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les articles sur la contagion du
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articles about contagious
yawning
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- Abstract
- Behavioural contagion is a widespread
phenomenon in animal species, which is thought
to promote coordination and group cohesion.
Among non-human primates, however, there is no
evidence of behavioural contagion in
Platyrrhines (i.e. primates from South and
Central America) yet.
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- Here, the authors investigated whether
behavioural contagion is also present in this
taxon, by assessing yawning and scratching
contagion in a wild group (N = 49) of Geoffroy's
spider monkeys (Ateles geoffroyi). We conducted
focal samples to examine whether individuals
observing the triggering event (i.e. a naturally
occurring yawning or scratching event in the
group) would be more likely to yawn or scratch
in the following 3 min, as compared to
individuals who did not observe the triggering
event. We ran generalized linear mixed models
using a Bayesian approach, and found that the
probability of yawning and scratching was higher
for individuals observing others yawning and
scratching, respectively, as compared to
individuals who did not observe such an event.
Behavioural contagion did not vary depending on
the observer's sex, kinship or relationship
quality with the individual performing the
triggering event.
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- These findings provide the first evidence
for yawning and scratching contagion in a wild
group of spider monkeys, and importantly
contribute to the debate about the evolutionary
origins of behavioural contagion in
primates.
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- La
contagion du bâillement et du grattage
chez des singes-araignées
- La contagion comportementale est un
phénomène très
répandu chez les espèces animales,
dont on pense qu'il favorise la coordination et
la cohésion du groupe. Parmi les primates
non humains, cependant, il n'existe pas encore
de preuve de contagion comportementale chez les
platyrrhiniens (c'est-à-dire les primates
d'Amérique du Sud et d'Amérique
centrale).
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- Ici, less auteurs ont cherché
à savoir si la contagion comportementale
était également présente
dans ce taxon, en évaluant la contagion
des bâillements et des griffures dans un
groupe sauvage (N = 49) de
singes-araignées de Geoffroy (Ateles
geoffroyi). Nous avons réalisé des
échantillons focaux pour examiner si les
individus observant l'événement
déclencheur (c'est-à-dire un
événement naturel de
bâillement ou de grattage dans le groupe)
seraient plus susceptibles de bâiller ou
de se gratter dans les 3 minutes suivantes, par
rapport aux individus qui n'ont pas
observé l'événement
déclencheur. Ils ont utilisé des
modèles linéaires mixtes
généralisés en utilisant
une approche bayésienne et avons
constaté que la probabilité de
bâiller et de se gratter était plus
élevée pour les individus
observant d'autres personnes bâiller et se
gratter, respectivement, par rapport aux
individus n'ayant pas observé un tel
événement. La contagion
comportementale ne varie pas en fonction du sexe
de l'observateur, de son lien de parenté
ou de la qualité de sa relation avec
l'individu qui a déclenché
l'événement.
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- Ces résultats constituent la
première preuve de la contagion des
bâillements et des grattages chez un
groupe sauvage de singes-araignées et
contribuent de manière importante au
débat sur les origines évolutives
de la contagion comportementale chez les
primates.
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- Introduction
- In group-living animals, the ability to
coordinate behaviour with other group members
may provide individuals with crucial fitness
benefits, by for instance promoting social
cohesion and increasing the effectiveness of
anti-predatory strategies1,2,3. Mechanisms that
allow individuals to effectively coordinate
their activities in the group include
behavioural synchrony (when individuals react to
an external stimulus in the same way) and
behavioural contagion (when the perception of
others' behaviour automatically triggers a
similar behaviour in the observers4,5). Although
some authors consider behavioural contagion to
be linked to emotional contagion, empathy and
perhaps even theory of mind6,7,8,9, behavioural
contagion can also be explained more
parsimoniously. For example, individuals can
unconsciously mimic others' behaviour (chameleon
effect)&emdash;a phenomenon that is also common
in humans10.
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- Yawning is one of the most studied examples
of behavioural contagion. Spontaneous yawning is
widespread across vertebrates11, and is thought
to serve different functions, from increasing
blood and brain oxygen intake, to regulating
brain temperature and maintaining attentional
levels and shared alertness11,12,13,14, although
none of these hypotheses have been yet fully
confirmed. In humans, yawning can be easily
triggered by seeing, hearing, reading or
thinking about others' yawning (i.e. contagious
yawning6,15,16). Contagious yawning has also
been shown in other species. For example,
contagious yawning has been observed in captive
budgerigars (Melopsittacus undulates17), wild
elephant seals (Mirounga leonina18), domestic
pigs (Sus scrofa19), captive wolves (Canis lupus
lupus20), and domesticated dogs (C. lupus
familiaris7,21). In non-human primates,
contagious yawning has been shown in several
Catharrine species, including captive
chimpanzees (Pan troglodytes9,22,23,24,25),
captive bonobos (P. paniscus26,27), captive
orangutans (Pongo pygmaeus28), captive and wild
geladas (Theropithecus gelada8,29), and captive
stump-tailed macaques (Macaca arctoides30).
Chimpanzees, for example, are more likely to
yawn after observing videos of conspecifics
yawning rather than not yawning9,22, even when
3D-animated yawning events are used23. However,
not all tested species show contagious yawning.
In primates, there has been no evidence for
contagious yawning in Strepsirrhines (captive
ring-tailed lemurs, Lemur catta and captive
black-and-white ruffed lemurs, Varecia
variegata31) until recently (wild indris, Indri
indri32), and there is no evidence in
Platyrrhines yet (captive common marmosets,
Callithrix jacchus33).
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- In addition to yawning, other behaviours can
spread across group members as a result of
behavioural contagion. Scratching, for instance,
is a self-directed behaviour that is considered
a reliable measure of anxiety in
primates34,35,36. Unlike yawning, very few
studies have assessed the contagious effect of
scratching37. In humans, scratching is triggered
by listening to the word "itching"38 or
itch-related sounds39, and by observing others
scratching40,41,42. In non-human primates,
contagious scratching has been shown in captive
orangutans37, captive Japanese macaques (Macaca
fuscata43), wild Tibetan macaques (M.
thibetana44) and captive rhesus macaques (M.
mulatta45). As in the case of yawning, however,
there is no evidence for scratching contagion in
Platyrrhines yet (captive common
marmosets33).
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- The occurrence of behavioural contagion may
vary across species, but also within species, as
it is not necessarily a ubiquitous phenomenon
across groups and individuals (e.g. Refs.25,46).
Behavioural contagion can vary across group
members depending on the relationship they have
with the individual performing the triggering
event, and/or their own individual
characteristics. Studies on primates and other
species found that yawning contagion is more
likely between kin and individuals that have
higher-quality relationships, as compared to
non-kin and individuals having lower-quality
relationships (captive primates: chimpanzees9,
bonobos26,27 and geladas8; captive wolves20,
dogs47 and domestic pigs19). However, other
studies found no effect of kin and quality
relationship on the probability of showing
behavioural contagion (captive chimpanzees24,
captive bonobos46,48, wild geladas29, dogs21).
Moreover, some studies suggest that females
observing a triggering event show shorter
latencies to contagion (captive wolves20), or a
higher likelihood of showing the same behaviour
than males (humans49,50, captive bonobos46; but
see wild geladas29). However, other studies
found no sex bias in behavioural contagion
(captive chimpanzees9,23, wild lemurs32,
dogs7).
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- In this study, we aimed to investigate
behavioural contagion in a wild group of
Geoffroy's spider monkeys (Ateles geoffroyi), a
species with no pronounced sexual dimorphism in
body and canine size51. In particular, we aimed
to assess whether contagious yawning and
scratching are present in Platyrrhines, and how
their natural occurrence varies across
individuals. First, we predicted that
individuals observing a yawning or scratching
event would be more likely to yawn or scratch,
respectively, as compared to individuals who did
not observe such events (Prediction 1). Second,
we predicted that behavioural contagion would be
more likely (a) between individuals with a
higher-quality relationship, (b) between
maternal kin, and (c) in female observers, as
compared to individuals having a lower-quality
relationship, non-kin and male observers
(Prediction 2).
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- Discussion
- Our study provided the first evidence for
behavioural contagion in spider monkeys. In
particular, we showed that individuals observing
a group member yawning or scratching were more
likely to yawn or scratch than individuals who
did not observe such an event, in line with our
Prediction 1. Therefore, our results show that
yawning and scratching contagion are also
present in Platyrrhines, and importantly
contribute to the debate about the evolutionary
origins of primate behavioural contagion. To
date, yawning contagion has been shown in a
variety of Catharrine
species8,9,22,23,24,25,26,27,28,29, and more
recently, in lemurs32. By providing evidence of
yawning and scratching contagion also in
Platyrrhines, our study provides further support
to the hypothesis that behavioural contagion
emerged before the evolutionary split between
these taxa68,69. However, it is of course
impossible to rule out that behavioural
contagion independently evolved multiple times
across taxa, perhaps in response to the specific
socio-ecological conditions experienced by
different species, groups and individuals.
Indeed, this might explain why behavioural
contagion is not present in some Catharrine
species (e.g. gorillas (Gorilla gorilla
gorilla): with video-recorded stimuli70), or in
some groups and individuals of species that
otherwise show behavioural contagion (see e.g.
within-species variation in humans: with
video-recorded stimuli6, with video-recorded and
photo stimuli50; bonobos: with conspecifics46,
and macaques: with video-recorded
stimuli30).
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- In spider monkeys, the contagion effect
occurred on average after 62 s from the
triggering yawning event and after 32 s from the
triggering scratching event. These results are
in line with previous studies in other species
showing that behavioural contagion takes place
within the first minute after the triggering
yawning event (with conspecifics:
Refs.26,27,46), or within the second minute
(with conspecifics: Refs.29,71; with
video-recorded stimuli: Ref.8), and within the
first 90 s after the triggering scratching event
(with conspecifics: Refs.37,45). Moreover, our
results show contagion rates similar to those
found in the literature. In our study, the
percentage of cases in which partners yawned
after observing the triggering event was 31% (in
contrast to 22% for individuals not observing
it), as compared to 15&endash;40% of contagion
after yawning events in captive bonobos27,46,
5&endash;20% in captive geladas8 and
15&endash;45% in wild geladas29, all tested with
conspecifics. Similarly, the percentage of cases
in which partners scratched after observing the
triggering event was 50% (in contrast to 32% for
individuals not observing it), as compared to
10&endash;25% of contagion after scratching
events in captive orangutans (with conspecifics:
Ref.37). At first sight, the percentage of cases
in which partners yawned and scratched after
observing no triggering events (22% and 32%,
respectively) might appear unusually high.
However, yawning and scratching can be caused by
specific social and environmental conditions
(e.g. uncertainty, low
oxygen12,13,14,15,34,35,36), so that,
individuals in spatial proximity, such as the
partners within 5 m of the focal animal, are
likely to co-experience. Therefore, partners
were more likely to yawn and scratch when the
focal animal yawned and scratched, regardless of
having observed the triggering event. By
directly comparing behaviour of partners exposed
to the same environmental conditions within the
same time window and only differing in whether
they observed the triggering event, we thus
ensured that differences between the two types
of partners likely depended on behavioural
contagion. Moreover, as explained in the
Methods, it is possible that we might have
partially underestimated the effect of
behavioural contagion, as some partners might
have observed group members other than the focal
animal producing the same behaviour as the
triggering event, thus being more likely to also
perform it through behavioural contagion,
despite being classified as not having observed
the triggering event. Crucially, this could not
lead to false positives, but rather biased
against finding evidence for our Prediction
1.
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- Spider monkeys are characterized by a high
degree of fission&endash;fusion dynamics, with
frequent changes in subgroup size and
composition: therefore, group members may not be
together for relatively long periods of time and
social relationships might change during these
periods72. Possibly, behavioural contagion might
thus serve as a cognitively undemanding way for
individuals to rapidly tune in to other group
members upon fusions (see Refs.73,74), by
mimicking others' behaviour, synchronizing
activities and ultimately promoting group
coordination and social cohesion in the face of
potentially important changes. Moreover, given
that behavioural contagion is considered a
precursor of other important social and
cognitive skills, like emotional contagion,
empathy or theory of mind6,7,8,9,75, it will be
interesting to assess whether these skills are
also present in this species.
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- In contrast to our Prediction 2, we did not
find an effect of partner's sex, maternal
kinship and relationship quality on yawning and
scratching contagion. We tested for this effect
by including the interaction between these
factors and whether the partner observed the
triggering event in our most complex models,
which however did not have a higher predictive
ability than the other models. Females were not
more likely to show yawning contagion than males
in line with previous results in wild geladas
(with conspecifics: Ref.29). Sex had however an
effect on the occurrence of yawning (regardless
of its spontaneous or contagious nature) with
females being more likely to yawn than males.
This may be related to the low sexual dimorphism
in canine size in spider monkeys51 as males yawn
more than females in sexually dimorphic
non-human primates76 (e.g. Japanese macaques,
long-tailed macaques (M. fascicularis77),
stump-tailed macaques78, Sulawesi crested black
macaques (M. nigra79), chacma baboons (Papio
ursinus80)). Moreover, we found no evidence that
behavioural contagion was higher between kin and
individuals with a better-quality relationship,
in contrast with what was found in other studies
(with conspecifics: gelada baboons8,
bonobos26,27; video-recorded stimuli:
chimpanzees9). However, there are also studies
that found no link between kinship and/or
relationship quality and behavioural contagion.
For example, chimpanzees did not yawn more
frequently after watching yawning videos of
familiar rather than unfamiliar conspecifics22,
and in wild geladas yawning contagion was higher
between individuals from different core units,
who are less likely to engage in positive social
interactions29. Similarly, Barbary macaques
watching scratching videos paid more attention
to familiar individuals with weaker rather than
stronger social relationships81. The absence of
evidence for an effect of relationship quality
and kinship in our study indicates that in
spider monkeys behavioural contagion might be
better explained by emotional synchrony rather
than emotional contagion, which is expected to
play a role between socially close
individuals4,5. However, the link between
behavioural contagion and kinship/relationship
quality is still unclear.
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- Overall, by providing the first evidence for
yawning and scratching contagion in wild spider
monkeys, and considering the recently findings
in wild lemurs32, our study supports the
hypothesis that behavioural contagion emerged
before the split between Strepsirrhines and
Haplorhines, and is therefore likely to be
present across primate species. Moreover, our
study opens up to new lines of investigation
that might provide novel perspectives on the
link between behavioural contagion and social
complexity, such as whether individuals might
more heavily rely on behavioural contagion to
effectively tune in with other group members in
species characterized by high levels of
fission&endash;fusion dynamics. Finally, our
results confirm the use of wild settings as a
powerful approach to study animal behaviour and
cognition, since they provide large sample sizes
and high ecological validity complementing
controlled studies in captive settings.
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