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La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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mystery of yawning 

 

 

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mise à jour du
28 mars 2019
J Comp Psychol
2019
Lowland gorillas (Gorilla gorilla gorilla)
failed to respond to others' yawn:
Experimental and naturalistic evidence. 
Palagi E, Norscia I, Cordoni G.  

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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.