- Tous
les articles sur la contagion du
bâillement
- All
articles about contagious
yawning
-
- -Palagi E,
Leone A, Mancini G, Ferrari PF. Contagious
yawning in gelada baboons as a possible
expression of empathy. Proc Natl Acad Sci USA.
2009;106(46):19262-19267
- -Palagi E,
Norscia I, Demuru E. Yawn contagion in
humans and bonobos: emotional affinity matters
more than species Peer J 2:e519
- -Palagi E,
Norscia I, Cordoni G. Lowland gorillas
(Gorilla gorilla gorilla) failed to respond to
others' yawn: Experimental and naturalistic
evidence. J Comp Psychol. 2019
- -Palagi
E, Guillén-Salazar F,
Llamazares-Martín C. Spontaneous
Yawning and its Potential Functions in South
American Sea Lions (Otaria flavescens). Sci Rep.
2019;9(1):17226.
- -Palagi
E, Cordoni G. Intraspecific Motor and
Emotional Alignment in Dogs and Wolves: The
Basic Building Blocks of
Dog&endash;Human
Affective Connectedness. Animals
2020;10(2):241
- -Norscia
I, Zanoli A, Gamba M, Palagi E. Auditory
Contagious Yawning Is Highest Between Friends
and Family Members: Support to the Emotional
Bias Hypothesis.
Front
Psychol. 2020 Apr 3;11:442
-
- Abstract
- Yawn contagion, possibly a form of emotional
contagion, occurs when a subject yawns in
response to others' yawns. Yawn contagion has
been reported in humans, chimpanzees, bonobos,
geladas, wolves, and dogs. In these species,
individuals form strong, long-term relationships
and yawn contagion is highest between closely
bonded individuals. This study focuses on the
possible expression of yawn contagion in western
lowland gorillas (Gorilla gorilla gorilla).
Gorillas share with geladas a similar basic
social structure (one dominant male and several
adult females with offspring) and differ from
bonobos and chimpanzees, which live in
multimale-multifemale societies. Gorillas stand
out because they are spatially aggregated but
show especially low levels of social
affiliation. If the expression of yawn contagion
is linked to the investment of animals in
establishing long-term social relationships, the
phenomenon should not be detected in gorillas
(social relationship hypothesis). For the first
time, we applied to the same subjects the
naturalistic approach typically used in ethology
(all occurrences behavioral sampling) and the
experimental approach typically used in
psychology (response to video stimuli). During
the video demonstration (avatar yawn/control;
unfamiliar gorilla yawn/control), we checked for
the attentional state of the subjects.
Anxiety-related self-directed behaviors were
recorded in all conditions and settings. We
failed to detect yawn contagion in both
naturalistic and experimental settings, with
yawning being possibly associated with anxiety
during video shows (revealed by the increased
frequency of self-directed behaviors). In
conclusion, yawn contagion may be a socially
modulated phenomenon that remains largely
unexpressed when individuals share weak social
affiliation.
-
- Résumé
- La contagion (réplication) du
bâillement, éventuelle forme de
contagion émotionnelle, se produit
lorsqu'un sujet bâille en réponse
aux bâillements des autres. La
réplication du bâillement a
été rapportée chez l'homme,
le chimpanzé, le bonobo, le gelada, le
loup et le chien. Chez ces espèces, les
individus forment de solides relations à
long terme et la réplication du
bâillement est la plus forte entre les
individus étroitement liés. Cette
étude porte sur l'expression possible de
la réplication du bâillement chez
les gorilles des plaines de l'ouest (Gorilla
gorilla gorilla). Les gorilles partagent avec
les geladas une structure sociale de base
similaire (un mâle dominant et plusieurs
femelles adultes avec une progéniture) et
diffèrent des bonobos et des
chimpanzés, qui vivent dans des
sociétés multi-males /
multi-féminines. Les gorilles se
distinguent par leur agrégation spatiale
mais montrent des niveaux
particulièrement faibles d'affiliation
sociale. Si l'expression de la
réplication du bâillement est
liée à l'investissement des
animaux dans l'établissement de relations
sociales à long terme, le
phénomène ne devrait pas
être détecté chez les
gorilles (hypothèse de relation sociale).
Pour la première fois, les auteurs ont
appliqué aux mêmes sujets
l'approche naturaliste typiquement
utilisée en éthologie
(échantillonnage comportemental toutes
occurrences) et l'approche expérimentale
typiquement utilisée en psychologie
(réponse aux stimuli vidéo). Au
cours de la démonstration vidéo
(avatar bâillement / contrôle ;
gorille inconnu bâillement /
contrôle), nous avons
vérifié l'état de
l'attention des sujets. Les comportements
autodirigés liés à
l'anxiété ont été
enregistrés dans toutes les conditions et
dans tous les contextes. Ils n'ont pas
réussi à détecter la
réplication du bâillement dans des
contextes à la fois naturalistes et
expérimentaux, le bâillement
étant peut-être associé
à de l'anxiété pendant les
émissions vidéo
(révélée par la
fréquence accrue de comportements
autodirigés). En conclusion, la
réplication des bâillements peut
être un phénomène
modulé par la société qui
reste largement inexprimé lorsque les
individus partagent une faible affiliation
sociale.
- Yawn contagion occurs when a subject yawns
in response to a triggering yawn emitted by
another subject (Campbell, Carter,Proctor,
Eisenberg, & de Waal, 2009; Provine, 1986,
2005). As a form of involuntary mimicry
(Thompson & Richer, 2015), yawn contagion
may be a form of emotional contagion, possibly
involving the mirror neuron system (Brown et
al., 2017; Haker, Kawohl,Herwig, &
Rössler, 2013; Nahab, Hattori, Saad, &
Hallett, 2009).Through the activation of this
system, two individuals can non consciously
share physiological and related affective states
based on perceived motor patterns (Gallese,
Keysers, & Rizzolatti,2004). This
perception&endash;action mechanism (de Waal
& Preston,2017) can facilitate behavioral
matching and social living because it allows
individuals to synchronize their emotional
states through the replication of the actions or
facial expressions of other individuals
(Christov-Moore et al., 2014). However,
contextual factors, such as environmental visual
and auditory information, can affect the rates
of involuntary mimicry (Wieser & Brosch,
2012).
-
- So far, there is strong evidence for yawn
contagion in one cercopithecid monkey species
(geladas, Theropithecus gelada; Palagi, Leone,
Mancini, & Ferrari, 2009). In the
stump-tailed macaques (Macaca arctoides), a yawn
video elicited significantly more yawns than a
control video, but also more self-directed
behaviors like scratching. Therefore, the
mechanism in these macaques might have been due
to increasing tension or arousal, and not
necessarily to social identification as required
by the perception - action mechanism (Paukner
& Anderson, 2006). Yawn contagion has been
found in two hominid species, chimpanzees (Pan
troglodytes: Anderson, Myowa-Yamakoshi, &
Matsuzawa,2004; Campbell & de Waal, 2011)
and humans (Homo sapiens: Provine, 1986, 1989),
and in both species there was a developmental
effect from infancy, childhood to adulthood
(Bartholomew& Cirulli, 2014; Madsen,
Persson, Sayehli, Lenninger, & Sonesson,
2013).
-
- One report failed to detect yawn contagion
in two other hominid species, bonobos (Pan
paniscus) and gorillas (Gorilla gorilla), but
the sample size (four to five animals) was too
small to be conclusive (Amici, Aureli, &
Call, 2014). Two other studies using larger
samples found that yawn contagion is indeed
present in bonobos (Demuru & Palagi, 2012;
Tan, Ariely, & Hare, 2017). No other
investigation has been carried out on Gorilla
gorilla, thus leaving the yawn contagion issue
open in this species. In humans, studies
typically report a yawn contagion rate of around
50%, although the incidence of this phenomenon
can be affected by psychological/neurological
disorders such as autism and schizophrenia (Chan
& Tseng, 2017). Additionally, there is
strong evidence that this phenomenon is socially
modulated in both human and nonhuman primates.
In geladas, Palagi et al. (2009) found that the
frequency of yawn contagion correlated with the
level of grooming between individuals but not
with their level of spatial proximity.
Therefore, the strength of social bonds ap pears
to modulate yawn contagion in this species.
Social modulation may have limited or no
influence on yawn contagion rates in young
chimpanzees (Madsen et al., 2013), but adults
were found to be more susceptible to yawns
performed by in-group than by out-group members
(Campbell & de Waal, 2011).
-
- In humans and bonobos, yawn contagion was
found to be more frequent between strongly
bonded than between weakly bonded individuals
(Demuru & Palagi, 2012), even though both
species also responded to strangers' yawns
(humans: Norscia & Palagi, 2011, 2016;
bonobos: Tan et al., 2017; both humans and
bonobos: Palagi, Norscia, & Demuru, 2014).
We investigated the possible expression of yawn
contagion in lowland gorillas (Gorilla gorilla
gorilla). To explore the phenomenon in a
comprehensive way, for the first time, we
combined both a naturalistic and an experimental
approach in a single study. Gorillas are
phylogenetically distant from geladas but very
close tothe other African hominids (Scally et
al., 2012; Stevens et al.,2013). The socio
ecology of gorillas contains some traits that
are similar to geladas at least in the mating
patterns. In both species, the basic social unit
includes one dominant male and several adult
females with offspring. Although geladas have a
multilevel structure where the different basic
social units gather together in larger
aggregations (e.g., herds), the members of the
different basic social units are always in sight
(Kummer, 1971; Palagi, Leone, Demuru,&
Ferrari, 2018).
-
- Similar to bonobos and chimpanzees, gorillas
possess a long ontogenetic trajectory (with the
weaning period lasting up to 4 - 6 years) and
highly developed cognitive abilities (de
Lathouwers &van Elsacker, 2006; Watts &
Pusey, 1993). On the other hand, gorillas differ
from both African great apes and geladas in the
levels of social affiliation between individuals
(Cordoni, Norscia,Bobbio, & Palagi, 2018).
Chimpanzees and bonobos live in fission - fusion
groups in which group-mates form strong and
enduring social bonds, for example, via grooming
exchange and agonistic support (Foerster et al.,
2016; Gruber & Clay, 2016; Langergraber,
Mitani, & Vigilant, 2009; Muller &
Mitani, 2005; Slocombe et al., 2010). In gelada
social basic units, females engage in high
levels of affiliative contact and establish long
term social relationships between them (Dunbar
& Dunbar, 1975).
-
- In lowland gorilla one-male groups, females
show extremely low levels of social affiliation
because they spatially aggregate around one
adult male, the silverback, mainly for
protection reasons (Harcourt & Stewart,
2007). The death of the silverback leads to
group disruption and females disaggregate moving
to other groups (Harcourt & Stewart, 2007).
In the wild, Stokes (2004) observed only eight
affiliative interactions during 802 hrs of
observation; six of them were between silverback
and reproductive females and involved sexual
behavior and physical contact. Grooming between
adults was never observed and females engaged in
almost no affiliative behavior with each other.
These findings led the authors to consider
lowland gorilla as a species characterized by
low levels of affiliation (Cordoni et al., 2018;
Masi, Cipolletta, & Robbins,2009; Stokes,
2004).
-
- In gorillas, the migrating males can join
together and form bachelor groups. It has been
found that these males share a certain amount of
affiliation and social cohesiveness that
strongly decrease when females join the group
(Harcourt &Stewart, 2007). Based on the
aforementioned framework, we formulated two
alternative hypotheses on yawn contagion. Social
relationship hypothesis - If the expression of
yawn contagion covaries with the level of
affiliative contacts that animals engage in to
form strong social interindividual
relationships, we expect that yawn contagion is
not expressed in gorillas, due to their
especially low investment in social affiliative
exchange (Prediction 1). Alternative hypothesis
- If the expression of yawn contagion does not
depend on the quality of the interindividual
social relationships but depends on shared
biological and cognitive features (common to all
African great apes), we expect that yawn
contagion is expressed in gorillas, as it is
expressed in other African hominids (Prediction
2).
-
-
- Discussion
- The results show that, in our study groups
of gorillas, yawncontagion was not found in
either the naturalistic (see Figure 3) orvideo
setting (see Figure 1; social relationship
hypothesis sup ported). In both settings, the
frequency of yawns following theyawning stimulus
(yawn condition) did not significantly
differfrom the control condition (mouth opening
and closing in the videosetting and no
detectable yawn in the naturalistic setting). In
thevideo setting, yawns were released from
unknown gorilla individ uals (and avatar)
whereas in the naturalistic setting yawns
camefrom familiar subjects (group-mates).
-
- Therefore, the absence of yawn contagion in
our study groups cannot be related to
theunfamiliarity between subjects. Moreover, the
inability to find yawn contagion in our gorilla
groups cannot be ascribed to their low rates of
spontaneous yawns because our results show that
thefrequency of spontaneous yawning recorded in
gorillas (yawn/hr/individual: mean 0.341 0.075
SE) tends to be higher than the frequency
recorded in geladas (yawn/min/individual: mean
0.085 0.035 SE calculated from Leone, Ferrari,
& Palagi, 2015) and in the other African
great apes (bonobo yawn/min/individual:
mean0.143 0.043 SE, Demuru & Palagi, 2012;
chimpanzee yawn/min/individual: mean 0.130 0.025
SE, calculated from Campbell& de Waal,
2011), all species in which yawn contagion was
found.
-
- In the experimental condition (video
setting), self-directed be haviors partly
influenced the distribution of yawning
frequencies(Table 4 and Figure 2), but the
levels of self-directed behavior didnot
significantly differ between yawn and control
condition, which suggests that anxiety may have
affected yawning in a similar wayin the two
conditions. There is behavioral and
pharmacological evidence that self-directed
behaviors, including self-scratching
andself-grooming, are good indicators of anxiety
in primates, fromlemurs to apes and humans
(Maestripieri, Schino, Aureli, &
Troisi,1992; Norscia & Palagi, 2016; Palagi
& Norscia, 2011; Schino,Perretta, Taglioni,
Monaco, & Troisi, 1996; Troisi, 2002).
-
- Yawning itself has been found to be linked
to anxiety in strepsirhine andhaplorhine
primates (Maestripieri et al., 1992; Troisi,
2002; Zan nella, Norscia, Stanyon, & Palagi,
2015). Moreover, "tension yawns" related
to conflict situations and possible arousal were
described in geladas (Leone et al., 2015),
Tonkean macaques(Zannella, Stanyon, &
Palagi, 2017), and chimpanzees (Vick
&Paukner, 2010). Even though yawning in our
groups may have been also related to anxiety, it
is not possible to conclude that anxiety is the
main factor responsible in suppressing yawn
contagion when animals are in their social
context.
-
- As a matter of fact, under the naturalistic
condition, yawning was not temporally as
sociated with self-directed behaviors. Moreover,
the increase of scratching observed in the
experimental setting does not necessarily imply
a negative effect on contagious yawning. In
humans, for example, the increase of cortisol
following the admin istration of a stressful
stimulus has been hypothesized to increaseall
yawning (Thompson, 2014). However, the
relationship between yawn contagion and anxiety
in human and nonhuman primates deserves further
investigations. Failing to find yawn contagion
in lowland gorillas might at first sound counter
intuitive due to the high levels of cognition of
this species and the close phylogenetic
relationship with other great apes and humans
(de Lathouwers & van Elsacker, 2006; Scally
etal., 2012).
-
- However, following the bottom-up approach
proposedby de Waal and Ferrari (2010) and the
Russian doll model of empathy (de Waal &
Preston, 2017), the expression of basic empathy
via emotional contagion does not necessarily
require complex cognitive abilities and can be
the outcome of a preconscious mechanism. High
cognition is not sufficient per se to assume
that emotional contagion is present because this
phenomenon is also strictly related to the
activity of subcortical areas (e.g.,amygdala,
insula, hippocampus) in mice and humans (Choi
&Jeong, 2017; Sturm et al., 2013).
-
- On the other hand, emotional contagion,
including yawn contagion, is affected by the
relationship quality between individuals and
social closeness (de Waal & Preston, 2017).
This is expected considering that the adaptive
role of empathy is to favor prosocial behavior
and cooperation leading to the increase of
direct and indirect fitness (Decety, Bartal,
Uzefovsky, & Knafo-Noam, 2016). Indeed, the
inability to find yawn contagion in our groups
of gorillas seems to support the hypothesis that
interindividual social affiliation more than
social structure or shared biological features
(e.g., neural complexity related to shared
phylogeny) is crucial to yawn contagion (social
relationship hypothesis sup ported). In this
study, we found that the level of social
affiliation (measured via spatial proximity,
grooming, contact sitting, andagonistic support)
was virtually close to zero in both the family
and the bachelor group. This result is
consistent with the findings of a comparative
study carried out by Cordoni et al. (2018)
including the same gorilla family group as the
present study, inwhich the authors demonstrated
that social affiliation was strikingly lower in
gorillas than in chimpanzees.
-
- Although in the gorilla society the
silverback plays the central role in protecting
and maintaining the integrity of the social
group (Harco urt & Stewart,2007), the
yawning stimuli emitted by the silverback did
not elicitany response in the females of our
family group.Two previous studies have shown
that social cohesion between individuals can
become the factor that is most important in
elicit ing yawn contagion, even more than
interspecific differences(Campbell & de
Waal, 2014; Palagi et al., 2014). In a direct
comparison between bonobos and humans, Palagi et
al. (2014) found that yawn contagion rates were
not affected by the species the individuals
belonged to when the individuals shared
weaksocial bonds. Campbell and de Waal (2014)
also found that the rateof chimpanzee response
to triggering yawns was similar when thestimulus
came from an in-group chimpanzee and from a
human subject, thus demonstrating that the
response can go beyond the species boundary.
Silva, Bessa, and de Sousa (2012) not only
showed that dogs were able to respond to human
yawns but also found that dogs yawned more at
yawns released by familiar than unfamiliar human
subjects.
-
- Recently, Tan et al. (2017) found
thatbonobos are infected by yawns of strangers
and familiar subjects at similar rates. However,
in humans, chimpanzees, bonobos, andwolves,
closely bonded individuals showed higher levels
of yawn contagion compared with weakly bonded
individuals (Campbell &de Waal, 2011; Demuru
& Palagi, 2012; Norscia & Palagi,
2011;Palagi et al., 2014; Romero, Ito, Saito,
& Hasegawa, 2014). The inability to find
yawn contagion in these gorillas may be linked
totheir lower levels of social affiliation
compared with other species.This view is
reinforced by the fact that yawn contagion is ex
pressed in geladas (Palagi et al., 2009), which
share with gorillasa similar basic social
structure but possess higher levels of
socialaffiliation compared with gorillas (Dunbar
& Dunbar, 1975; Kummer, 1971). It seems
therefore that interindividual spatial associ
ation does not equate with social
closeness.Emotional contagion through facial
mimicry can enhance affective and behavioral
synchronization with others (Couzin, 2007;
deWaal & Preston, 2017) and, for this
reason, contagion might have acquired an
important adaptive value in social groups that
are built upon solid interindividual
relationships. When the factor keeping agroup
together is mainly spatial proximity (as it is
the case of adult gorilla females aggregated
around the silverback), the selectivepressure
over the mechanisms promoting behavioral and
emotional matching, including yawn contagion,
may have weakened. Some scholars have pointed
out that low frequencies of yawn contagion might
reflect low attention to the stimulus, which can
vary depending on the stimulus source (e.g.,
familiar vs. unfamiliar subject; for a review,
see Massen & Gallup, 2017). It could be
therefore argued that the low attention that
individuals pay to each other in the group makes
it difficult for gorillas to express
yawncontagion. It is indeed true that the
response to a stimulus can beelicited only if
the source of the stimulus is detected.
-
- In this study,we made sure that the yawning
stimulus fell into the stereoscopicvisual range
of the potential gorilla responders, and in the
exper imental setting we also controlled for the
time that the subjectactually looked at the
video (Video S1 in the online
supplementalmaterials). Despite this control,
yawning did not transfer from onegorilla to
another. Usui and colleagues (2013) found that
children with autism spectrum disorder showed
yawn contagion as typically developing children
when specific measures were taken to ensure that
the subjects could detect the video stimulus. In
the only study published so far on the influence
of selective attention on yawn contagion in
nonclinical human subjects, Chan and Tseng
(2017) found that the perceptual detection
sensitivity to yawning expression (the ability
to detect a yawn as such) was related to the
duration of gaze to the eyes of the
stimulus-releasing face, but the authors failed
to find evidence that eye-gaze patterns
modulated contagious yawning behavior. Previous
studies in humans also found that yawn contagion
seems not to be sensitive to the number of
triggering yawns (Norscia & Palagi, 2011),
the sensory modality (auditory, visual, or
audio&endash;visual; Arnott, Singhal, &
Goodale, 2009; Norscia & Palagi, 2011), or
the visual perspective of thetriggering stimulus
(yawns in orientations of 90°, 180°,
and 270° were as potent or nearly as potent
as normal, upright, 0° yawns;Provine, 1989,
1996). Campbell and de Waal (2011) found that
chimpanzees yawned more frequently in response
to in-group mate yawns compared with out-group
chimpanzee yawns, even thought hey looked longer
at out-group chimpanzee videos.In sum, the
existing evidence suggests that attention is
important in eliciting the yawning response in
so far as it ensures stimulus detection. In this
respect, nonconscious processing and
bottom-up(stimulus driven) attention and not
top-down, selective attention (sensu Bachmann,
2011; Katsuki & Constantinidis, 2014; Kaya
&Elhilali, 2017) is likely to be involved in
yawn contagion. More over, the level of the
yawning response seems not to be sensitive to
the level of attentiveness or overstimulation
(more than astimulus). Further studies on larger
sample sizes are necessary to understand whether
the inability to find yawn contagion in our
gorilla groups reflects the actual lack of the
phenomenon. If this is the case, it will remain
to be clarified whether the absence of yawn
contagion is linked to gorillas' scarce baseline
attention to conspecifics or to their scarce
responsiveness to others' stimuli in a society
that is characterized by loose social
relationships.
|
