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
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 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

mise à jour du
17 juillet 2022
Anim Cogn
2023 Mar 16
 

 Contagious yawning in African painted dogs
Kanako Ake, Nobuyuki Kutsukake
 
Department of Evolutionary Studies of Biosystems, Sokendai
Hayama, Kanagawa, Japan

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 Tous les articles sur la contagion du bâillement
All articles about contagious yawning
 
Abstract
Contagious yawning (CY), which is yawning elicited by sensing another yawning, has been observed only in social species and is considered linked to high sociality. Although this idea&emdash;the social communication hypothesis&emdash;is supported by pre- vious studies, investigating the occurrence of CY in various species remains necessary.The authors investigated the occurrence of CY in one of the most social canine species, the African painted dog (Lycaon pictus). We recorded 1387 yawn events from five pairs (10 individuals) in captivity. Temporal analysis showed that subsequent yawns occurred frequently within 15 s or 30 s after spontaneous yawns (SYs). SYs that were detectable by another individual (i.e., visible to the other individual or performed in close proximity) were more likely to elicit subsequent yawns by the other individual. However, the influence of contextual factors on CY differed according to the time window, implying that a conservative time window should be used to reduce overcounting of CY and misattribution of its determinants. The proportion of CY was positively related to time spent in physical proximity to another, a proxy for a social bond. Overall, our results provide the first evidence of CY in African painted dogs and further support the notion that such behavior is prevalent among social animals. They also strongly imply that an appropriate time window should be used to define yawn contagion.
 
Résumé
La contagion du bâillement, c'est-à-dire le bâillement provoqué par la perception d'un autre bâillement, n'est observé que chez les espèces ayant une vie sociale. Elle et est considérés comme liée à une grande sociabilité. Bien que cette idée - l'hypothèse de la communication sociale - soit étayée par des études antérieures, il reste nécessaire d'étudier l'occurrence de la contagion du bâillement chez diverses espèces. Les auteurs ont étudié l'occurrence de cette contagion au sein d'une des espèces canines à vie sociale évoluée, le chien Lycaon pictus. Ils ont enregistré 1387 bâillements chez cinq paires d'individus en captivité. L'analyse temporelle a montré que les bâillements déclenchés se produisaient fréquemment dans les 15 s ou 30 s après les bâillements spontanés (émetteur). Les bâillements spontanés détectables par un autre individu (c'est-à-dire visibles par l'autre individu ou effectués à proximité) étaient plus susceptibles de provoquer des bâillements ultérieurs chez l'autre individu. Cependant, l'influence des facteurs contextuels sur cette contagion diffère selon la temporalité, ce qui implique d'éviter l'attribution erronée de ces bâillements (synchronisation des activités identiques liée aux rythmes circadiens et sans lien avec la réelle contagion).

 
Yawning is of interest as an evolutionarily conserved motor action observed across diverse taxa. Numerous functional hypotheses have been proposed for yawning. Some of these hypotheses focus on physiological functions: absorbing much oxygen into the body (the respiratory hypothesis); stimulating the body under exhausted or sleepy states (the stress-related arousal hypothesis); and cooling the brain by absorbing cool air (the brain-cooling hypothesis). The social communication hypothesis, on the other hand, states that yawning functions as a social cue or signal to express physiological or emotional status to other individuals (Guggisberg et al. 2010; Gallup 2022).
 
The social communication hypothesis has been supported by the phenomenon that sensing other individuals yawning often elicits yawning in humans (Krestel et al. 2018). Such contagious yawning (CY) is categorized into automatic mimicry or emotional contagion, which is both considered to promote synchronization among group members (Palagi et al. 2020). Thus, the social communication hypothesis predicts that animals with a high degree of cooperative inter- action among group members will show CY (Palagi et al. 2020; Norscia et al. 2021). Behavioral studies have tested this prediction and found that group-living animals show CY (Gallup 2022). Moreover, the social communication hypothesis predicts that CY promotes behavioral synchronization within a group, which has been observed in lions (Panthera leo, Casetta et al. 2021). The hypothesis further predicts a positive relationship between the frequency of CY and relationship closeness. Indeed, yawning is more contagious between bonded individuals than between weakly bonded individuals in humans (Homo sapiens, Norscia et al. 2020), bonobos (Pan paniscus, Palagi et al. 2014), chimpanzees (Pan troglodytes, Demuru and Palagi 2012; Campbell and de Waal 2011), wolves (Canis lupus lupus, Romero et al. 2014), and domestic pigs (Sus scrofa, Norscia et al. 2021).
 
Several studies, however, failed to demonstrate the relation- ship between the frequency of CY and relationship closeness (e.g., budgerigars, Melopsittacus undulatus, Gallup et al. 2015; see review by Massen and Gallup 2017). Although empirical studies of the occurrence and determinants of CY have accumulated, at least two points require further examination. First, the phylogenetic distribution of CY remains unclear, as systematic research on diverse species is limited (Gallup 2010; Guggisberg et al. 2010). Thus, research on the occurrence of CY in diverse taxa is needed. Second, a methodological controversy exists regarding the definition of CY. The prevalent method of determining CY involves evaluating the frequency of yawning within a defined temporal interval, with and without prior exposure to yawning stimuli from another individual. The majority of these studies have defined CY as all following yawns within 3&endash;5 min after the detection of a yawn by another individual. However, this time window has been noted to be too long for determining whether the following yawn is spontaneous or contagious (Massen and Gallup 2017).
 
For example, in bonobos, the occurrence of CY is detected only early in the time window (i.e., the first minute), not in the second or third minute (Norscia et al. 2022). As such, the use of an arbitrary time window can result in an inaccurate determination of CY. To date, no studies have examined the impacts of different time windows on biological conclusions, such as attribution of the determinants of CY. If the peak time window in which a response yawn follows a preceding spontaneous yawn (SY) is less than 3 min in the studied species, overcounting of CY due to the inclusion of SY or misattribution of the contextual or social factors influencing CY could occur. Other methodologies have been used for CY studies (e.g., Romero et al. 2014; Miller et al. 2012; Massen et al. 2016; Gallup et al. 2022). Some stud- ies showed video clips of yawning to subject animals (e.g., Amici et al. 2014; Reddy et al. 2016; Pedruzzi et al. 2022).
 
Here, we conducted behavioral observations of yawning in one of the most social canine species, the African painted dog (Robbins 2000; Walker et al. 2017). This cooperatively breeding carnivore lives in a cohesive group of 3&endash;20 members per pack. This species exhibits various social behaviors, including synchronized actions (Walker et al. 2017), cooperative hunting, and food sharing (regurgitation to pups or weakened adult individuals, Creel and Creel 1995). They have the largest repertoire of vocal communication among canids, which depends on social context (Robbins 2000). Based on the cooperation scores proposed by Smith et al. (2012), canine species show uniquely strong cooperative behavior, with the highest score for cooperation in African painted dogs. Thus, this species is an ideal subject for studying the occurrence of CY.
 
Previous studies using the time window method have confirmed that the peak time window in which CY occurs is clearly shorter than 3 min (Table 1). Therefore, we first examined whether successive yawns by two individuals occurred within a relatively short time window. To this end, we examined the peak time window in which CY occurred frequently to determine an appropriate time window for operationally defining CY in this species. To assess the occurrence of CY, we tested whether yawning is contagious when an individual can detect another individual yawning. If this species exhibits CY, individuals will yawn more frequently after visible SYs than after nonvisible yawns (Prediction 1a), as well as when two individuals are in close proximity than at a distance (Prediction 1b). Next, we predicted that different contextual or social factors would affect the occurrence of CY depending on the time window used for the operational definition (Prediction 2). We tested this through a comparison of the results obtained using different time windows. Furthermore, as bonded individuals tend to detect the actions of others (Massen and Gallup 2017), yawning should be detected by bonded individuals, resulting in a high frequency of CY in such individuals. Therefore, we predicted that strongly bonded pairs would show CY more frequently than weakly bonded pairs (Prediction 3).
 
 
Discussion
 
We found that yawn contagion occurred immediately after visible SYs, with steep and gradual peak windows observed within approximately 15 and 30 s, respectively). Model 1 showed that responders yawned more frequently after visible SYs than after nonvisible SYs, supporting Pre- diction 1a (Table 3). The positive effect of visibility of SYs on FYs is a key factor used to define the occurrence of CY in previous studies (e.g., Gallo et al. 2021; Casetta et al. 2021). Model 1 revealed that physical proximity between the trigger and responder during an SY positively affected the occurrence of FYs (Table 3). This result supports Prediction 1b. A similar effect of physical proximity on CY has been reported in previous studies (e.g., Norscia et al. 2021). As African painted dogs show less facial expression than other social canine species such as wolves (Kleiman 1967; Fox 1971), they may require close proximity to detect a trigger. However, once they detect others yawn, one yawn is sufficient to elicit CY, as indicated by our finding that the number of SYs did not affect the occurrence of CY. The effect of the detectability of SYs and our observation of FY occurrence immediately after SYs imply that African painted dogs exhibit CY. Other social canine species also exhibited CY (wolves: Romero et al. 2014). While some studies showed CY of domestic dogs (Canis lupus familiaris) in response to human yawning (e.g., Joly-Mascheroni et al. 2008), the results are controversial (e.g., Buttner and Strasser 2014; Harr et al. 2009). In addition, CY in response to conspecifics has not yet been demonstrated (Harr et al. 2009).
 
Our analysis implies that the selection of an appropriate time window is critical. Using a 3 min time window to define CY could lead to overcounting yawns as CYs, as proposed previously (Massen and Gallup 2017). We should note that some yawns occurring in the 15 s and 30 s time windows could also be incorrectly categorized as CY. How- ever, the frequency of the misidentification of SY as CY in the 3 min window led to notable overcounting. Some studies have shown that the peak CY occurrence times are within 1 min or less; nonetheless, arbitrary time windows are commonly used to define an FY after a trigger yawn as a potential CY (Table 1). Campbell and Cox (2019) showed that the 3 min time window is suitable for chimpanzees, but noted that the same result would not be expected for other species. To minimize overcounting and misevaluation, time windows for FYs shorter than 3 min have been used in some studies (i.e., Demuru and Palagi 2012; Wojczulanis-Jakubas et al. 2019; Miller et al. 2012). If CY is truly a type of motor mimicry, CY would be predicted to occur within about 5 s after an SY, in accordance with other motor mimicry behaviors (Prochazkova and Kret 2017). In this study, frequent FYs indeed occurred between 3 and 8 s after SYs (Fig. 2). Most previous studies, however, did not subdivide the observation window into shorter periods of 30 s less (however, 20 s was arbitrarily selected by Wojczulanis-Jakubas et al. 2019). Subdivision of the time window and consideration of species-specific peak time windows are essential to avoiding missing CY or misattributing an SY as CY.
 
Model 1 indicated that the difference among time win- dows affected the results for significant explanatory variables, which supported Prediction 2. We found a negative effect of distance between the trigger and responder during an SY on the proportion of FYs when using the 15 and 30 s time windows but not the 3 min time window. Similarly, different effects on CY frequency were found with different time windows (Table 4), as reported in previous studies. In humans and bonobos, Palagi et al. (2014) defined all FYs within 3 min after an SY as CY. Their study showed that frequent CY occurs among strongly bonded individuals in the first minute, whereas CY among weakly bonded individuals is more frequent in the second and third minute. Based on this result, they suggested that the latency of CY differs according to familiarity. In wild gelada baboons, CY was confirmed when the analysis employed a time window including the peak time (the second minute) but not when the analysis considered only the first minute (Gallo et al. 2021). The results of these studies raise the possibility that some reported CY actually included SYs due to the use of too-long a time window, indicating that species-specific time windows should be used to define CY and evaluate the fac- tors affecting CY.
 
Hereafter, we discuss testing predictions using the results for FYs within 30 s, as the results did not differ between the 15 s and 30 s time windows. In agreement with Prediction 3, the proportion of time spent in physical proximity per day positively affected the proportion of CY per individual per day. Similarly, previous studies have shown that CY occurs more frequently in more strongly bonded pairs of individuals than in weakly bonded pairs as measured based on affilia- tive behavior (Demuru and Palagi 2012; Palagi et al. 2014; Gallo et al. 2021; Norscia et al. 2021; but see Gallup et al. 2015). All pairs of individuals in this study were related and bonded to the extent that they could live in a limited space with no severe fights, as the pairs were selected by zoo staff based on observed social interactions. Our scan sam- pling implied that paired individuals spent approximately half of the time within 1 BL of each other (mean = 0.44, standard deviation = 0.12), which allowed them to detect the SYs. Such same-sexed relatives with strong social bonds can be found in the wild, in which related same-sex siblings disperse and form a pack by encountering an opposite-sex group (Creel and Creel 2002). They maintain close distances and frequently interact with group members to synchronize their behaviors, using cues such as sneezing before departure for hunting (Walker et al. 2017). Strongly bonded pairs are more likely to detect facial expressions than weakly bonded pairs (i.e., attention bias; Massen and Gallup 2017). There- fore, it is plausible that the stronger the bond of a pair is, the more reliably they can detect SYs from each other, resulting in more frequent CY.
 
In summary, this is the first study demonstrating CY in the African painted dog, one of the most social canine species. Our results have at least two general implications. First, the occurrence of CY in this species is in line with the idea that social species exhibit CY. African painted dogs show various social behaviors that require coordination with other pack members (e.g., cooperative hunting). The social communication hypothesis predicts that CY occurs in species with a high degree of cooperative interaction among conspecifics (Guggisberg et al. 2010). In addition, previous studies have shown that species with few cooperative interactions between individuals do not exhibit CY, such as gorillas (Amici et al. 2014; Palagi and Norscia 2019) and red-footed tortoises (Wilkinson et al. 2011, Table 1). However, some studies of CY on social species have failed to show CY due to rare occurrences of yawning during observations (e.g., ravens, Corvus corax: Gallup et al. 2022; common marmosets, Callithrix jacchus: Massen et al. 2016). Accumulating data regarding CY in both social and nonsocial species will be required to test the social communication hypothesis. As a second general implication, our results show that the most commonly used arbitrary time window was not appropriate for detecting CY in this species. Using an appropriate time window based on the peak timing of CY in each species, rather than a conventionally used but arbitrary time window that may not fit the study species, is essential to evaluate the presence of CY and the contextual or social factors affecting CY frequency.