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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
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mise à jour du
19 juin 2020
Front. Vet. Sci
08 May 2020
Contagious Yawning in African Elephants
(Loxodonta africana):
Responses to Other Elephants and Familiar Humans  
Rossman ZT, Padfield C, Young D, Hart BL, Hart LA  
 

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Rossman ZT , Hart BL, Greco BJ, Young D, Padfield C, Weidner L, Gates J, Hart L. Yawning Occurs in Elephants
Front. Vet. Sci. 28 February 2017
 
Abstract
While spontaneous yawning is common across all vertebrate classes, contagious yawning is less common and has been observed only in a few species of social animals. Interspecific contagious yawning in response to yawning by humans has been observed only by chimpanzees and dogs. After confirming additional occurrences of intraspecific contagious yawning in a group of captive African elephants previously studied, we further investigated the potential for the same group of elephants to engage in interspecific contagious yawning with familiar human handlers. Ten captive African elephants, most of whom had been previously studied, were observed over 13 nights for evidence of intraspecific contagious yawning. Seven of these elephants were also involved in trials where familiar handlers performed staged yawns, as well as trials with staged non-yawning gapes, or trials with no yawns or gapes. Incorporating previously collected contagious yawning data, we describe nine instances of intraspecific contagious yawning in the elephants. Three of the seven elephants yawned contagiously in response to humans during the interspecific yawning trials. This is the first report of interspecific contagious yawning by elephants in response to yawns by familiar humans.
 
 
Bâillements contagieux d'éléphants en réponse à des bâillements d'humains familiers
 
Alors que le bâillement spontané s'observe dans toutes les classes de vertébrés, le bâillement contagieux est moins courant et n'a été observé que chez quelques espèces d'animaux sociaux. Le bâillement contagieux interspécifique en réponse au bâillement par l'homme n'a été observé que par les chimpanzés et les chiens. Après avoir confirmé des occurrences supplémentaires de bâillements contagieux intraspécifiques dans un groupe d'éléphants africains captifs précédemment étudiés, nous avons approfondi la possibilité pour le même groupe d'éléphants de s'engager dans des bâillements contagieux interspécifiques avec des soigneurs humains familiers.
 
Dix éléphants africains en captivité, dont la plupart avaient déjà été étudiés, ont été observés pendant 13 nuits pour visualiser leurs bâillements contagieux intraspécifiques. Sept de ces éléphants ont également participé à des essais où des soigneurs familiers (ou cornacs) effectuaient des bâillements répétés, ainsi que des essais avec des ouvertures de bouche banales, ou des essais sans bâillements ni bouche ouverte.
 
En incorporant les données de bâillements contagieux précédemment collectées, nous décrivons neuf cas de bâillements contagieux intraspécifiques chez les éléphants. Trois des sept éléphants ont bâillé de manière contagieuse en réponse aux humains lors des essais de bâillements interspécifiques. Il s'agit du premier signalement de bâillements contagieux interspécifiques d'éléphants en réponse à des bâillements d'humains familiers.
Introduction
Spontaneous yawning is an ancestral trait that has been identified in many species across all classes of vertebrates (1). There are several hypotheses relating to the function of yawning, but it is generally accepted that yawning relates to a state change and plays a role in brain activation (1, 2). While spontaneous yawning is an ancestral trait, involving the older parts of the brain, contagious yawning, in which an animal yawns upon seeing another yawn, is thought to be controlled by the neocortex which is essential for complex social interactions (3). Contagious yawning with conspecifics (intraspecific contagious yawning) has been reported in several species of social animals including humans, chimpanzees, baboons, wolves, sheep, and budgerigars (4&endash;9). These studies generally show a positive relationship between familiarity among the participants and likelihood of yawning.
 
Contagious yawning between members of different species (interspecific contagious yawning) has been observed between humans and chimpanzees as well as humans and dogs (10&endash;13). Interestingly, yawn contagion has been reported in different situations between humans and dogs, but not between dogs. In the studies of contagious yawning with humans in both dogs and chimpanzees, there was no evident difference in yawning responses to familiar versus unfamiliar humans; this was also the case in a study looking at contagious yawning by chimpanzees in response to an android (14).
 
Contagious yawning is, by nature, a social behavior, but it is not entirely clear what communicative function it serves. Several investigators associate the phenomenon with empathy (4&endash;8). Other investigators have questioned the link to empathy (15). In humans, a contagious yawn can be prompted not only by seeing a yawn, but also by hearing or even thinking about a yawn (16, 17).
 
Since African elephants have a highly developed cognitive brain (18, 19), and are a social mammal adapted for group living, it is reasonable to expect that they would exhibit contagious yawning with other familiar elephants. Our previous study investigated yawning behavior in captive African elephants at the same study site as the present study, reporting 6 instances of contagious yawning (20), 4 of which were by standing elephants.
 
As background information for the frequency of yawning by standing elephants at night, in the previous study, we accumulated 73.3 h of observations in the nighttime enclosure; this excluded all 2-min periods that were associated with an elephant arousing. During these non-arousing time periods, we observed only 4 spontaneous yawns by the standing elephants, meaning that the rate of a standing elephant spontaneously yawning apart from the 2-min periods of an arousing elephant that might be yawning was 0.055 yawns/h (4 yawns/73.3 h), or one yawn in over 18 h. Spontaneous yawns by standing elephants outside of arousal episodes within the group thus were extremely rare. This previous study, along with information about elephant-initiated interactions with people at the same study site (21), provided the context for the current study.
 
One goal of the present study was to confirm and expand upon our previous descriptions of intraspecific contagious yawning among the same group of elephants, at a different time and with some changes in the group composition. The second goal was to determine if the human handlers that regularly interacted with the elephants during the day would evoke yawning from the elephants by yawning in a manner similar to that used in the studies of humans evoking yawns from dogs and captive chimpanzees. These observations were conducted in the early morning, outside the nighttime enclosure, a time when spontaneous yawning would be highly unlikely.
 
The setting of this study included videorecording of the behavior of the elephants freely moving at night; these recordings were available for perusal later by an investigator. The structured interactions of the handlers with the elephants each morning were a daily routine. As noted, the occurrence of contagious yawning is rare compared with spontaneous yawning, so the number of elephants exhibiting intraspecific and/or interspecific contagious yawns by elephants was expected to be small. With elephants, where opportunities to record some behaviors is limited, but the behaviors are meaningful in understanding elephants' comparative behavior, a documented occurrence in just a few individuals is important. The parameters used in designating a yawn as contagious are presented in detail. Recent examples of reports of just one or two instances of elephant behavior, where details are given, are of sleeping bouts in two wild African elephants in nature (22) and self-identification in a mirror by one elephant (23).
 
Discussion
Intraspecific Contagious Yawning
The results from our nighttime observations, with three instances of contagious yawning meeting the specific criteria, expand upon and confirm our previous report of intraspecific contagious yawning between elephants (20). There were two instances where a standing elephant yawned in response to an arousing elephant yawning and one from a standing elephant yawning in response to another standing elephant yawning. This latter instance expands the contexts in which contagious yawning in African elephants may be expected to occur. The most frequent context is that where a standing elephant yawns in response to yawning by an elephant arousing or just after arousing and standing. The next most frequent context is an arousing elephant yawning in response to yawning by another arousing elephant. This was not seen in this present study, but was seen in the previous study. The third context is a standing elephant yawning in response to yawning by another standing elephant. To address the issue of a spontaneous yawn occurring in a standing elephant being mistaken for a contagious yawn, we calculated the probability of a spontaneous yawn by a standing elephant, being < 0.001. Table 1 outlines the nine occurrences of intraspecific contagious yawns seen in the two studies. The varieties of contexts are mindful of the different contexts of contagious yawning in humans, ranging from directly looking at another person, to just hearing someone talking about yawning (4, 16).
 
Interspecific Contagious Yawning
Trials to test for interspecific yawning were conducted early in the morning when the elephants had just been taken from the nighttime enclosure. This was a few hours after the time when spontaneous yawning and contagious yawning between elephants had been observed. As noted in the introduction, spontaneous yawning was almost always seen in association with arousal from recumbent sleeping or resting bouts, and not at other times. Thus, yawns that occurred during these handler trials are unlikely to have been spontaneous.
 
The testing protocol followed was similar to that used in trials with dogs and chimpanzees to observe for yawning by the animal in response to yawning by the human that was facing the animal. In trials on dogs and chimpanzees, the human yawned several times before a yawn occurred by the animal, if it occurred. The durations and patterns of contagious yawning in handler trials were typical of spontaneous yawns and of those seen in the contagious yawns between elephants. In contrast with prior studies investigating interspecific contagious yawning, our study was conducted using only familiar humans. We do not know if elephants would respond contagiously to the yawn of a strange human.
 
The observations of Keisha during yawning trials, in which she initially yawned in response to the handler's yawn and then yawned several times during her control and gape trials, and those of other elephants, provide evidence for her yawns being provoked in ways other than directly seeing a yawn. Given that spontaneous yawning is infrequent during periods of time not associated with arousal, it is unlikely that Keisha's prevalent yawning was occurring as spontaneous yawns. This yawning behavior by Keisha seems analogous to observations on human yawning being triggered by thinking about a yawn (17), suggesting that Keisha began to associate the trial context with handlers yawning. An alternative explanation is that the yawning was a reflection of the positive reinforcement from the handler after her initial contagious yawn, implying that she then began yawning deliberately due to the positive association of yawning with praise. Both possibilities illustrate the involvement of the neocortex in contagious yawning (discussed in the introduction), as opposed to spontaneous yawning.
 
Whether yawning, let alone contagious yawning, occurs in wild free-ranging African elephants has not been investigated at this point. The study of two matriarchs in Botswana from two herds of free-ranging wild elephants, using a trunk-movement proxy for sleep, found that the elephants slept about 2 h per night, standing or in recumbency (22). There was no video recording of the elephants, so it is unknown whether or not contagious yawning, or even spontaneous yawning, may have occurred. Based on our studies, elephant yawns are rather subtle. mostly occurring at night, and would likely be missed by observers of wild elephants.
 
Including the first interspecific yawn of Keisha, we documented six interspecific yawns in three elephants. While the number of yawns is small, the observations meeting specific criteria should be sufficient to establish that elephants can, and do, display yawning in response to seeing a familiar human yawning. As mentioned above, at least two other notable behaviors have been recently documented in elephants based on just one or two individuals: nighttime sleeping (22) and self-recognition in a mirror (23).
 
A possible function of contagious yawning among elephants living in nature, assuming it occurs, and based on the presumed function of yawning, is brain arousal and activation. Yawning by an arousing elephant, leading to a contagious yawn from elephants already awake, or another simultaneously arousing elephant, could facilitate a state of higher awareness and arousal throughout the herd. Although our data are on captive elephants, these elephants are a well-integrated herd with group dynamics similar to wild elephants where it would be advantageous for an aroused state to quickly spread through a herd in response to an external stimulus that caused the arousal of some individuals.
 
The findings presented here with regard to contagious yawning among a close group of captive elephants, plus the occurrence of some contagious yawning of the elephants in response to staged human handler yawning, are consistent with the perspective of the highly-developed brain of elephants. Elephants have a larger associative neural cortex than other mammals; a neural cortex that is involved in social-empathic responses (18, 19). As discussed in the introduction, several studies associate contagious yawning with empathic behavior. In elephants, von Economo neurons (VENs) have recently been discovered in the neocortex, and are virtually identical to the VENs of humans and chimpanzees (19, 24). These neurons subserve the mental attributes of empathy and compassion in humans. Although we cannot infer the emotions or behavioral motivations of elephants, the presence of VENs in elephants suggests that elephants and humans share an important mediating substrate for social-empathic behaviors. While there is no currently proven link between contagious yawning and empathy thus far, the potential empathic aspect of contagious yawning in elephants would be consistent with the cytoarchitecture of the elephant brain.