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- -Gallup
A, Wozny S. Interspecific Contagious Yawning
in Humans. Animals (Basel)
2022;12(15):1908.
-
- Abstract
- Interspecific contagious yawning (CY),
whereby yawns from one species trigger yawning
in different species, has now been reported
across various taxa. This response to human
yawning appears common among animals in
captivity and has been interpreted as an
empathic response towards human
handlers/caregivers. A recent study found that
humans also display interspecific CY, though
this response was not modulated by proxies of
empathic processing (i.e., phylogenetic
relatedness or social closeness to the animals).
-
- Here, the authors explored this relationship
more explicitly by assessing how interspecific
CY to yawns from common household pets relates
to self-reported empathic concern. Participants
(N = 103) completed a survey measuring empathic
concern and then reported on their yawning
behavior following exposure to a control
condition or yawning images either from
domesticated cats or domesticated dogs.
-
- The results provide further evidence for
interspecific CY in humans, but empathic concern
was negatively predictive of this response.
There was also no sex difference in
interspecific CY, though when comparing the
sexes across CY conditions, women reported a
higher frequency of yawning in response to dog
yawns, and men reported a higher frequency of
yawning in response to cat yawns. Overall, these
findings do not support a strong connection
between interspecific CY and empathy or
emotional contagion.
-
- Résumé
- La contagion interspécifique des
bâillements (CY), par lequel les
bâillements d'une espèce
déclenchent des bâillements
d'autres espèces, a été
signalé dans divers taxons. Cette
réaction aux bâillements humains
semble commune chez les animaux en
captivité et a été
interprétée comme une
réponse empathique envers les humains qui
les manipulent ou les soignent. Une étude
récente a montré que les humains
présentent également un CY
interspécifique, bien que cette
réponse ne soit pas modulée par
des indicateurs de traitement empathique
(c'est-à-dire la parenté
phylogénétique ou la
proximité sociale avec les animaux).
-
- Ici, les auteurs ont exploré cette
relation de manière plus explicite en
évaluant comment le CY
interspécifique aux bâillements des
animaux domestiques est lié à la
préoccupation empathique
auto-déclarée. Les participants (N
= 103) ont répondu à une
enquête mesurant la préoccupation
empathique et ont ensuite rapporté leur
comportement de bâillements après
avoir été exposés à
une condition de contrôle ou à des
images de bâillements provenant soit de
chats domestiques, soit de chiens domestiques.
-
- Les résultats fournissent des preuves
supplémentaires de l'existence d'un CY
interspécifique chez l'homme, mais la
préoccupation empathique était un
facteur prédictif négatif de cette
réponse. Il n'y avait pas non plus de
différence entre les sexes dans le CY
interspécifique, bien que lorsque l'on
compare les sexes entre les conditions du CY,
les femmes ont rapporté une
fréquence plus élevée de
bâillements en réponse aux
bâillements de chiens, et les hommes ont
rapporté une fréquence plus
élevée de bâillements en
réponse aux bâillements de chats.
Dans l'ensemble, ces résultats ne
confirment pas l'existence d'un lien
étroit entre le CY interspécifique
et l'empathie ou la contagion
émotionnelle.
- Introduction
- Contagious yawning (CY) is a distinctive
pattern of behavioral coupling that occurs when
the mere detection of yawns by others elicits
the automatic and reflexive tendency for an
observer to yawn. Yawning can be reliably
elicited in this way in humans using images,
videos, or audio clips of yawning
[1&endash;5], though there is
considerable variability in this response
[6,7]. While the first experimental
demonstration of CY in a nonhuman animal was
published less than two decades ago [8],
evidence for CY is now present for a growing
number of social vertebrates (for a review, see
[9]). Various theories have been
proposed pertaining to the biological
significance of CY [10], with recent
evidence indicating a role in facilitating motor
synchrony and enhancing vigilance in groups
[11,12].
-
- Independent of its ultimate function, one
view that has gained considerable traction in
the scientific community is that CY represents a
primitive form of empathic processing, i.e., the
tendency to yawn after detecting this action in
another could reflect a form of emotional
contagion. This idea, which could explain the
distinctive individual differences in CY across
studies, was initially proposed in a monograph
by Lehmann [13] and further elaborated
within the perception&endash;action model of
empathy [14,15]. Empirical support for a
connection between empathy and CY was first
published by Platek et al. [6], and this
continues to be a prevailing view in the current
literature [16]. However, systematic
reviews of the studies examining the linkage
between CY and empathy have shown that the
totality of evidence is rather mixed and
inconsistent [17]. Alternatively, CY
could instead represent a simple feature of
behavioral contagion or facial mimicry
[18,19] that would show a statistical
correlation to markers of empathy or emotional
contagion without a causal relation. For
example, one key issue in this debate is that at
a proximate level CY requires the detection of
yawns in others, and social attention and
empathy are often difficult to disentangle
[20,21]. Thus, while the use of CY as a
potential indicator of empathy or emotional
contagion is intriguing, a direct linkage
remains unclear.
-
- Recently, interspecific CY, whereby yawns
from one species trigger a member of a different
species to yawn, has been examined in relation
to empathy. The first evidence for interspecific
CY came 15 years ago from a study showing that
the overt display of human yawning was
sufficient to induce a similar response among
domesticated dogs [22]. This initial
report garnered considerable attention and led
to numerous follow-up studies designed to
explore the interspecific CY/empathy connection.
If this cross-species facial mimicry was
enhanced by empathy, it had been predicted that
dogs should respond more strongly to yawns from
caregivers/owners where there was an existing
social bond or attachment. This view was based
largely on a 2011 study of chimpanzees, whereby
an ingroup bias for CY was observed and
interpreted as a sign of empathy [23].
The authors of this work suggested that since
humans show ingroup biases for empathy for pain
[24&endash;26], similar biases in CY
could be used as a measure of affective empathy.
Overall, the evidence in support of this effect
among dogs is mixed [27&endash;29], and
a recent study, including a meta-analysis of
this literature, concluded that human-initiated
CY in dogs was, in fact, not a signal of empathy
[30].
-
- Studies on other captive species, however,
have reported more consistent familiar-
ity/ingroup biases when it comes to
interspecific CY. In line with the view that CY
may reflect a form of empathy or emotional
contagion, familiarity has been shown to enhance
both intra- and interspecific CY among nonhuman
primates [23,31,32]. In one study on
chimpanzees, subjects responded with CY to
stimuli from familiar humans (i.e., researchers
and husbandry staff) and ingroup conspecifics
but not to outgroup chimps or unfamil- iar
members from other species [31]. A more
recent and very similar study on captive
red-capped mangabeys produced the same basic
findings: subjects showed a higher CY response
to familiar human caretakers and conspecifics
compared to unfamiliar individuals from across
three species [32]. In addition, one
study on African elephants found that
individuals responded with CY to yawns from
familiar human handlers [33], though no
comparisons were made with unfamiliar
humans.
-
- To further examine this relationship, Gallup
and Wozny [5] investigated whether
humans also display interspecific CY. Using an
online format, participants were shown a series
of yawning stimuli from one of the following
categories: fish, amphibians, reptiles, birds,
non-primate mammals, great apes, and a
compilation of common household pets (including
an equal representation of domesticated cats and
dogs). Given that prior studies have shown that
people display greater empathy and attachment
towards both more closely related species
[34&endash;36] and domesticated animals
that are commonly kept as pets
[37&endash;39], it was predicted that
interspecific CY would be enhanced by
phylogenetic proximity and domestication/social
closeness. The findings provided clear evidence
for interspecific CY when compared to the
control images, with 69% of participants
reporting interspecific CY. Yet, while it was
expected that yawns from great apes
(chimpanzees, gorillas, and orangutans) and
common pets (cats and dogs) would elicit the
greatest response, this was not the case.
Consequently, these findings did not support the
purported connection between interspecific CY
and empathy or emotional contagion in humans and
instead suggest that the mechanisms governing CY
are generalized. Importantly, Gallup and Wozny
[5] included a task that ensured
attention towards the yawning stimuli during
testing. Given CY is a reflexive and automatic
response, it seems that the detection of yawns,
independent of the taxa represented, may be
sufficient to generate this response. However,
like previous works, overt measures of empathy
or attitudes towards animals were not obtained
in this experiment. In addition, subsequent
exploratory analyses from this open-access
dataset indicated that women may be more likely
to yawn in response to yawns from a compilation
of CY stimuli from domesticated cats and dogs.
While sex differences in CY are rarely observed
(for a review, see [40]), and an overall
effect of gender was not found. In general, it
has been argued that a female bias in CY would
be consistent with links to empathy and/or
emotional contagion [41]. Thus, future
research could help clarify this picture by
assessing whether this interaction is
reproducible.
-
- The current study served as a direct
follow-up to Gallup and Wozny [5],
providing a more explicit examination of the
relationship between interspecific CY and
empathy in humans. We sought to examine whether
validated measures of empathic concern and
animal attitudes predicted interspecific CY to
common household pets while controlling for
attention. Empathic concern was selected because
it has previously been shown to correlate with
animal attitudes [42,43] and
intraspecific CY in humans [44], while
measures of cognitive empathy (i.e., reading
emotions and perspective-taking) tend to be less
correlated with animal attitudes and have more
often failed to predict CY in humans
[45&endash;47]. Given that dogs have
undergone a long period of domestication that
involved distinct forms of social communication
and cooperation with humans [48] and
that people tend to perceive both human and dog
facial expressions in a similar manner
[49], we examined interspecific CY
separately to domesticated cats and dogs.
Moreover, based on exploratory analyses showing
a potential female bias in interspecific CY to
common household pets, we aimed to replicate
this effect of participant gender. If empathy
was related to interspecific CY, empathic
concern should positively predict this behavior,
and perhaps women would show a greater response
[41]. If interspecific CY is
generalized, due to it being more of an
automatic and reflexive response, merely
attending to the animal stimuli should elicit
yawns independent of empathic concern or
gender.
-
- Discussion
- The current findings provide further
evidence of interspecific CY in humans, repli-
cating previous research [5]. While the
magnitude of this effect was relatively limited
for yawning images of domesticated dogs, showing
up only when examining CY frequency, there was a
larger and significant effect observed within
the cat yawning condition across both the binary
and frequency models. This difference in
interspecific CY when viewing images of cat and
dog yawns was not expected given the coevolution
of human&endash;dog bonding and social
communication [48,49,61]. Nonetheless,
these results, coupled with the report of Gallup
and Wozny [5], provide strong support
that, in general, yawns from common household
pets can reliably elicit CY among humans.
-
- A primary objective of the current study,
outside of replicating interspecific CY in
humans, was to more explicitly assess how this
response varied as a function of individual
differences in a self-reported measure of
affective empathy. To date, prior studies in
this area have only used proxies for empathy,
focusing on features pertaining to the
familiarity (e.g., human handlers/caregivers) or
phylogenetic closeness of the interspecific
stimuli. Here, we had participants complete the
empathic concern subscale of the IRI
[54] as well as the five-item version of
the Animal Attitude Scale (AAS-5) [55]
to assess how this predicted interspecific CY.
Although the reliability of the AAS-5 was poor,
the internal consistency of the empathic concern
scale was acceptable and included in the
analysis. Moreover, this measure of affective
empathy towards humans has previously been shown
to predict attitudes towards animals
[42,43]. Despite people generally
showing high levels of empathy towards
domesticated cats and dogs
[37&endash;39], this measure was not a
positive predictor of interspecific CY. In fact,
participants with greater empathic concern were
less likely to yawn during testing, casting
doubt on the view that interspecific CY is
strongly linked to features of empathy or
emotional contagion [16,23,31,32].
Together, these results add to a growing number
of psychological studies providing mixed support
for a connection between CY and empathy when
using self-reported trait measures (reviewed by
[17]).
-
- Based on exploratory analyses of the dataset
from Gallup and Wozny [5], a secondary
objective of the current study was to further
examine the role of gender in interspecific CY
among humans. Consistent with most studies in
the literature, the current results revealed no
overall gender bias in interspecific CY.
However, a significant gender _ stimulus
condition interaction emerged whereby women
reported a higher frequency of CY to dog yawns,
and men reported a higher frequency of CY to cat
yawns. Given that this particular result was not
anticipated, we can only speculate as to the
mechanisms governing this effect. Prior work has
shown, for example, that interactions with pet
dogs tend to enhance oxytocin (OT) among female
owners, while they lead to no change or
decreases in OT among men [62,63].
Moreover, in contrast to human interfaces with
dogs, a recent study including only women found
no overall increase in OT following interactions
with pet cats [64]. Thus, one potential
explanation for the female bias in CY to dog
stimuli could be differences in OT among
participants. However, we are skeptical of this
possibility for at least two reasons. First,
while OT has been implicated in CY
[65,66], studies that have manipulated
OT via intranasal administration have failed to
yield support for this connection
[57,67]. Second, the studies measuring
changes in human OT levels were undertaken
following real-world interactions with bonded
cats and dogs (i.e., pets and their owners), and
it seems unlikely that the current procedures of
merely viewing static images of unknown animals
would elicit similar neurochemical changes.
Nevertheless, this represents a potentially
fruitful area for future research to
explore.
-
- Consistent with similar online studies
examining both intra- and interspecific CY in
humans [5,7], indices of arousal/fatigue
were the strongest predictors of self-reported
yawning in the current sample. As expected,
sleep duration the night before was nega- tively
correlated with interspecific CY, while
tiredness during the study was positively
correlated with this response. These findings
align with a large body of comparative evi-
dence suggesting that circadian rhythms and
internal temperature drive yawning behavior
(reviewed by [9]).
-
- While the current research serves as a
replication of interspecific CY in humans and
furthers our understanding of the factors
contributing to this response, this study has
several limitations. First, no measure of pet
ownership was captured from the participants.
Prior studies suggest that just over half of US
households have a pet, with the majority
reporting dog and/or cat ownership [68],
and thus further work could assess how living
and bonding with a pet cat or dog contributes to
interspecific CY in these conditions. Another
limitation to this study was the relatively
small sample of participants, which was reduced
primarily due to attentional checks. However,
the attentional measures obtained during testing
remains a strength of this study, as they
ensured (1) high quality data and (2) that
visual attention was directed towards the
yawning stimuli. That said, the manipulation was
not robust, particularly for the binomial
outcome. Though common in the literature, the
use of one-time measures of yawning to assess
the relationship to psychological traits could
be considered a further limitation. While we
included a self- report measure of affective
empathy, we did assess the ability to engage in
empathy. Follow- up studies in this area could
explore this further while also examining the
relationship between interspecific CY and
cognitive measures of empathy (i.e., emotion
reading and perspective-taking). In addition,
further work in this area could attempt to
improve the ecological validity of this online
experiment, perhaps including live
demonstrations of yawning in the laboratory or
the use of dynamic (i.e., video) yawn stimuli to
enhance the participant response. While
self-report CY has proven to be a valid measure
of this behavior in psychology
[3,56,57], future studies could attempt
to capture a combination of both self-report and
objective measures of CY.
-
- Conclusions
- In summary, this study replicates recent
findings providing evidence for interspecific CY
in humans. By comparing separate conditions for
common household pets, we were able to show a
slightly greater CY response to yawns of
domesticated cats compared to domesticated dogs.
Furthermore, when explicitly examining how
individual differences in empathic concern and
gender influence this response, our findings do
not support a strong connection between
interspecific CY and empathy or emotional
contagion.
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