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

mystery of yawning 

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15 septembre 2019
(2019) 9:13271
 Observational data reveal evidence and parameters of contagious yawning in the behavioral repertoire of captive-reared chimpanzees (Pan troglodytes) 
Matthew W. Campbell, Cathleen R. Cox
California State University, Channel Islands, California, USA and Los Angeles Zoo and Botanical Gardens, California, USA.  


 Tous les articles sur la contagion du bâillement
All articles about contagious yawning
There is robust experimental evidence for contagious yawning, yet observational studies of naturalistic behavior have been fewer. Without data from real-world behavior, researchers have questioned the existence of contagious yawning and made assumptions about some parameters (e.g., the duration of the effect). The authors observed contagious yawning in chimpanzees to confirm/disconfirm its existence in the behavioral repertoire of this species, and if present, provide some of the missing descriptives. They recorded yawns on an all-occurrence basis from 18 captive-reared chimpanzees at the Los Angeles Zoo. They recorded identity, time, and individuals who could have been affected. They calculated a threshold for contagion by taking the mean and adding 1.96 standard deviations, constructing a response curve. Across multiple measures they see a consistent pattern in which there is a strong effect of contagion for 1.5 minutes, a less strong but still significant effect lasting up to 3.5 minutes in some measures, and no evidence of contagion beyond 3.5 minutes. From the time stamp on each yawn they were able to rule out temporal synchrony as an alternative hypothesis. Thus, contagious yawning appears to be a natural phenomenon in chimpanzees lending support to the myriad experimental and observational studies to date.
Il existe de solides preuves expérimentales que les bâillements peuvent être contagieux, mais des études observationnelles de ce comportement sont peu nombreuses. Sans données sur les comportements du monde réel, certains chercheurs ont mis en doute l'existence de bâillements contagieux et ont formulé des hypothèses sur certains paramètres (par exemple, la durée de l'effet). Les auteurs ont observé des bâillements contagieux chez les chimpanzés pour confirmer / infirmer son existence dans le répertoire comportemental de cette espèce et, s'il existe, fournir certaines des descriptions manquantes. Ils ont enregistré tous les bâillements de 18 chimpanzés élevés en captivité au zoo de Los Angeles.
Ils ont enregistré l'identité, l'heure et les congénères qui auraient pu être touchés. Ils ont calculé un seuil pour la contagion en prenant la moyenne et en ajoutant 1,96 écart-type, en construisant une courbe de réponse.
À travers plusieurs mesures, ils observent, de façon constante, une réponse à un bâillement dans la minute et demi après l'émetteur, un effet moins puissant mais toujours significatif pouvant durer jusqu'à 3,5 minutes dans certaines mesures, et aucune preuve de contagion au-delà de 3,5 minutes.
La mesure de ce délai, leur a permis d'exclure la synchronisation temporelle comme hypothèse alternative. Ainsi, le bâillement contagieux apparaît comme un phénomène naturel en accord avec les études expérimentales et observationnelles antérieures.
Contagious yawning is when a yawn by one individual induces a yawn in another individual. An assumption of this definition is that the second individual (termed here: the observer) would not have yawned except for the stimulation, visual or auditory, by the first individual (termed here: the trigger). Evidence for the existence of contagious yawning has typically come from experimental approaches: in the most robust designs subjects are exposed to yawns and some other stimulus for control, and rates of yawning in each condition are compared.
This approach has yielded consistent, replicated evidence for contagious yawning in humans (Homo sapiens) and chimpanzees (Pan troglodytes). There is conflicting experimental evidence of contagious yawning in bonobos (Pan paniscus), with one study finding an effect while another did not, but the larger sample size of Tan et al. may explain why they found a significant population-level effect while Amici et al. did not. It is notewor- thy that Amici et al. did find a significant effect in chimpanzees, which they had many more of than bonobos. Budgerigars (Melopsittacus undulates) have shown experimental and observational (discussed below) evidence of contagion. Stumptail macaques (Macaca arctoides) showed statistically significant contagion in response to video, but it is not clear if the yawning resulted from increased arousal as opposed to copying the expression or affective state of the yawner. Some studies on dogs (Canis lupus familiaris) have found evidence of contagious yawning while others have not, which may stem from the different methods used. Lastly, two species of lemur (Lemur catta and Varecia variegata), lowland gorillas (Gorilla gorilla), orangutans (Pongo abelii), and red-footed tortoises (Geochelone carbonaria) did not show evidence of contagion in experimental settings, although the sample size issues mentioned for the bonobo studies also pertain to the orangutans and tortoises.
One issue is that experimental paradigms present subjects with a supernormal stimulus: they encounter more yawns in a shorter amount of time than they would in real life. Anderson raised the issue of whether contagious yawning is an artifact of experimental designs and is not present in the normal social behavior of the species tested. Taking chimpanzees as an example, despite decades of observational studies in both the field and captivity, no one has reported contagious yawning in their data. Most likely this is because no one has looked for it. As Vick & Paukner pointed out, previous ethograms of chimpanzee facial expressions did not include yawning. Thus, the lack of contagious yawning in natural behavior that concerned Anderson could stem from the issue of supernormal stimuli that he raised, but it could just as well stem from researchers not measuring the behavior in the first place, as there are no published data, positive or negative. Whatever the cause, the criticism by Anderson has thus far not been directly and adequately addressed.
There is some evidence that contagious yawning exists in the normal behavioral repertoires of at least some species. Observational methods have allowed researchers to record yawns of individuals without resorting to playback. These studies found that gelada baboons (Theropithecus gelada), humans, bonobos, and wolves (Canis lupus) were more likely to catch yawns from individuals they had stronger bonds with. The primary goal of these studies was to examine the social relationships of contagion as a means of studying empathy. Three of the four studies also performed some kind of yawn vs. control statistical comparison, which is essential to establishing the existence of contagion. Gelada baboons were more likely to yawn within 5 minutes of perceiving a yawn than other expressions, bonobos who could perceive a yawn were more likely to yawn within 3 minutes than bonobos who could not perceive the yawn, and wolves yawned more within 3 minutes of perceiving a yawn than during a 3-minute matched control. One limitation is that the time window of 3 minutes or 5 minutes is an arbitrary one. There is no empirical evidence that we can find that demonstrates that these are the exact windows of contagion in these, or any, species. Thus, the windows used seem to be judgement calls rather than determined by data.
Using observational methods but a different analysis, budgerigars showed a nonrandom distribution of yawns such that short inter-yawn latencies were more common than would be expected by chance. The benefit of this method is that it lets the data determine the rate of yawning at different time spans post yawn. The authors found a strong effect of yawning within 40 seconds of another yawn, after which the response tapered off. However, it is unclear exactly what the statistical baseline rate of yawning was and when the yawning became statistically indistinguishable from it. Together, these 5 studies using observational methods provide varying support that contagious yawning is not merely an artifact of experimental designs.
The two approaches have resulted in an empirical jump from experimental evidence of the existence of con- tagious yawning to observational applications of contagious yawning as a means of studying empathy. What is missing is a rigorous assessment of the observational evidence of contagious yawning and contagious yawning alone, comparing the rate of contagious yawning to a baseline, and ruling out alternative explanations, like yawns being synchronized over the time of day by similar circadian patterns of activity. An exception is the observational study of budgerigars, which identified a window of contagion (40 s) and ruled out circadian synchrony from their data. The difference in window of contagion between budgerigars (40 s) and those used for mammals (3 or 5 min) is quite large, and it could result from the different methodologies or species differences. Whatever the reason, the budgerigar window of 40 s does not appear to relate well to the mammals that have been studied. Perhaps it is the lack of comparative data that has led some to question the existence of contagious yawning as a natural phenomenon in some species or at all.
Establishing whether contagious yawning exists in behavioral repertoires is important because before we can apply contagious yawning as a method to examine social relationships, we need to know whether it is present in real-world data. If contagious yawning is not present in the daily lives in these species, whether captive or wild, then the applications of contagious yawning as a measure of empathy rests on faulty assumptions. The social relationships in the pattern of contagious yawning may reflect other, unidentified variables, not empathy-based contagion.
In this study we sought to identify whether there is statistical evidence of contagious yawning in observational data of a well-established group of captive-living chimpanzees. Our hypothesis was that if yawns are contagious, then there should be a significantly greater chance of a yawn occurring after observing a yawn than the baseline rate of yawning. Rather than selecting an arbitrary time window for contagion, we analyzed all latencies between a yawn and when the individual last saw a yawn and let the data build a response curve. Rates of yawning significantly above the baseline rate of yawning would be evidence of contagion.
In addition to the presence or absence of contagious yawning, our data allow us to describe the parameters of contagion, if it exists. One aspect of contagious yawning that appears different from contagion of other expressions is the extended latency between observing and performing a yawn. With copying other facial expressions (e.g., smiles, frowns, expressions of fear), the window of contagion is 0.5&endash;1.0 seconds 41. Yawning appears different, however, with an observer yawning some seconds, possibly even minutes, later. This difference between copying yawns and copying other expressions has been enough for some to question the existence of contagious yawning. The window of contagion for yawns is not known for any species other than the budgerigars. Within the mammals, we do not know how quickly one yawn can affect another or for how long as the observational studies used durations that had not been empirically established. Our data allow us to measure how soon yawns may affect observer chimpanzees within our temporal resolution. Our data also show how long yawns may be contagious for, but this is only in relation to the population-level rate. Our method is not sensitive to and therefore cannot supply the maximum duration possible for an individual to yawn in response to another.
We also measured some other variables that could affect the rate of contagion, including the number of yawns seen by the observer, the physical proximity to the yawning individual, and the sex of both the observer and the trigger. Since each yawn was time stamped, we examined yawning by time within our 09:30&endash;12:30 observation window. This allowed us to evaluate temporal synchrony (due to internal circadian rhythms or external cues) within our observation times as an alternative hypothesis to contagion if yawns appear to be clustered. In addition, we used the timestamps to examine whether rates of contagion change with time (other studies will need to fill in times for the rest of the day). The group of chimpanzees we studied included 5 infants.
Experimental studies have shown an absence of contagious yawning in chimpanzees aged 1&endash;4 years old with emergence beginning at 5 years old. The limitation is that these were experimental studies, and the artificial setting could potentially result in evidence of contagious yawning at an earlier or later age than what occurs naturally. Observational data can reveal when individuals begin to show contagious yawning in their normal social interactions, which could have implications for their social-emotional development. With these data we hope to find out whether statistical evidence of contagious yawning can be identified from observational data, and if so, what its parameters are like.
The results show evidence that yawns are contagious in the normal daily life of one captive group of chimpanzees. Our observations allow us to dispel a couple of concerns about contagious yawning. First of all, Anderson was rightly concerned that experimental studies presented supernormal stimuli to subjects. He raised the question of whether contagion was an artifact of experimental designs, or if it functioned in the normal lives of the animals studied, whether captive or wild. Our results show that contagious yawning does exist in the normal lives of this captive group of chimpanzees, that the effect is strong (6 standard deviations above baseline during the first minute after viewing a yawn), and that experiments on contagious yawning have probed a natural phenomenon, not an artifact.
Further support that yawns are contagious comes from the chains of transmission analysis. There would be no reason to predict that contagion should stop at only two individuals (one trigger and one observer), and it should be possible for yawns to continue to be transmitted to additional individuals. With our conservative criteria we observed 4 instances of triadic contagion in which yawning proceed from a trigger to observer 1 to observer 2. With a slightly more relaxed definition of contagion, the longest chain moved from a trigger to 4 successive observers. We believe that documenting chains of transmission also supports the existence of contagious yawning as a natural phenomenon.
A second concern is that previous observational studies of contagious yawning did not test for the existence of contagion statistically, as we have done. Three studies chose a window of contagion and found more yawning during that window than baseline, whereas another did not run an analysis of this sort 33. The limitation here is that the window of 3 minutes or 5 minutes was informed by experimental studies, rather than being determined by their own data or other observational studies. Thus, there is some arbitrariness in the choice of times. Only Miller et al. used their data to examine a window of contagion. The problems here are that it is not clear when yawning statistically deviates or returns to baseline from their analysis, the use of one-tailed statistics, and the window identified of only about 40 seconds for budgerigars does not appear to be applicable to the mammals studied.
Because of the issues with observational data, and a lack of it, Anderson accepted the existence of contagious yawning under experimental conditions and questioned its existence in natural behavior (at least for nonhu- mans). However, Kapitány & Nielsen went so far as to question whether contagious yawning exists at all, for any species, including humans. With our results we can dispel the concern of Kapitány & Nielsen as well. We provide strong statistical support for the existence of contagious yawning in chimpanzees through observational data, which augments the multiple experiments also finding strong statistical support for contagious yawning in this species. In addition, our results serve as support for the observational studies that did not test for contagion directly, as we have. The window we identified is similar to ones that have been used previously, and having identified contagious yawning in the behavioral repertoire of two species (chimpanzees in the current study and budgerigars), we expect that similar response curves would be found in the data of others, though the exact numbers may vary by species.
It would also be a mistake to question the findings of the studies that used 5 minutes or 3 minutes as a window of contagious yawning when our evidence extends to 3.5 minutes. For one thing, our results describe only this group (housed at the Los Angeles Zoo and Botanical Gardens) of this species (Pan troglodytes). Our exact numbers may not be indicative of the species as a whole. The group we studied is large by captive standards (N = 18) and diverse (8 adult females, 5 adult males, 5 infants), especially for zoos, but 18 is not enough to establish a species-wide rate of response. In small samples, one or two high functioning or low functioning individuals can skew the precise numbers. The overall pattern should be consistent (yawns are contagious for some time after viewing a yawn), but the exact time window measured might vary between groups. Future testing will be needed to show how representative our parameters of contagion are for chimpanzees as a whole, as well as if they vary at other times of the day.
In addition, there is no reason to expect the parameters we measured to be the same for all species. Different species could have longer or shorter windows of contagion based on their evolution. The other observational studies were on geladas, humans, bonobos, and wolves, and each species may have its own parameters of contagion. We would have to measure them to find out. Lastly, and perhaps most importantly from a statistical perspective, these studies were looking at social patterns of contagion. The expectation was that contagious yawning, if based on empathy mechanisms, should be biased toward closer social affiliates than distant ones.
Thus, contagious yawning should show a social pattern, but noncontagious yawning should not. Noncontagious yawning should be randomly distributed in the group. Using a window of contagion that is too long would be adding noncontagious yawns (i.e., noise) to the experimental condition, and using one that is too short would be adding some contagious yawns (i.e., signal) to the control condition. If the experimenters still find a significant difference, that implies that the signal is so strong that it can be identified statistically even with extra noise or reduced signal in the input. The implication is that if 5 minutes is too long or 3 minutes is too short and a signal is found, the signal should be even stronger for the optimum window. The problem in including too long a window of contagion is the possibility that the noise (noncontagious yawns) masks the signal (contagious yawns) leading to a null result. With too short of a window there would be a large amount of signal (contagious yawns) in both the contagion condition and the baseline, leading to no significant difference between them. Thus, the problem of using too long or too short of a window of contagion is the risk of a type 2 error (false negative), not a type 1 error (false positive). In our view, our results support the previous observational studies by showing that contagious yawning is present in observational data and do not undermine them by identifying a slightly different and more precise window of contagion.
Unlike previous studies, our results allow us to describe the natural parameters of contagious yawning. We applied numerous different approaches to operationally defining contagious yawning, and the results are remark- ably consistent. Using a conservative subset of our data, we found that yawning was contagious for 3.5 minutes after observing a yawn. Applying different criteria changed the outcome only subtly, and a larger scale pat- tern emerged with a very strong effect of contagion up until 1.5 min, a less strong but still above threshold effect of contagion after 1.5 min and lasting as long as 3.5 min, and then yawning falling below threshold and staying there. Different measures disagree exactly where the contagion effect falls below threshold (e.g., 1.5 min, 3 min, or 3.5 min), but none extend the window of contagion beyond 3.5 min after viewing a yawn. Since our primary measure of contagion, which we established with a conservative subset of the total yawns, yielded a window of contagion up until 3.5 min, and since this number was supported by other measures, we feel confident in accepting 3.5 min as a duration for which yawns are measurably contagious in this group of chimpanzees. Nonetheless, other researchers may disagree and prefer a more stringent window. The window from using only yawns from 10:00&endash;12:00 to avoid feeding times is tighter, with strong evidence only for the 1.5 minutes post yawn exposure. We have provided our data across multiple criteria for contagious yawning so that readers can come to their own conclusions, based on the evidence we gathered, as to what constitutes the most appropriate window of measuring yawn contagion.
One note, it would be the wrong interpretation to conclude that all yawns within 3.5 minutes of viewing a yawn are contagious, and that no yawns after 3.5 minutes are contagious. We cannot know for certain, currently, whether any given yawn is contagious or non-contagious. There are no behavioral cues that have been identified to distinguish them, and the only way to determine this conclusively would be through differing neural signatures between yawns originating internally (noncontagious) or through visual or auditory stimulation (contagious). These neural signatures have not yet been identified, and, of course, they would not be helpful outside of laboratory studies. Instead, the window shows the duration of time for which reliable assumptions of pooled data can be made. As done already, the window of the time is the one in which to look for social biases in contagion. The window says that a high number of these yawns will be contagious (signal), and that after 3.5 minutes many/ most of the yawns will be noncontagious (noise). Nothing says that yawns within 3.5 minutes of view another must be contagious. Only that if we are going to look for social patterns, this window provides us with the greatest signal-to-noise contrast with which to do so. In addition, our data do not say that it is impossible for yawns to be contagious beyond 3.5 minutes in chimpanzees. That is also the wrong interpretation. Currently, there is no known difference in the motor pattern between contagious and noncontagious yawns, and one may not exist. Without an observable difference, only a neural method could conceivably label each yawn as contagious or non-contagious, so only that method could establish the absolute maximum duration for which yawns are contagious in any individual or species.
An alternative hypothesis to yawns being contagious is that they are temporally synchronized, perhaps due to circadian rhythms or regular, daily events. Yawning varies over the time of day. Theoretically, a tight enough peak could produce a pattern that looks statistically like contagion but arises from yawns being temporally synchronized, rather than contagious. However, yawning was not tightly grouped enough in our observations to account for the greater chance of observing a yawn after another yawn. The window we measured was only 3.5 minutes long, at its longest. That would require the temporal pattern of yawning to have a similar peak lasting no more than a few minutes. Yawning does appear to occur at higher rates at the very beginning and end of our observations, which differs from Vick & Paukner. The increased rates we observed correspond with feedings (just after morning feed and just before lunch), so it is possible that they are displacement behaviors related to tension or anticipation of meal times. Increased yawning around feeding times was also observed in lions (Panthera leo) and mandrills (Mandrillus). However, the times close to the chimpanzees' feedings (9:30&endash;10:00 and 12:00&endash;12:30) do not correspond exclusively with the time stamps of the contagious yawns we observed. Yawns meeting our criteria for contagion appear throughout the observation times, even with a rise toward the end. Furthermore, if we remove these two half-hour ranges and only analyze yawns occurring between 10:00&endash;12:00, we find similar evidence of contagion with a strong effect for 1.5 minutes after viewing a yawn, responses bordering threshold until 3.5 minutes, and then dropping well below threshold thereafter. Thus, patterns of temporal synchrony cannot explain our data.
The only social data we have in this analysis are the sex and early developmental age of the yawner. Males yawned significantly more than females, which was not recorded in chimpanzees previously. These differences may reflect how a few individuals can influence population-level statistics in the group sizes available in captivity. Larger sample sizes, perhaps from wild groups or sanctuaries, may clarify sex differences in yawning in chimpanzees. Using the higher baseline rate of yawning by males as the expected values, males did not deviate from this rate in their propensity for contagion. In an observational study, female humans showed higher susceptibility to yawn contagion, and the authors linked this difference to females being more empathetic than males in general. We did not make this same observation in chimpanzees as both sexes showed rates of contagion similar to their baseline rate of yawning. Looking at the triggering individual, male chimpanzees and female bonobos were more likely to serve as triggers than the opposite sex. However, we did not observe this result, either, as neither sex was more likely to serve as a trigger than expected based on the baseline rate of yawning. Thus, our data do not support either of the previously identified sex differences in contagious yawning. Two of the studies were on different species, so it is possible a female bias in contagion 49 and triggering 34 exists in those species, but not in chimpanzees. As for Massen et al., that study was experimental, and ours was observational. One possibility is that the supernormal exposure of video playback 30 draws out a difference that does not exist in natural behavior. Conversely, the difference may have been too subtle for us to measure with our sample size. The latter seems unlikely because we did not even observe a trend in the direction of males being triggers more often than females. Our observed values match our expected values very closely. Another possibility is that there are differences between the groups of chimpanzees; each study may accurately describe an effect for the group observed, which is not unreasonable when thinking about the diversity of chimpanzee behavior and the relatively small sample sizes of captive groups. Lastly, our study could have a false negative, or Massen et al. could have a false positive. Only replication will solve the discrepancy in these observed effects.
Regarding development, we have too few cases to analyze them statistically, so we need to be cautious with our discussion. We can say that we did record potential contagious yawns from individuals slightly younger than has been seen in experimental studies. Anderson et al. used video playback with infants (3 years old) accompanying their parents, and the infants did not yawn at all. The authors did not provide data on attention, so we do not know to what extent the infants perceived the yawns. It is possible the infants were distracted by the presence of their mother, or perhaps the artificiality of video playback does not stimulate contagious yawning at this young age. Madsen et al. used live yawn demonstrations from humans (familiar and unfamiliar) and did not see evidence of contagious yawning under the age of 5 years old. As with Anderson et al., perhaps the artificiality of experimentation fails to elicit behaviors that are developmentally in transition. It is also possible that empathy-based contagion expresses itself sooner for members of the social group, which we can assume would be socially closer to the chimpanzees than members of another species. One last possibility that occurs to us, Madsen et al. studied orphaned chimpanzees, and differences in emotional development have been found between mother-reared and orphaned bonobos. It is interesting that of the potential contagious yawns by infants that we recorded, none of the triggers were the infant's mother. Because our numbers are so small, we cannot conclude that contagious yawning is in fact present at younger ages than has been recorded previously, but our data do suggest that observational methods may reveal different developmental patterns than experimentation.
In conclusion, we found strong evidence that contagious yawning is a natural phenomenon in a captive group of chimpanzees. We can dispel with the concerns about the very existence of contagious yawning and accept previous experimental and observational studies as measuring aspects of behaviors that exist in the normal rep- ertoires of the species studied. Our methods can be applied widely, and we hope researchers will build response curves for different species. It would be very interesting to know whether the parameters of contagion differ between groups of the same species and across species. Combining the comparative method and observational studies of contagious yawning could tell us about the evolution of contagious expressions, empathy as a possible mechanism, and the socioecological factors that may have shaped this behavior.