- Tous
les articles sur la contagion du
bâillement
- All
articles about contagious
yawning
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- Yawning, a fixed action pattern, is
widespread in almost all vertebrate taxa.
Several hypotheses have been proposed to explain
the functions of yawning. These hypotheses, not
mutually exclusive, can be conventionally
arranged according to both physiological (e.g.
drowsiness hypothesis: yawning when switching
between sleep and being awake; arousal
hypothesis: yawning in contexts of high social
tension) and social communicative domains (e.g.
contagion hypothesis, activity synchronization
hypothesis). Owing to their high social cohesion
and synchronized group activity, wild lions are
a good model to investigate both spontaneous
yawning from the physiological domain and,
possibly, contagious yawning, from the social
communicative domain.
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- The authors videorecorded two groups of
lions in the Makalali Reserve (Limpopo region,
South Africa) and analysed their yawning
behaviour. Spontaneous yawning was particularly
frequent when the lions were relaxed and, in
agreement with the 24 h activity cycle typical
of the species, was similarly distributed over
the night and day. These findings support the
drowsiness hypothesis predicting that yawning is
linked to the transition between sleeping and
waking (and vice versa). Lions did not show high
levels of yawning during competition over
clumped food such as carcasses; hence, the
arousal hypothesis was not supported. They found
that yawn contagion was present, supporting the
contagion hypothesis and the activity
synchronization hypothesis. Their findings
suggest that the convergence of motor behaviour
triggered by yawn contagion (to our knowledge
never explored in any other species) could
represent an important tool to shed light on the
adaptive and immediate benefits that underlie
the evolution of the yawn contagion phenomenon
in human and nonhuman animals.
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 -
- Le bâillement, un modèle de
comportement, est répandu dans presque
tous les taxons de vertébrés.
Plusieurs hypothèses ont
été proposées pour
expliquer les fonctions du bâillement. Ces
hypothèses, non exclusives l'une de
l'autre, peuvent être classiquement
classées en physiologiques (ex:
hypothèse de somnolence: bâillement
lors du passage du sommeil à
l'éveil; hypothèse de relaxation:
bâillements dans des contextes de forte
tension sociale) et des domaines de
communication sociale (ex: hypothèse de
contagion, activité de synchronisation).
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- En raison de leur forte cohésion
sociale et de leur activité de groupe
synchronisée, les lions sauvages sont un
bon modèle pour étudier à
la fois le bâillement spontané d'un
point de vue physiologique et, aussi la
contagion du bâillement dasn le domaine de
la communication sociale. Les auteurs ont
observé deux groupes de lions dans la
réserve de Makalali (région du
Limpopo, Afrique du Sud) et analysé leurs
bâillements.
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- Les bâillements spontanés
étaient particulièrement
fréquents lorsque les lions
étaient détendus et correspondant
avec le cycle d'activité de 24 h typique
de l'espèce. Ils étaient
répartis de manière similaire
pendant la nuit et le jour. Ces résultats
confirment l'hypothèse de la somnolence
prédisant que le bâillement est
lié à la transition entre le
sommeil et l'éveil (et vice versa). Les
Lions n'ont pas montré des niveaux
élevés de bâillement lors de
la compétition pour des aliments tels que
des carcasses d'animaux ; par conséquent,
l'hypothèse d'effet stimulant n'a pas
été démontrée. Ils
ont constaté que la contagion du
bâillement était présente,
confirmant cette hypothèse et
l'hypothèse d'un effet de synchronisation
d'activité. Leurs résultats
suggèrent que la convergence du
comportement moteur déclenché par
la contagion du bâillement (à notre
connaissance, jamais explorée dans aucune
autre espèce) pourrait représenter
un outil important pour faire la lumière
sur les avantages adaptatifs et immédiats
qui sous-tendent l'évolution du
phénomène de contagion du
bâillement chez l'homme et animaux non
humains.
- Yawning is a ubiquitous behaviour which is
present in many taxa including fish, reptiles,
birds and mammals (Baenninger, 1997). It is
described as a fixed action pattern which is
stereotyped and often repetitive. It is
characterized by mouth gaping that is
accompanied by a long breath inspiration
followed by a brief apnoea and then by a quick
expiration (Walusinski & Deputte, 2004).
Many hypotheses have been proposed to explain
the prox- imate and ultimate factors involved in
spontaneous yawning. These hypotheses
conventionally fall into two domains:
physiological (nondirected yawns, sensu Moyaho,
Flores Urbina, Monjaraz Guzma n, &
Walusinski, 2017) and social communicative
(directed yawn, sensu Moyaho et al., 2017).
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- The physiological hypotheses predict that
internal factors, such as drowsiness, arousal,
thermoregulation or brain oxygenation modulate
the occurrence and frequency of yawning (Gallup,
2010, 2011, 2014; Giganti & Zilli, 2011;
Guggisberg, Mathis, Schnider, & Hess, 2010;
Krestel, Bassetti, & Walusinski, 2018;
Walusinski, 2014). According to the drowsiness
hypothesis, spontaneous yawning often occurs
during resting periods (Provine & Hamernik,
1986; Provine, Hamernik, & Curchack, 1987)
and is performed when animals switch from being
awake to sleeping and vice versa (ostrich,
Struthio camelus australis, Sauer & Sauer,
1967; African elephant, Loxodonta africana,
Rossman et al., 2017; South American sea lion,
Otaria flavescens, Palagi, Guille n-Salazar,
& Llamazares- Marti_n, 2019; humans,
Giganti, Zilli, Aboudan, & Salzarulo, 2010,
Greco, Baenninger, & Govern, 1993, Provine,
2005). In these behavioural transitions, the
role of yawning is to increase alertness, thus
making human and nonhuman animals able to adjust
their behaviour in response to sudden and
unexpected situations (Provine, 2005).
- Spontaneous yawning can also vary as a
function of the stimuli an animal receives from
its social environment (Baenninger, 1997;
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- Deputte, 1994; Greco et al., 1993;
Guggisberg et al., 2010; Provine 1997). The
arousal hypothesis predicts that anxiogenic
events (e.g. competition over food, agonistic
contacts, predation attacks) can lead to an
increase in yawning. This has been reported in
many different taxa such as birds (Nazca booby,
Sula granti, Liang, Grace, Tompkins, &
Anderson, 2015; budgerigar, Melopsittacus
undulatus, Miller, Gallup, Vogel, & Clark,
2010), rats, Rattus norvegicus (Moyaho &
Valencia, 2002), South American sea lions
(Palagi, et al., 2019) and primates (ringtailed
lemur, Lemur catta, Verreaux's sifaka,
Propithecus verreauxi, Zannella, Norscia,
Stanyon & Palagi, 2015; gelada baboon,
Theropithecus gelada, Leone, Ferrari, &
Palagi, 2014; longtailed macaque, Macaca
fascicularis, Schino, Maestripieri, Scucchi,
& Turillazzi, 1990; Japanese macaque, Macaca
fuscata, Tonkean macaque, Macaca tonkeana,
Zannella, Stanyon & Palagi, 2017). In
accordance with the arousal hypothesis, Baker
and Aureli (1997) showed that chimpanzees, Pan
troglodytes, yawned more frequently after
periods of high social tension that induced
arousal in the subjects, and in South American
sea lions, yawning peaked immediately after an
aggressive conflict in both aggressors and
victims (Palagi, et al., 2019). Several studies
indicate that, under such circumstances, yawning
can function as a stress-releaser mechanism by
facilitating physiological/emotional homeostasis
(Eldakar et al., 2017; Liang et al., 2015;
Miller et al., 2010; Miller, Gallup, Vogel &
Clark, 2012; Moyaho et al., 2017; Walusinski,
2006, 2010).
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- The social communicative hypothesis claims
that yawns, a physiological response, can
nevertheless convey information about the
internal/affective state (e.g. threat yawns) of
the yawner that can be used by group members to
modify their behavioural response according to
specific contexts (Deputte, 1994; Guggisberg et
al., 2010; Leone et al., 2014; Zannella et al.,
2015). One phe- nomenon that seems to support
this hypothesis of yawning is its contagious
nature (Provine, 1986). Contagious yawning, a
behav- ioural response provoked automatically by
viewing or listening to others' yawns (Provine,
2005), has been demonstrated in humans and
several nonhuman species (humans, Anderson,
2020; Chan & Tseng, 2017; Cooper et al.,
2012; Franzen, Mader, & Winter, 2018;
Giganti & Esposito Ziello, 2009; Giganti
& Zilli, 2011; Norscia & Palagi, 2011;
Platek, Critton, Myers, & Gallup, 2003;
Provine, 1986, 1989; chimpanzees, Amici, Aureli,
& Call, 2014; Anderson, Myowa-Yamakoshi,
& Matsuzawa, 2004; Campbell, Carter,
Proctor, Eisenberg, & de Waal, 2009;
Campbell & de Waal, 2011, 2014; Madsen,
Persson, Sayehli, Lenninger, & Sonesson,
2013; Massen Vermunt & Sterck, 2012;
bonobos, Pan paniscus, Demuru & Palagi,
2012; Tan, Ariely, & Hare, 2017; geladas,
Palagi, Leone, Mancini & Ferrari, 2009;
wolves, Canis lupus lupus, Romero, Ito, Saito
& Hasegawa, 2014; domestic dogs, Canis lupus
familiaris, Neilands et al., 2020, Romero,
Konno, & Hasegawa, 2013; domestic pigs, Sus
scrofa, Norscia, Coco, Robino, Chierto &
Cordoni, 2021; sheep, Ovis aries, Yonezawa,
Sato, Uchida, Matsuki, & Yamazaki, 2016;
budgerigars, Miller et al., 2012; African
elephants, Rossman, Padfield, Young, Hart &
Hart, 2020). Although the issue is still un- der
debate (Adriaense, Koski, Huber, & Lamm,
2020; Gallup & Massen, 2020; Kis, To th,
Kanizsa r, & Topa l, 2020; Massen &
Gallup, 2017; Neilands et al., 2020), yawn
contagion is considered a proxy of emotional
contagion since the phenomenon has been found to
be modulated by the level of social attachment
between the interacting partners (Campbell &
de Waal, 2011; Norscia, Zanoli, Gamba, &
Palagi, 2020; Palagi, Celeghin, Tamietto,
Winkielman, & Norscia, 2020; Romero et al.,
2014, 2013; Tan et al., 2017).
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- One of the most parsimonious explanations
for yawn contagion is the so-called 'chameleon
effect' (Chartrand & Bargh, 1999). This
predicts that the perception of a behaviour
leads to unconscious imitation by the observer
that in turn provokes an alignment, or
convergence, of behaviours (Arnott, Singhal
& Goodale, 2009; Lakin & Chartrand,
2003; Palagi & Cordoni, 2020). This
convergence is highly adaptive because it can
foster social cohesion, coordination and
synchrony between subjects that do not
necessarily share strong affiliation (Clay &
de Waal, 2013; Lakin, Jefferis, Cheng, &
Chartrand, 2003; Palagi et al., 2020; Preston
& de Waal, 2002; Prochazkova & Kret,
2017). For example, the synchronization of
movements and vigilance activities in a group
can increase the effectiveness of resource
exploitation (e.g. hunting) and defence from
predators (Duranton & Gaunet, 2016).
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- Lions are a good model to explore the
yawning phenomenon. Among felids, lions are the
most social species (Bertram, 1975) whose social
structure is characterized by fission-fusion
dynamics (Mosser & Packer, 2009; Packer,
Pusey, & Eberly, 2001). Moreover, a recent
social network analysis revealed that cohesion
and conver- gent activities are fundamental for
the success of a group (Dunston et al., 2016).
Here, we tried to identify the contexts in which
spontaneous yawning occurs and whether yawn
contagion is pre- sent in a wild population of
lions. To do this, we tested the drowsiness,
arousal and social communicative hypotheses,
which, owing to the versatile nature of yawning,
are not necessarily mutually exclusive.
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- Rudnai (2012) observed that most yawning in
wild lions occurred during the resting periods
and, particularly, during the transition from
sleeping to being awake. This finding suggests
that in lions yawning can be linked to changes
in mood/state (e.g. from sleep to being awake or
vice versa; from lying down to licking a
groupmate). If yawning, as in other mammals
(Guggisberg et al., 2010; Guggisberg, Mathis,
Herrmann, & Hess, 2007; Leone et al., 2014;
Palagi et al., 2019; Zannella et al., 2015), is
a mechanism signalling a switch between
different moods/states, we predicted it to be
significantly more frequent during relaxed
contexts, charac- terized by a fluctuation in
resting/sleeping/affiliative behavioural
patterns, than during contexts characterized by
motor activity such as moving or hunting
(Prediction 1a).
- In Japanese macaques and grey-cheeked
mangabeys, Lophoce- bus albigena, Deputte (1994,
p. 238) found that 'yawn duration was influenced
by the activity or emotional level of the
yawner'; yawns with a long duration were
significantly more frequent during pe- riods of
relaxation than during periods of locomotor
activity or other physiologically arousing
contexts (e.g. agonistic context). If relaxation
is one of the main proximate factors (sensu
Tinbergen, 1963) determining the duration of
yawning, we predicted animals would perform
long-lasting yawns when relaxed (Prediction
1b).
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- Since lions are active throughout the 24 h
daily cycle and engage in relaxing activities
both during the night and during the day
(Hayward & Hayward, 2006; Schaller, 1972),
we predicted no dif- ference in the frequency
and duration of spontaneous yawning between
night and day (Prediction 2).
- In a study on a captive group of lions,
Baenninger (1987, p. 351) reported that subjects
increased their level of yawning just before
food provisioning and that the yawning frequency
tended to decrease in the postfeeding period
'During the morning there were relatively few
yawns (0.8/lion-hour), but there was a
progressive increase before feeding time (to 1.8
yawns/lion hour between 1:00 and 2:00 p.m.).
During and after feeding there was a sharp
decline in the frequency of yawns (0.35
yawn/lion-hour)'. In agreement with Deputte's
(1994) findings, in Sulawesi macaques, Macaca
nigra, short yawns were observed in aroused
individuals during situations of high social
tension such as immediately after object shaking
or stamping, two behavioural patterns
characterized by high levels of
locomotor/arousal activity (Thierry, Bynum,
Baker, Kinnaird, Matsumura, & et al, 2000).
If yawning is a behavioural response linked to
the arousal state of the subjects, we predicted
that spontaneous yawning would increase during
contexts with
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- high social tension, for example when
animals are competing for access to a clumped
food resource such as a carcass (Prediction 3a).
Moreover, we predicted that yawning events would
be shorter under arousing than under relaxed
circumstances (Prediction 3b).
- Compared to other carnivore taxa, felids
tend to yawn at a higher frequency (Leyhausen,
1956). Rudnai (2012) observed that wild lions
tend to yawn in chorus with two or more
individuals yawning within 14 min after viewing
others' yawns. In agreement with Rudnai's
anecdotal observations and due to the social
cohe- sion characterizing the groups of wild
lions, we predicted that yawn contagion would be
present (Prediction 4). If yawn contagion has a
role in the social alignment of animals'
activities (Vick & Paukner, 2010), we
predicted that those subjects that respond with
a yawn to the first yawner will also show
behavioural convergence by replicating the exact
motor pattern the first yawner performs
immediately after yawning (Prediction 5).
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- DISCUSSION
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- This is the first systematic study on the
yawning activity in wild lions. Yawning tended
to be frequent during relaxing and moving, two
activities that often involved all group members
at the same time (Prediction 1a drowsiness
hypothesis partially supported; Fig. 3).
Moreover, we found that the frequency of the
yawns and their duration did not differ between
the day and night in agree- ment with the 24 h
resting cycle of lions (Hayward & Hayward,
2006; Schaller, 1972; Prediction 2 drowsiness
hypothesis supported).
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- In wild lions, spontaneous yawning
punctuated the switch be- tween sleeping and
being awake, between lying and sitting and
between sitting and standing and vice versa,
being particularly frequent during the relaxing
contexts which involved many of these switches.
Since relaxing contexts occurred during both the
day and the night, the similar distribution of
yawning in these periods supports the drowsiness
hypothesis (Guggisberg et al., 2007, 2010). This
is in line with previous descriptions provided
by Rudnai (2012, p. 45) on the presence of
yawning in this species: 'All yawning observed
(ninety-five individual observations) occurred
between 1530 and 1830 hours, indicating that
lions [...], do not usually yawn before
sleeping but only after resting'. In our case,
it was not possible to determine whether the
animals were sleeping; however, the lions
alternated periods of total inactivity (lying
down) with periods of low activity (moving
slightly, changing po- sition, sometimes sitting
and engaging in affiliative interactions).
Moreover, Baenninger (1987) observed that lions
often yawned when they were lying down, thus
suggesting that the behaviour was linked to a
relaxed state. The link between yawning and pe-
riods of relaxation has been found in several
mammalian species, including humans (Zilli,
Giganti, & Salzarulo, 2007). In geladas,
yawning is context dependent: during periods of
relaxation and affiliative interactions, geladas
yawn with the teeth and gums covered (Leone et
al., 2014). In Verreaux's sifakas and ringtailed
lemurs, Zannella et al. (2015) demonstrated that
yawning was particularly frequent during the
behavioural switches during relaxed contexts
(e.g. sleep/awake, sitting/lying). Our results
show that in wild lions, yawning was also linked
to moving, another activity that mostly involves
all members of the group which frequently
alternate walking and standing. Since our
observations were not uniformly distributed over
the 24 h cycle, it would be interesting to
expand the data collection to additional time
windows (e.g. 2200e0500) to describe more
precisely the daily fluctuation in spontaneous
yawning across the different contexts.
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- We did not find any empirical evidence in
support of the arousal hypothesis. Indeed,
yawning frequency did not peak during
competition over clumped food (Prediction 3a
arousal hypothesis not supported; Fig. 3). The
high frequency of agonistic contacts we recorded
in wild lions indicates that feeding was
characterized by a high level of social tension.
The low frequency of yawning we recorded in this
context cannot be because the lions were using
their mouths to feed, as not all group members
could feed at the same time. If yawning is a
sign of arousal/frustration, we would expect to
find a peak frequency in lions that had to wait
or fight to have access to the carcass. Our
finding is not in agreement with the data
obtained by Baenninger (1987) who reported that
captive lions increased their level of yawning
just before food provisioning (at 1500) and that
the yawning frequency tended to decrease after
feeding. It is possible that the distribution of
food in a confined space with few escape
opportunities could increase levels of anxiety
in animals, thus stimulating their yawning
activity. Owing to the polyfunctional nature of
yawning, additional data, in both wild and
captive conditions, would help us understand
whether it can be an indicator of anxiety in
lions as it is in other species (Tonkean
macaques, Zannella et al., 2017; budgerigars,
Miller et al., 2010; South American sea lions,
Palagi et al., 2019; rats, Kubota, Amemiya,
Yanagita, Nishijima, & Kita, 2014; Nazca
boobies, Liang et al., 2015).
- Unlike some primate species, which engage in
shorter yawns during periods of high social
tension and arousal (longtailed ma- caque,
grey-cheeked mangabey, Deputte, 1994; Sulawesi
macaque, Thierry et al., 2000), in wild lions we
did not find any difference in the mean duration
of yawning events across the three contexts
considered (relaxing, feeding, moving). This
basic uniformity in the duration and execution
of the behaviour (Fig. 1) makes the inter-
pretation of yawning even more difficult in this
species.
-
- Yawning seems to have an important social
communicative role in wild lions (social
communicative hypothesis, Guggisberg et al.,
2010). We found that contagious yawning was
present in this species (Prediction 4 contagious
yawning hypothesis supported; Figs. 2 and 4) and
that, after being infected by others' yawns,
both juveniles and adults tended to align their
subsequent motor actions (Figs. 2 and 5) thus
suggesting that yawn contagion can have a role
in promoting synchrony in group activity
(Prediction 5 effect of yawn contagion on motor
convergence supported). This supports the
hypothesis proposed by Vick and Paukner (2010)
predicting that yawning can be a reliable
indicator of change in activity state and may
help synchronize group behaviours.
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- The yawning response mostly occurred within
the first minute (75.47%) after the yawning
stimulus was seen. The short latency in the
response would be particularly adaptive if
animals need to coordinate their movements in
the minutes immediately following the yawn
contagion event. This response latency is
similar to that observed in human (Norscia &
Palagi, 2011) and nonhuman pri- mates (bonobo,
Demuru & Palagi, 2012; chimpanzee, Campbell
& Cox, 2019; gelada, Palagi et al., 2009),
in which yawn contagion typically peaks within
the second minute after the triggering
stimulus.
- In lions, most maintenance activities are
collectively performed by engaging in
cooperative behaviours (Borrego, 2019; Packer
& Ruttan, 1988; Rudnai, 2012; Schaller,
1972). Lions cooperate in hunting (Packer &
Pusey, 1997), territory defence (Grinnell, 2002;
Heinsohn, & Packer, 1995; Heinsohn, Packer,
& Pusey, 1996; McComb, Packer, & Pusey,
1994; Mosser & Packer, 2009) and rearing
their offspring (Packer & Pusey, 1994).
Since lion society is free from the tolerance
constraints imposed by rigid dominance
hierarchies, the species has been defined as
egalitarian (Borrego, 2019; Packer et al.,
2001). Rudnai (2012) proposed that utilitarian
interactions, which are strongly adaptive, can
also serve to strengthen the bond between group
members. Through social network analysis,
Dunston et al. (2016) demonstrated that social
cohesion and stability are central to the
success of a lion group. The presence of yawn
contagion and its effect on subsequent behav-
iours of interacting subjects can foster the
synchronization of motor activity, thus leading
to group coordination, stability and
cohesion.
-
- Yawn contagion and its short response
latency have often been interpreted in the light
of emotional contagion, a basic building block
of empathy (Palagi et al., 2009, 2020; Preston
& de Waal, 2002; Romero et al., 2013, 2014).
However, this issue is still under strong debate
not only in nonhuman animals (canids, monkeys,
great apes), but also in humans (Adriaense et
al., 2020; Gallup, 2021; Massen & Gallup,
2017; Neilands et al., 2020). To our knowledge,
motor convergence following episodes of
contagious yawning has never been explored in
other species. Yet, focusing on the immediate
effects of yawn contagion could represent an
important step in shedding light on the
short-term benefits that underlie the evolution
of yawn contagion and, possibly, emotional
contagion.
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