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mystery of yawning 

 

 

 

 

mise à jour du
9 février 2017
Front. Vet. Sci.
28 February 2017
When Yawning Occurs in Elephants
 
Zoë T. Rossman, Benjamin L. Hart, Brian J. Greco, Debbie Young, Clare Padfield, Lisa Weidner, Jennifer Gates, Lynette A. Hart
 
Department of Evolution and Ecology, University of California Davis, USA
African Elephant Research Unit, Knysna Elephant Park, Western Cape, South Africa

Chat-logomini

 
Yawning is a widely recognized behavior in mammalian species. One would expect that elephants yawn, although to our knowledge, no one has reported observations of yawning in any species of elephant. After confirming a behavioral pattern matching the criteria of yawning in two Asian elephants (Elephas maximus) in a zoological setting, this study was pursued with nine captive African elephants (Loxodonta africana) at a private reserve in the Western Cape, South Africa, the Knysna Elephant Park.
 
Observations were made in June&endash;September and in December. In the daytime, handlers managed seven of the elephants for guided interactions with visitors. At night, all elephants were maintained in a large enclosure with six having limited outdoor access. With infrared illumination, the elephants were continuously recorded by video cameras. During the nights, the elephants typically had 1&endash;3 recumbent sleeping/resting bouts, each lasting 1&endash;2 h.
 
Yawning was a regular occurrence upon arousal from a recumbency, especially in the final recumbency of the night. Yawning was significantly more frequent in some elephants. Yawning was rare during the daytime and during periods of standing around in the enclosure at night. In six occurrences of likely contagious yawning, one elephant yawned upon seeing another elephant yawning upon arousal from a final recumbency; we recorded the sex and age category of the participants.
 
The generality of yawning in both African and Asian elephants in other environments was documented in video recordings from 39 zoological facilities.
 
In summary, the study provides evidence that yawning does occur in both African and Asian elephants, and in African elephants, yawning was particularly associated with arousal from nighttime recumbencies.
 
Introduction
 
Yawning is a widely recognized behavior in many mammalian and avian species and even some fish (1). In species with which we are familiar, yawning is basically self-evident; no one argues about whether a dog, cat, horse, rat, raccoon, or human is yawning when shown a photo or video clip, or seeing the behavior firsthand. But what about a species where the anatomy is considerably different from familiar mammals, and where a yawn may not be very evident even to experienced field investigators? We hypothesized that elephants may fall into this category. Prior to the initiation of our study, we were aware of no published report of yawning for any of the species of elephants in either a wild or captive/zoological setting.
 
Research on the function of yawning has increased markedly in the last decade or so, with several schools of thought about its function. Experimental evidence clearly shows that yawning does not influence blood oxygen or carbon dioxide levels (2&endash;4). While there is some debate about the role of yawning in arousal (5), investigators generally agree about the association of yawning with brain activation (2&endash;4, 6). Another proposed function of yawning, consistent with the brain activation role, is in cooling of the brain after its heating due to inactivity (7, 8).
 
If yawning does occur in elephants, one would expect a fixed-action pattern, as described in other species, with a slow opening of the mouth, followed by a brief frozen open posture, and then followed by a rapid, snap-like closure (1, 2, 6), with the size of the mouth opening varying from small to wide.
 
In this study, we first confirmed that elephants could perform an oral gaping behavior that met these descriptive criteria for yawning in pilot observations of African and Asian elephants at the San Diego Zoo and San Diego Zoo Safari Park. Once a behavioral pattern for elephant yawning was confirmed, we pursued a quantitative study of yawning in captive African elephants at a South African elephant park. Of particular concern was the occurrence of yawning as related to brain activation, particularly in the transition from sleeping or resting to wakefulness. Therefore, we focused on the likelihood of yawning in early morning hours compared with other times during the night. Because the study group was very stable, and we could observe the same individuals night after night, we looked for individual differences in the likelihood of yawning.
 
We also had an interest in whether or not a specific type of infrasonic vocalization occurred during yawning as in other circumstances, such as elephants greeting other elephants at waterholes or when leaving waterholes (9).
 
A particularly interesting aspect of yawning that has attracted considerable interest is so-called contagious yawning that is documented for humans, some non-human primates, wolves and budgerigars, and which is especially noteworthy among individuals that are familiar with each other (10&endash;17). Contagious yawning is sometimes considered a manifestation of empathy, and elephants in nature form stable social groups, and their social empathic behavior is well documented (18). Therefore, we took the opportunity to observe the elephants for possible occurrences of contagious yawning.
 
Finally, the generality of yawning in both African and Asian elephants in other environments was investigated by examining video recordings from 39 zoological facilities in the U.S.
 
Discussion
 
To our knowledge, this is the first data-based report of the occurrence of yawning in African and Asian elephants. The observations reveal that yawning in African elephants at the South African study site was a pervasive behavior that occurs in a very specific context&emdash;that is, in association with arousals from nighttime recumbent sleeping/resting bouts. Using observations from this well-established group of nine elephants in a South Africa reserve, where at night they were maintained in an open-air enclosure with infrared video recording, we were able to compile data on virtually all yawning episodes during the study periods. This unique opportunity allowed us to document which elephants yawned the least and the most, and when yawning was most likely to occur. There was no age or sex pattern with regard to which elephants yawned the least or the most. For example, of the two sub-adult males, Mashudu yawned the most, and Shungu was one of those yawning the least.
 
Of the 133 yawns associated with arousals from recumbencies, over half occurred in association with an arousal from the final recumbency of the night, just prior to the morning. There were significantly fewer yawns, per elephant, associated with arousals from 1 to 3 nightly non-final recumbencies. This finding is consistent with our prediction from the brain activation theory of yawning, proposed by others (2&endash;4, 6). The recording of infrasonic vocalizations in the enclosure at night revealed that while the elephants did vocalize from time to time, there were no evident vocalizations associated with yawning.
 
The degree to which the pattern of yawning we describe here might apply to wild free-ranging African elephants remains to be seen. Such observations would be difficult because they would be expected to occur primarily between midnight and early morning when visibility would be restricted and the observation distance would likely be much greater. No vocalizations would be expected to indicate that an elephant was yawning. That said, the generality of yawning in both African and Asian elephants in both sexes was evident in examination of video recordings from North American Zoos where 38 yawns were observed in male and female African and Asian elephants.
 
With the opportunity to observe a well-integrated herd of elephants throughout the night, via video recordings, we observed five instances of what appeared to be contagious yawning in pairs of elephants arousing together from recumbent bouts, in which the yawning was usually overlapping but differed in start times, and one instance when a standing elephant yawned after observing another arousing elephant that yawned. The contagious yawning episodes seen in pairs of elephants arousing together all occurred in the final recumbencies of the night, suggesting an association with the brain activation theory of yawning that may even be socially facilitated. We were able to establish that contagious yawning occurred in pairs of the same or different sexes and in pairs of the same and different age categories (adults and sub-adults). While our designation of some yawning episodes as contagious is consistent with descriptions of contagious yawning in other species (10&endash;17), the findings are unique with regard to individual details pertaining to the contagious yawning pairs. As with the occurrence of yawning in general, observations on yawning in an integrated group of elephants in natural settings are needed to reliably establish the occurrence and context of contagious yawning in this species.
Conclusion
 
In addition to being useful in understanding the occurrence of yawning as an essential aspect of elephant behavior, this study adds an important comparative component for current research on the brain activation function of yawning. Elephants now represent the first megafauna species with data on when yawning occurs and some variables that may influence yawning. In addition, our finding of likely occurrences of contagious yawning in elephants adds to a comparative perspective on this aspect of yawning.