A
test of the yawning contagion and emotional
connectedness hypothesis in dogs, Canis
familiaris
Sean J. O'Hara, Amy V. Reeve
School of Environment and
Life Sciences, University of Salford
The idea that yawning contagion in humans is
predicated on an empathetic response was
recently extended to dogs following the report
of cross-species contagious yawning in this
species (human-dogs). We attempted to replicate
contagious yawning in dogs and to investigate
what conditions promote yawning contagion. We
tested the emotional connectedness hypothesis,
which predicts that contagious yawning is
precipitated by exposure to (1) familiar model
(primary caregiver) and/or (2) similar model
(conspecific) stimuli, if contagious yawning is
empathy related. In our sample of family-owned
and rescue centre dogs we further predicted that
rescue centre dogs would yawn contagiously less
than owned dogs on the basis that they are more
lacking in emotional closeness and have more
weakly bonded relationships with their primary
care provider than owned dogs. We also
controlled for stress since stress can induce
yawning. While we found that five of 19 dogs did
yawn in response to an unfamiliar human yawning,
we were unable to confirm contagion. Our results
provide no support for empathy-based,
emotionally connected yawning contagion in dogs
and casts doubt on the recently documented
phenomenon of crossspecies contagious yawning.
We interpret our findings as showing that if
dogs are seen yawning contagiously then the
contagion must be explained on less cognitively
stringent grounds than empathy.
A contagion effect of yawning is well
established in humans. Even mention of yawning
can be sufficient to induce yawning in some
people (Provine 1986). Recent attempts to
understand what underlies the contagion have
focused on the suggestion that catching'
another's yawn may be an empathetic response
(e.g. JolyMascheroni et al. 2008; Arnott et al.
2009; Palagi et al. 2009) which, in turn,
potentially requires self-awareness (Platek et
al. 2003). According to this view, although
yawning is widespread in vertebrates, the
capacity to yawn contagiously is expected to be
limited to those species capable of inferring
the mental states of others and possessing a
concept of self.
The first empirical evidence for contagious
yawning in nonhuman subjects came from a study
of chimpanzees, Pan troglodytes (Anderson et al.
2004; see also Anderson & Matsuzawa 2006)
where the contagion effect was only marginally
lower than those reported for humans (Provine
1986; Platek et al. 2003); while a more recent
attempt to test for contagious yawning in
stumptailed macaques, Macaca arctoides, proved
equivocal, as although the macaques yawned
significantly more when exposed to conspecific
yawning stimuli than to controls, the authors
themselves acknowledged that they could not
exclude the possibility that some yawns were
tension induced (i.e. anxiety yawns), and not
real' yawns (Paukner & Anderson 2006). These
results are consistent with current thinking
that higher mental state attribution (e.g.
theory of mind) may be limited, among primates,
to humans and perhaps great apes (Call &
Tomasello 2008; Kaminski et al. 2008), species
known also to demonstrate empathy (de Waal 1996,
2008).
It was thus somewhat surprising then that
Joly-Mascheroni et al. (2008) recently claimed
that domestic dogs yawned contagiously and did
so at rates 12-32% higher than had been reported
for humans. The authors speculated that dogs
might possess rudimentary forms of empathy. This
view arises from suggestions that dogs may have
the capacity to empathize with humans since they
adjust their behaviour to coincide with human
behaviour (Topal et al. 1998), and, through the
process of domestication, dogs have acquired
exceptional abilities to decode human signals
through positive selection for this trait (Hare
& Tomasello 2005; Hare 2007). Dog
sensitivity to human directives could thus
potentially make them capable of interpreting
human emotions through behavioural cueing. A
recent similarly framed duplication of the dog
study by Harr et al. (2009) failed to replicate
Joly-Mascheroni et al's (2008) original
findings. One problem that dogged the macaque
study was the presence of tension yawns in the
sample. The same problem could not be ruled out
from Joly-Mascheroni et al's. (2008) dog study.
Harr et al. (2009) attended to this concern in
their study design by visually monitoring the
study subjects for behavioural indicators of
anxiety so that they could exclude 'tension'
yawns. They differed also by presenting their
stimuli visually on an LCD screen rather than in
person and they added a conspecific test
alongside the human yawn stimulus. Harr et al.
(2009) found very limited evidence for
contagious yawning in dogs. With such
conflicting results where do these findings
leave us?
Empathy research in humans asserts that
empathic tendencies are strongest or most likely
to arise as a function of familiarity (Kahlil
2002; Preston & de Waal 2002; de Waal 2008),
and Bates et al.'s (2008) analyses of the
emotions of wild elephants, Loxodonta africana,
suggest the same might be true for them. In a
recent study of contagious yawning in gelada
baboons, Theropithecus gelada, Palagi et al.
(2009) found that contagion was best predicted
by emotional closeness to the yawner. However,
although widely assumed, direct tests of the
familiarity hypothesis are rare.
Yoon & Tennie (2010) are also open to
the possibility that contagious yawning can
occur in vertebrates lacking a theory of mind.
They recently proposed that nonconscious
mimicry, and 'an even lower-level mechanism',
contagion, could also provide potential
explanations for contagious yawning (Yoon &
Tennie 2010, page e2) and outlined ways in which
to distinguish them. For example, mimicry would
occur in social contexts with preferred or
desirable partners and would be likely to
involve copying a wider range of behaviours than
are normally attributed to contagion. Contagion
under these criteria would apply if a full
response occurs in an agent even when only a
part of the full action was observed in the
target.
In our study we used domestic dogs. Through
cohabitation, dogs have acquired a putative
shared emotional connectedness to humans as well
as social and environmental proximities.
Archaeological dog burial evidence suggests
sharing our environment, dependence and
companionship have been features of the
human-dog relationship for ca. 8500 years (Morey
& Wiant 1992). During this time there has
been selection for levels of communication and
interaction with humans that are unparalleled in
any other nonhuman animal.
Here, we tested for a yawning contagion in
dogs. We built into our study design trials
using familiar and similar yawner stimuli
(owners and conspecifics, respectively) with the
prediction that dogs should be more likely to
yawn contagiously at (1) familiar humans (i.e.
owners) than unfamiliar humans (i.e. a female
researcher) and (2) to members of their own
species (conspecifics) than heterospecifics
(especially unfamiliar humans), if dogs are
showing familiarity/similarity-based
empathy-induced yawning contagion. We further
hypothesized that dogs in human-bonded
relationships (i.e. owned pets) should be more
likely to yawn contagiously than dogs living in
rescue shelters, which are potentially more
contact deprived and/or have more weakly bonded
relationships with their primary care
provider(s) (i.e. more lacking in emotional
closeness), if contagious yawning is empathy
related.
DISCUSSION
Our results show that if dogs yawn
contagiously, then they do so only at a low
level. Although we detected some contagion
effect in rescue centre dogs (less likely to
yawn at controls than owned dogs), we did not
find any evidence for contagion at the
individual level or in our overall sample. Our
tests of familiarity, similarity and bonding to
humans all failed to predict yawning and thus we
found little support for an empathy-related
yawning contagion in dogs. These results,
together with those of Harr et al. (2009), cast
further doubt on the recently documented
phenomenon of cross-species contagious yawning
reported by Joly-Mascheroni et al. (2008).
Importantly, while our trial conditions were
shown not to affect subjects' heart rates
adversely, they do hint at the possibility that
first exposure to a test condition elevates
heart rate. This suggests one-off testing
procedures might be susceptible to stressing
dogs if other systems are not put in place to
mitigate against this risk. Because stressing
has the potential to induce 'tension' yawns we
took several steps to ensure against this:
(owned) dogs were tested in familiar
surroundings: we used a single researcher who
was a female: the dog's companion was present
throughout: and each trial condition component
was limited to a fixed time. From our methods it
is not possible to distinguish whether
experimental order or first testing was
responsible for the higher heart rate in week 1:
however, we suggest the latter as experimental
order would predict the reverse effect: a higher
heart rate in week 2 when dogs were exposed to
the unfamiliar researcher rather than in week I
trials where dogs were tested with a familiar
person. Knowing baseline heart rates for each
subject could have given us clearer indications
of deviations from 'normal' levels; however, our
main interest here was simply to evaluate how
stressful or otherwise the trial condition
procedure might be on subjects and it was not
practical for us to gather baseline data.
Twenty-one of the 29 pet dogs (72%) in
Joly-Mascheroni et al's (2008) study yawned at
the unfamiliar human and none yawned in response
to the control. By this criterion the equivalent
percentage of yawning dogs here is 26% (five
dogs). Six of our subjects yawned in mouth
movement control trials and three of these did
not yawn when presented with yawn stimuli. This
to us suggests the lack of a contagion effect in
our sample. Furthermore, when dogs did yawn it
was unclear exactly to what they were
responding. Each trial condition prompted a
yawning response in two or more of our subjects
and the audio-only stimuli elicited more yawn
responses than any other condition. Familiarity
also did not induce more yawning than
unfamiliarity as was predicted. Indeed, the
trend was in the opposite direction: rescue
centre dogs yawned more at the unfamiliar
researcher. It has been argued that familiar
companions (Preston & de Waal 2002) and, in
particular, those with whom one has a close
emotional connection (Palagi et al. 2009) are
the most likely agents to promote contagious
yawning in a target. Dogs appear not to follow
this rule, which could suggest that dogs lack
the putative emotional connectedness impetus.
Humans form close and strong emotional bonds to
their dogs (Steward 1983) and dog owners might
often claim a mutual, emotionally bonded
relationship with their pets. However, the
notion that dogs show an empathic reciprocity
towards their owners has not been proven and the
emotional connectivity bond is likely to be only
unidirectional, from owner to dog. Thus, if
contagious yawning is underscored by empathy, a
lack of emotional connection on the part of the
dogs could account for our result. Testing
subjects in reverse, however, might yield
interesting results: that is might owners yawn
contagiously when exposed to their dog's
yawns?
Similarity also failed to induce yawning in
our dogs. Until recently, yawning contagion
studies tested subjects only against
conspecifics and reported contagion, but in the
present study just two dogs responded only to
the conspecific stimulus (10.5%) and not the
control stimulus. There are limitations that we
acknowledge. First, we used an unfamiliar
conspecific model (as have other studies).
Second, we used a video recording played back on
a laptop screen, which may not be optimal for
dogs. While this method has been successfully
pioneered in human and nonhuman primate studies
(and LCD playback has been successfully applied
in other dog studies e.g. Pongrácz et al.
2003), this form of playback is potentially less
ecologically relevant for dogs. Furthermore, our
dogs might have been perceptually disadvantaged
as, unfortunately, we did not compensate for
dogs' faster eye rate flicker. Coile et al.
(1989) have suggested an equivalent playback to
what humans see on a laptop screen requires the
flicker rate of the screen to be adjusted
upwards of 70-80 Hz. One way future trials could
address both similarity and familiarity issues
is by using subjects from homes with more than
one dog.
If yawning in dogs is not empathy related
but a low level of yawning contagion is
observed, what might account for it? Yoon &
Tennie (2010) posited a further alternative for
catching another's yawn: nonconscious mimicry,
also referred to as priming by response
facilitation (Byrne 1994, 2002; Hoppitt et al.
2007). The ability to imitate another's
behaviour, motivated by the desire to promote
affiliative interaction in social contexts
(Chartrand & Bargh 1999), might explain some
cases of contagious yawning (Yoon & Tennie
2010). Such social behaviour copying is well
known in humans when attempting to establish a
rapport with another and could be adaptive (e.g.
van Baaren et al. 2004). In our study it was the
rescue centre dogs that yawned most at human
models, and mostly at the unfamiliar one.
Nonconscious mimicry could explain this
observation: when attention is directed towards
rescue dogs by a newly arrived human stranger,
contact-deprived dogs may recognize the
potential for new social affiliation and thus
respond by returning nonconscious mimicking
actions. Overall, however, domesticated dogs may
have a reduced response to such priming as they
have become less adult-like in form, psychology
and behaviour, at least relative to wild canids
such as wolves, Canis lupus. An absence of
contagious yawning in young children (Anderson
& Meno 2003) potentially reflects the fact
that they, as followers', have less of a
requirement to be sensitive to synchronizing and
coordinating needs within their social unit
(Palagi et al. 2009). The same may be true for
dogs. We suggest one way to test this hypothesis
is to investigate yawning contagion in wild
social-living canids with fully adult
personalities, comparing adult and young animal
responses to peer yawning. Furthermore, the
communicative nature of the social contagion
hypothesis can be tested by observing the
regulating effect of yawning on synchronized
group behaviour.
Contagion studies are providing productive
gateways to helping illuminate social cognition
and contagion is an emerging field of research
(Yoon & Tennie 2010). In our contagion study
we found little evidence of cross-species
contagious yawning in dogs and our results left
the emotional connectedness hypothesis
unsupported. Furthermore, the variation we
observed in responsiveness among the different
groups of dogs corresponds with the findings of
UdelI et al. (2010) where shelter dog
performance differed from owned dog performance
and lends weight to their caution against
regarding the dog population as a homogeneous
grouping and extrapolating inferences to all
dogs after testing only owned dogs. We conclude
that if dogs yawn contagiously then the
releasing mechanism appears unrelated to
empathy. We think it seems most unlikely that
yawning contagion is limited to only those
species capable of inferring the mental states
of others and possessing a concept of self; and
there is no compelling case to suggest a unitary
underlying releasing mechanism across all
vertebrates. For dogs, we have outlined
alternative approaches to shedding light on this
problem and we encourage researchers to shift
focus on to social-living canids and other
carnivores.
