Contagious yawning is a form of response
facilitation found in humans and other primates
in which observing a model yawning enhances the
chance that the observer will also yawn. Because
contagious yawning seems to be more easily
triggered when models are conspecifics or have a
strong social bond with the observer, it has
been proposed that contagious yawning is linked
to empathy. A possible way to test this
hypothesis is to analyze whether individuals'
responses differ when they observe models
yawning or performing different involuntary
(i.e., nose wiping, scratching) and voluntary
(i.e., hand closing, wrist shaking) actions that
are not linked to empathy. In this study, we
tested the four great ape species with two
different setups by exposing them to a human
experimenter repeatedly performing these actions
online, and video-recorded conspecifics
repeatedly performing these actions on a screen.
We examined which behaviors were subject to
response facilitation, whether response
facilitation was triggered by both human models
and video-recorded conspecifics, and whether all
species showed evidence of response
facilitation. Our results showed that
chimpanzees yawned significantly more when and
shortly after watching videos of conspecifics
(but not humans) yawning than in control
conditions, and they did not do so as a response
to increased levels of anxiety. For all other
behaviors, no species produced more target
actions when being exposed to either model than
under control conditions. Moreover, the
individuals that were more "reactive" when
watching yawning videos were not more reactive
when exposed to other actions. Since, at least
in chimpanzees, (1) subjects only showed
response facilitation when they were exposed to
yawning and (2) only if models were
conspecifics, it appears that contagious yawning
is triggered by unique mechanisms and might be
linked to empathy.
La réplication, alias contagion, du
bâillement est un réponse
comportementale mimétique observée
chez les humains et d'autres primates.
L'observation du bâillement d'un
congénère augmente la chance que
l'observateur se mette également à
bâiller.
La réplication du bâillement
semble être plus facilement
déclenchée entre
congénères, en particulier entre
ceux partageant un lien social fort. Il en a
été déduit la proposition
que la réplication du bâillement
est liée à l'empathie.
Une façon de tester cette
hypothèse est d'analyser si les
réponses des sujets diffèrent
quand ils observent des bâillements ou
d'autres comportements qu'ils soient
involontaires (essuyage du nez, grattage) ou
volontaires (fermeture de la main, serrer le
poignet), ces actions n'étant pas
liées à l'empathie.
Dans cette étude, les auteurs ont
testé quatre espèces de grands
singes dans deux situations différentes:
soit en les exposant à un
expérimentateur humain exécutant
à plusieurs reprises ces actions
successivement, soit en leur présentant,
sur un écran, leurs
congénères qui avaient
été enregistrés en video,
effectuant à plusieurs reprises ces
actions.
Les auteurs ont examiné ces
comportements "à la réponse
induite facilitée" et comparé si
le déclenchement diffèrent suivant
que le comportement est réalisé
par des humains ou par leurs
congénères (vidéo
enregistrés) et si toutes les
espèces ont montré des
réponses comparables.
Leurs résultats ont montré que
les chimpanzés bâillaient beaucoup
plus quand ils regardent leurs
congénères bâiller et peu de
temps après, mais pas en regardant les
bâillements humains. Ces bâillements
ne correspondent pas à une réponse
par augmentation des niveaux
d'anxiété comprartivement aux
conditions de contrôle.Aucun autre
comportement, avec examen en siutuations
contrôles, n'ait reproduit par aucune
espèce.
Ceux qui étaient les plus sensibles
à la réplication des
bâillements n'ont pas montré de
sensiblité particulière à
mimer d'autres comportements. Chez le
chimpanzé, en particulier, le fait que la
réplication soit nettement
facilitée par l'observation d'un
congénère, il semble que la
réplication du bâillement soit
déclenchée par des
mécanismes uniques et qu'ils pourraient
être liés à l'empathie.
Introduction
Response facilitation happens when observing
a model performing an action increases the
likelihood that the observer will also perform
the same action (Byrne 1994). Although some
authors prefer to refer to contagion when the
target action is reflexive or involuntary, as in
yawning (Zentall 2003), the more general term
''response facilitation'' is usually preferred,
as for most actions it is not possible to
exactly know whether the target action is
reflexive or has been learned (e.g., Hoppitt et
al. 2007). There are many examples of response
facilitation across animal taxa. Synchronous
courtship behavior and synchronized predator
evasion in flocks and herds have been explained
in terms of response facilitation (Armstrong
1951; Nuechterlein and Storer 1982). More
recently, response facilitation has also been
postulated as a more likely mechanism than
imitation and social learning in some situations
(e.g., Hoppitt et al. 2007). One of the most
basic examples of response facilitation is
yawning. In 40-60 % of adult humans, yawning is
easily triggered by seeing, reading or thinking
about another individual yawning (Provine 1986,
2005; Platek et al. 2003). On the basis of
experimental evidence, several authors have
proposed that contagious yawning is linked to
the ability to share others' emotions and engage
in successful social interactions; in other
words, it is linked to empathy (Preston and de
Waal 2002; Platek et al. 2003; Singer 2006;
Senju et al. 2007; but see Provine 1986; Nahab
et al. 2009). In particular, both empathy and
contagious yawning may rely on a
perception-action mechanism in which perceiving
one behavior would lead the subject to activate
shared representations and involuntarily
re-enact the observed behavior (Platek et al.
2003). For example, humans showing higher levels
of response facilitation to yawning stimuli also
score higher in questionnaires evaluating
empathy, self-recognition, and theory of mind
(Platek et al. 2003). Moreover, presumed
emotional closeness between individuals best
predicts yawning contagion in humans (Norscia
and Palagi 2011).
Yawning is common across vertebrates, and
yawning contagion has been shown in species
other than humans (e.g., Anderson et al. 2004).
Chimpanzees (Pan troglodytes), for example, yawn
more when watching videos in which conspecifics
are yawning than in control videos in which
conspecifics are not yawning (Anderson et al.
2004; Campbell and de Waal 2011). Chimpanzees
even show contagious yawning in response to
3D-animated chimpanzee yawns (Campbell et al.
2009). In gelada baboons (Theropithecus gelada)
and bonobos (Pan paniscus), yawning is
contagious and more frequent when subject and
model have a stronger social bond, suggesting
that contagious yawning might also be linked to
empathy in nonhuman primates (Palagi et al.
2009; Demuru and Palagi 2012). Contagious
yawning has also been documented in stump-tailed
macaques (Macaca arctoides), although yawning
responses elicited by unfamiliar video-recorded
monkeys yawning were accompanied by
self-scratching, suggesting that yawning was
rather triggered by increased anxiety (Paukner
and Anderson 2006).
Finally, dogs may also show contagious
yawning when watching videos of humans or
conspecifics yawning (Joly- Mascheroni et al.
2008), although these findings are controversial
(Harr et al. 2009; O'Hara and Reeve 2010).
Although there are several actions other
than yawning which subjects can copy from
conspecifics, to our knowledge no study has so
far compared primates' response when subjects
are exposed to several different target actions.
This comparison can be informative to understand
whether different mechanisms trigger response
facilitation of yawning as compared to other
behaviors, i.e., whether contagious yawning
might be linked to empathic skills while other
behaviors are not. Apart from yawning, for
example, individuals can copy other
conspecifics' behaviors that are already present
in the subject's repertoire, such as nose wiping
(i.e., quickly touching the nose with the hand),
scratching (i.e., rubbing the skin with the
fingers), hand closing (i.e., making a fist with
the fingers and then opening it again), and
wrist shaking (i.e., quickly rotating the hand
around the wrist). These behaviors are all
typically present in the behavioral repertoire
of great apes (see Nishida et al. 1999), but
only contagious yawning has been linked to
empathy (see above); nose wiping and scratching
can be involuntary actions like yawning (e.g.,
Leavens et al. 2001), but they have never been
linked to empathy; hand closing and wrist
shaking are more under voluntary control than
the other actions (Napier 1980) and have also
never been linked to empathy. If different
mechanisms trigger response facilitation to
different target actions, subjects should
respond differently in the different situations.
In particular, subjects might show response
facilitation whenever they are exposed to
involuntary actions, or only when they are
exposed to yawning.
In this study, we tested the four great ape
species (Pan troglodytes, Pan paniscus, Pongo
abelii, Gorilla gorilla) with two different
setups aimed at assessing the propensity of
individuals to spontaneously reproduce the
following target actions: yawning, nose wiping,
scratching, hand closing, and wrist shaking.
Unlike previous studies (e.g., Anderson et al.
2004; Campbell et al. 2009), we did not have a
condition involving the mouth in addition to
yawning, but included several target actions
involving other body parts. We did this because
our main goal was not to assess whether
individuals produced yawning upon seeing it,
which had already been established by previous
studies; instead, our main goal was to assess
response facilitation more broadly (i.e., we did
not only address how yawning varied under
different conditions but also how other
behaviors varied under different
conditions).
As a model, we used a human experimenter
repeatedly performing several actions online,
and video-recorded conspecifics repeatedly
performing several actions on a screen. We used
both online and video-recorded models because
subjects might attend differently to videos and
live models, possibly showing stronger
reactivity in the mirrorneuron system when
observing live motor acts (Jarvelainen et al.
2001). All models were familiar to the subjects,
as unfamiliar models might hinder response
facilitation (e.g., Harr et al. 2009; Campbell
and de Waal 2011). Our aim was to examine (1)
which behaviors are subject to response
facilitation, (2) whether response facilitation
is triggered by both human models and
video-recorded conspecifics, and (3) whether all
species show evidence of response
facilitation.
Discussion
Chimpanzees yawned significantly more when
watching videos of conspecifics yawning and
shortly after they had watched such videos, as
compared to before they watched the videos. In
contrast, their scratching behavior did not
change across phases of the yawning video. For
all the other behaviors of the human and video
setups, no species produced more target actions
when being exposed to the model. Finally, the
individuals that were more ''reactive'' to
yawning in the video setup were significantly
less reactive to nose wiping in the same setup.
No other correlations within and across setups
were found.
As in previous studies, chimpanzees yawned
more when and after watching videos of
conspecifics yawning than under control
conditions (Anderson et al. 2004; Campbell and
de Waal 2010). Chimpanzees did not yawn more as
a response to enhanced levels of anxiety, as
their scratching behavior did not significantly
vary across phases of the yawning videos (in
contrast to stump-tailed macaques: Paukner and
Anderson 2006). Interestingly, yawning was the
only behavior that elicited response
facilitation. However, response facilitation
only occurred in the video setup, suggesting
that contagious yawning in chimpanzees is more
easily triggered by conspecifics yawning than by
human experimenters yawning, despite
conspecifics in our study being video-recorded
and video-recorded conspecifics tending to
elicit weaker reactivity in the mirror-neuron
system than live conspecifics (Jarvelainen et
al. 2001). This is in line with contagious
yawning in animals having so far only been
triggered by watching conspecifics or
mirrorimages yawning (Anderson et al. 2004;
Paukner and Anderson 2006; Palagi et al. 2009;
Campbell and de Waal 2011; Demuru and Palagi
2012). If empathy underlies contagious yawning,
contagious yawning should be triggered more
frequently by familiar conspecifics living in
the same social group rather than by human
models, since the former have a stronger bond
with the tested subjects (see Campbell and de
Waal 2011). Dogs might be the only exception to
this pattern, as they have shown contagious
yawning when exposed to a human model
(Joly-Mascheroni et al. 2008), but these
findings are controversial (Harr et al. 2009;
O'Hara and Reeve 2010).
Importantly, no action other than yawning
elicited response facilitation. This result
supports the hypothesis that contagious yawning
might be triggered by mechanisms other than
those eliciting response facilitation of other
behaviors, even when these behaviors are
involuntary. In addition, individuals that
showed more response facilitation to yawning
were those that showed less response
facilitation to another involuntary target
action such as nose wiping, confirming that
reactivity to other involuntary actions might
depend on different mechanisms than those
triggering contagious yawning (Platek et al.
2003; Anderson et al. 2004; Campbell and de Waal
2011; Norscia and Palagi 2011). For example, it
has been proposed that contagious yawning is a
simple form of response facilitation that does
not require empathic skills and thus also occurs
in vertebrates that lack empathy (e.g., Yoon and
Tennie 2010). However, the only study, to our
knowledge, which tested yawning in species other
than mammals showed that contagious yawning was
never elicited in redfooted tortoises
(Geochelone carbonaria) under different
conditions, leading the authors to conclude that
contagious yawning may involve more complex
social processes than mere response facilitation
(Wilkinson et al. 2011).
The three great ape species other than
chimpanzees showed no effect upon watching
either type of model performing target actions,
including yawning. It might be speculated that
chimpanzees better activate shared
representations to re-enact observed behaviors,
thus showing more reactivity to contagious
yawning as compared to the other great apes. If
empathy is really linked to contagious behavior,
however, the fact that all great apes possess
the cognitive skills usually considered to be
prerequisites for the understanding of others'
mental states, such as perspective taking and
mirror self-recognition (e.g., Gallup et al.
2003; Braeuer et al. 2005), would suggest that
all great apes should be responsive to
contagious behavior. It is indeed conceivable
that our small sample size, together with
important interindividual differences in terms
of reactivity to the target actions (e.g.,
Anderson et al. 2004), might be responsible for
our results. Future studies with larger sample
sizes are clearly needed to confirm our
findings.
To conclude, our study provided evidence for
differences in response facilitation depending
on the target action and species. In particular,
our study found response facilitation only when
chimpanzees watched conspecifics yawn, but not
when humans yawned, or when conspecifics
performed other actions. These findings support
the view that mechanisms triggering contagious
yawning may be different from those involved in
other behaviors, and that contagious yawning may
involve more complex social processes than mere
response facilitation, such as empathic
skills.
