yawn can be sufficient to elicit
yawning in humans [8,12], gelada baboons
[16], and dogs: [25], and thus
it seems unsuitable as a control stimulus.
Furthermore, in the dog study using yawn sound
as a control, the authors themselves stated that
the ''audio-only stimuli reported more yawn
responses than any other condition''
([24], pp. 339), suggesting that a high
proportion of dogs might have actually yawned
contagiously during their study (11 out of 19
dogs yawned in response of the visual or
auditory yawn stimuli but not at the mouth
movements, from Table 3 in O'Hara and Reeve
[24]). As Campbell and de Waal
[28] suggested, further studies should
focus on the impact of methodological variations
on contagious yawning to facilitate comparisons
across studies.
It could be argued that the silent mouth
movements used as control stimuli in the present
study could have the potential to impact our
results. That is, the sound of a yawn could have
drawn dogs' attention to a socially relevant
stimulus (i.e. the mouth movements) during the
yawning condition but not during the control
one, since the control stimulus was silent.
However, it has been reported that the
perception of the eye region of yawning people
is a potent stimulus in eliciting yawning, while
yawning mouth is not [4]. Moreover,
recent studies on children with autism spectrum
disorder, who tend to spontaneously fixate more
to the mouth than to the eyes when watching
dynamic facial stimuli [43], repeatedly
failed to show contagious yawning [12]
except when they were instructed to fixate on
the yawning eyes [44]. Thus, it seems
unlikely that the possible more fixation to the
mouth during the yawn condition increased dogs'
probability to yawn contagiously. On the other
hand, it could be also argued that a combination
of mouth movements and sound stimuli could have
served as a releasing stimulus in the
experimental condition but not in the control
one, since the sound was not present. However,
the empirical evidence from human and non-human
animals shows that the presence of acoustic cues
are not required to evoke a yawn since the mere
view of a (silent) yawn is sufficient to elicit
contagious (e.g. [11,14,15,21]).
Furthermore, using the same general design of
the present experiment an additional group of
dogs (N =12, 7 females, 5 males, mean age =51.9
months) were tested using open-mouth movements
with vocalization as control stimuli (an ''a''
sound similar to the one produced during the
yawning condition). Preliminary results show
that while 33.3% of the dogs (N = 4) yawned
during the yawning condition, none of the
subjects did yawn during the control condition
(McNemar Chisquare test: P =0.045) suggesting
that a combination of mouth movements and sounds
per se does not work as a releasing stimuli for
yawn contagion in dogs.
It has been suggested that contagious
behaviors function to coordinate activities in
group living animals [45,46]. Therefore,
it seems reasonable that the susceptibility to
yawn contagiously is not specific to humans or
primates but shared with other social species,
since synchronizing behavioral activities has
undoubted adaptive value for group-living
animals. The contagious effect of human yawning
on dogs may be interpreted in line with this
argument: a communicative signal that helps to
synchronize human-dog activities. Although there
is anecdotal evidence that human yawns might
produce similar, synchronous states in dogs
[26], this hypothesis remains untested
and further studies on the social function of
contagious yawning in dogs are needed. Most
studies on yawn contagion in non-human animals
have demonstrated the intra-specific effect of
yawn contagion (chimpanzees: [14,17,19];
bonobos: [18]; gelada baboons:
[16]; stumptailed macaques:
[31]; budgerigars: [21]).
However, studies on dogs have only been able to
demonstrate cross-species (humandog) contagious
yawning. Dogs are unusually skilled at reading
human social and communicative behaviors
[47]. They can use human gaze and
pointing to locate hiding food [27,48],
they respond to the attentional state of humans
[49], and they can imitate human actions
[50]. Thus, it is not surprising that
they are also able to 'catch' human yawns.
However, it is puzzling that dogs have not
responded in a similar way to the yawns of
conspecifics. During domestication, dogs have
become selected to maintain attention towards
humans, which seems to be critical for dog-human
communication and social learning [51].
Thus, it is possible that dogs are predisposed
to respond more intensively, or only, to human
social cues rather than conspecifics' ones.
However, observations of spontaneous social
behavior of dogs [52-54], as well as
experimental evidence on social cognition
[55], do not support this hypothesis.
Dogs use visual communicative signals, from body
position to expressive use of eyes, lips, and
teeth [52], and are able to use visual
attention cues when interacting with other dogs
[54]. Thus, it is also possible that the
capacity for contagious yawning evolved as an
adaptation for communication with conspecifics,
and that this capacity was later transferred to
dog-human interaction. The current experimental
evidence, however, does not allow us to
discriminate between these two possible
explanations, since different methodology has
been used to test intra and inter-species
contagious yawning (i.e., videoed stimuli of
conspecifics vs. human live demonstrators). The
use of a standardized methodology in further
investigations would be critical to understand
dogs' reactions to human and dog stimuli, which
in turn will help us to gain insight into the
evolutionary origin of contagious yawning.
An important implication of the present
findings is that the contagion effect of human
yawns in dogs is modulated by affective
components of the behavior. Dogs yawned more
frequently at the familiar yawns than at the
unfamiliar, which is consistent with the
observation that empathy is more pronounced the
stronger the social attachment between
individuals [10,20]. Preston and de Waal
[10] presented a theoretical model in
which empathy is linked to all facilitation
behaviors that rely on perception-action,
including imitation and coordination, but also
unconscious motor mimicry. According to this
model, contagious yawning would be underscored
by empathy and therefore individuals with a
close emotional connection with the observer
would be the most likely individuals to elicit
contagious yawning [10,11,16,17].
Through close cohabitation, dogs are able to
establish close bonding and attachment with
people. For instance, dogs show selective
responsiveness to their owners and exhibit a
range of attachment behaviors, i.e., search and
proximity seeking behaviors, when separated from
them [56]. Hence, the observed effect of
familiarity on dogs' contagious yawning probably
reflects that positive affect may regulate
unconscious motor mimicry in the domestic dog.
Some authors have suggested that familiarity
bias would be also expected if an even
lower-level mechanism underlies the phenomenon
of contagious yawning [57]. According to
this view, a yawn would be a special stimulus
that ''serves as a releaser to the unlearned
behavior of others'' [58]. In this
scenario, a familiarity bias would be explained
as a consequence of the different levels of
attention of individuals toward different group
members. That is, since subjects usually pay
closer attention to close affiliates, attention
bias rather than empathy differences would be
responsible for the observed pattern. However,
the studies that have controlled for levels of
attention in animal studies do not support this
view [17,25]. Campbell & de Waal
[17] and Silva et al. [25]
measured the total amount of time subjects
looked to the source of the stimuli (i.e. screen
or speakers) finding that either there were no
differences between familiar and unfamiliar
conditions [25] or that subjects
attended more to the unfamiliar yawns but yawned
more to the familiar yawns [17].
Finally, in the present study a significant
familiarity bias was also found after having
controlled for the possibility to perceive the
stimulus (i.e. the stimuli were presented only
when the subject established eye contact with
the model). Although these results cannot
exclude the possibility that attention might
have an effect on the responses of the subjects,
they rule out the possibility that attention per
se explains the observed pattern.
The importance of the social bond in shaping
yawn contagion has also been demonstrated in
humans [11], chimpanzees [17];
bonobos [18] and geladas baboons
[16], with all studies reporting an
association between the degree of bonding and
the occurrence, rate, and/or latency of yawn
contagion. The studies examining the empathic
basis of contagious yawning in dogs have
produced conflicting results, though. While two
studies found an association between contagious
yawning and empathy, with dogs yawning more at
familiar than unfamiliar yawns [25]; two
other studies failed to find such association
[24,26]. The problematic control stimuli
used in O'Hara & Reeve's study [24]
(see above) raise questions about the
interpretation of their negative results. On the
other hand, Madsen & Persson [26]
examined the ontogeny of contagious yawning, and
their target sample was juvenile dogs (mean age=
7.23 months). Human and non-human primates show
a developmental increase in susceptibility to
yawn contagiously (humans: [6,13];
chimpanzees: [14]; gelada baboons:
[16]) which is suggested to reflect the
developmental process of social cognitive
skills, including the ability to identify
other's emotions [6]. Indeed, Madsen
& Persson [26] found a similar
developmental effect with only dogs above 7
months evidencing a contagion effect. Thus, it
is possible that the social modulation of
contagious yawning in dogs is more pronounced at
older ages. In our study, only dogs older than
12 months of age were tested and a significant
effect of the social attachment on contagious
yawning was found. More data are clearly needed,
and further studies could benefit from including
a wider range of ages to clarify not only the
empathic bias of contagious yawning, but also to
better understand the social function of yawning
in dogs.
Our findings go further in supporting the
empathic bias of contagious yawning in dogs,
since our methodological procedure allowed us to
discard the alternative hypothesis that yawn
responses were elicited by any kind of stressful
event. In dogs, high frequencies of spontaneous
yawns have been associated with middle tension
states [30]. Thus, even if Silva et al.
[25] found an effect of familiarity on
contagious yawning (i.e., dogs yawned more
frequently when they heard their owners yawning
than when they heard an unfamiliar person
yawning), their results could be interpreted in
line with the tension hypothesis: hearing, but
not seeing, their owners could produce
uncertainty in the dogs and consequently evoke
''tension yawns''. In our study, telemetric
measures of dogs' HR and HRV did not differ
significantly between conditions, suggesting
that the familiarity bias detected in this study
was not due to changes in the subjects' anxiety
levels, but rather it reflects the modulating
effect of the affective components of contagious
yawning. Since the demonstration of the
occurrence of contagious yawning in non-human
species does not necessarily warrant that the
underlying mechanism of the phenomenon is shared
with human yawn contagion, further research
should test for alternative hypothesis and
control for factors that are known to affect the
occurrence of yawning in animals.
