mise à jour du
15 janvier 2012
Behav Processes
Evidence for contagious behaviors in budgerigars
(Melopsittacus undulatus):
An observational study of yawning and stretching
Miller ML, Gallup AC, Vogel AR, Vicario SM, Clark AB.
Integrative Neuroscience Program, Department of Psychology,
Binghamton University, NY USA


Tous les articles sur la contagion du bâillement
All articles about contagious yawning
Yawning is contagious in humans and some non-human primates. If there are social functions to contagious behaviors, such as yawning, they might occur in other highly social vertebrates. To investigate this possibility, we conducted an observational study of yawning and an associated behavior, stretching, in budgerigars (Melopsittacus undulatus), a social, flock-living parrot. Flock-housed budgerigars were videotaped for 1.5h at three time-blocks during the day (early morning, afternoon and early evening), and the times of all yawns and stretches for each bird were recorded.
Both yawning and stretching were temporally clumped within sessions, but were uniformly distributed across the trials of a particular time-block. This suggests that clumping was not a result of circadian patterning and that both behaviors could be contagious. There was additional evidence of contagion in stretching, which occurred in two forms - a posterior-dorsal extension of either one foot or both feet. Birds that could have observed a conspecific stretch, and that then stretched themselves within 20s, replicated the form of the earlier stretch significantly more often than expected by chance.
This study provides the first detailed description of temporal patterns of yawning under social conditions in a flock-living species as well as the first support for contagious yawning and stretching in a non-primate species in a natural context. Experimental evidence will be necessary to confirm the extent of contagion in either behavior
Tous les articles d'Andrew Gallup
-Miller ML, Gallup AC et al. Handling stress initially inhibits, but then potentiates yawning in budgerigars (Melopsittacus undulatus). Animal Behaviour. 2010;80(4):615-619
Although yawning has been observed across vertebrate classes (Baenninger, 1987; Craemer, 1924; Gallup et al., 2009; Luttenberger, 1975), its function is still poorly understood (Provine, 2005). It is characterized by an involuntary opening of the mouth, with a deep inspiration and shorter expiration, that is stereotyped within and across individuals, and is morphologically similar across species (Provine, 1986a). Yawning is contextually associated with transitions between activity and inactivity, and for this reason it has been suggested that yawning stimulates brain arousal (Baenninger, 1997). Although physiological evidence in support of this view is sparse (Guggisberg et al., 2010), contextual evidence is accumulating (Greco et al., 1993). For instance, yawning is associated with fatigue in humans (Zilli et al., 2008) and birds (Sauer and Sauer, 1967), movement in humans (Baenninger et al., 1996) and primates (Vick and Paukner, 2010), stress in rodents (Moyaho and Valencia, 2002) and birds (Miller et al., 2010), and boredom in humans (Provine, 1986b). Recent comparative research also supports a role of yawning in brain thermoregulation (e.g., Gallup and Gallup, 2007; Gallup, 2008; Gallup and Hack, 2011; Gallup and Eldakar, 2011; Shoup-Knox et al., 2010), and it has been suggested that the cooling component of yawning may facilitate arousal by reinstating optimal brain temperature. Thus, building evidence from numerous laboratories suggests that yawning is multifunctional (Vick and Paukner, 2010; Gallup, 2011), which may explain its ubiquity across vertebrates (Baenninger, 1987).
In contrast with spontaneous yawning, contagious yawning has been convincingly documented only in humans and a few non-human primates. Contagion is defined as the matching of reflexive or involuntary behaviors (Zentall, 2003), of which yawning provides a classic example. For instance, just observing or even reading about yawns stimulates yawning in humans (Baenninger and Greco, 1991), and attempts to shield a yawn do not stop its contagion (Provine, 2005). Under laboratory conditions, watching videotaped yawns produces contagious yawning for roughly 50% of human participants (Gallup and Gallup, 2007; Platek et al., 2003). Similar methods have been used to document contagious yawning in chimpanzees (Pan troglodytes) (Anderson et al., 2004), and recently this result has been replicated using threedimensional computer animations as a stimulus (Campbell et al., 2009). Video-induced yawning has also been reported in stumptail macaques (Macaca arctoides) (Paukner and Anderson, 2006), but since the same stimulus also induced significantly more selfdirected scratching responses, the degree to which the increased yawning represents social contagion, rather than social tension or stress, remains unclear.
A more recent study tested for a contagious yawning in red-footed tortoises (Geochelone carbonaria) by either displaying video clips of a yawning conspecific, or using a live model trained to yawn in the presence of other tortoises (Wilkinson et al., 2011). In eithercase, however, there was no evidence forcontagious yawning in this species. Further research using a live demonstrator as a stimulus has involved the testing of domesticated dogs (Canis familiaris). The first report of this topic provided evidence to suggest that dogs yawn in response to human yawns (Joly-Mascheroni et al., 2008). However, more recent research attempting to replicate this finding, using both live demonstrators as well as video clips, has failed to demonstrate this cross-species contagion effect (Harr et al., 2009; O'Hara and Reeve, 2010). In addition, one report using video clips of dog yawns also failed to provide evidence for conspecific contagious yawning (Harr et al., 2009), casting doubt on whether dogs yawn contagiously at all. Using a different approach, a recent observational study reported evidence of contagious yawning in gelada baboons (Theropithecus gelada) (Palagi et al., 2009). The authors recorded all instances of yawning from a colony of captive baboons, revealing that the frequency of this behavior increased among individuals when in the presence of both visual and acoustic yawning signals from conspecifics. Similar to other research on primates (Vick and Paukner, 2010), several distinct types of yawns were identified. Socially close baboons, especially females, were more likely to yawn contagiously, and these females matched the observed yawn-type when they yawned immediately after.
If contagious behaviors serve important functions, e.g., group coordination, in social mammals, it seems reasonable that yawning may be contagious in social, non-mammalian species as well. Furthermore, different behaviors could also be contagious and serve the same function, depending on the activity or social changes signaled. Here we present an observational study, in which we documented patterns of yawning and an associated behavior, stretching, in a flock of budgerigars (Melopsittacus undulatus) housed in an indoor aviary. Budgerigars are highly social, small parrots indigenous to Australia. They move in highly coordinated flocks throughout the year, even breeding as pairs within a larger flock (Wyndham, 1980), and signals of intention to move could certainly play a role in coordinating group activity. Stretching is a stereotyped behavior that is associated with yawning in humans and rodents (Baenninger, 1997), but there is little evidence that stretching is contagious in humans or other animals (for evidence of synchronized group displays, see Stevens, 1991). Nonetheless, stretching and yawning may predict changes in activity and/or an individual's level of stress, and therefore, the spread of either, or perhaps both behaviors, may coordinate group activity. Similar to yawning, stretching is believed to be a reflexive, automatic action in these birds, so unlike the copying of voluntary, learnt behaviors, known as imitation or response facilitation (e.g., Hoppitt et al., 2007), in this study the temporal coupling of either behavior refers to contagion.
Our previous research has recently explored the contagious nature of these behaviors in budgerigars through video stimuli, finding mixed support for a social influence in yawning (unpublished data). In particular, the latency to yawn was significantly reduced following clips of conspecific yawns compared with control clips, but the frequency of yawning and stretching did not increase following clips of the respective behavior (unpublished data). There were, however, limitations in the quality of the stimulus (recorded from freely behaving birds) and the degree to which the experimental birds were attending to the video screen. Therefore, in this study we tried to lay a stronger foundation for future experimental work by taking a naturalistic approach similar to the study performed on gelada baboons (Palagi et al., 2009). To explore how individual birds responded to the actions of nearby group members, we video recorded an undisturbed, established flock of captive budgerigars, and measured the time and occurrence of each yawn and stretch. For yawning and stretching separately, we analyzed the distribution of successive behaviors.
We also looked for any diel patterns, and associations between stretching and yawning at three different times of the day (early morning, afternoon and early evening). It was hypothesized that, if contagious, each behavior would be non-randomly clumped into closely spaced bouts within recording sessions, as birds were stimulated by their neighbors' behavior, and separated by longer periods without these behaviors. Even if clumped within a particular testing session, we further predicted that these behaviors would be evenly spaced across multiple sessions, when comparing sessions that were recorded at the same time of day. This would suggest that it is not a specific time of day that causes the clumping pattern. Lastly, a strong circadian or other temporal pattern, previously established for humans and rats (Baenninger, 1997; Anias et al., 1984; Zilli et al., 2007), would potentially illuminate the context and function of these behaviors, whether contagious or not. In summary, although these behaviors may have a general circadian pattern over distinct periods of the day (i.e., they may occur more frequently in the morning or evening), we predict that within a particular session, behaviors will be clumped due to social factors.
boy bird yawwn
Occurrences of both yawning and stretching were temporally clumped in an unmanipulated, captive flock of budgerigars, as would be expected if these behaviors are contagious. Despite the low frequency of yawning (1.28-2.96 yawns per bird per hour, depending on time of day), a bird was more likely to yawn within 40s or less of another bird's yawn. There were also a substantial number of yawns separated by at least 300s from the previous yawn, but few spaced at intermediate intervals. Taken together, the inter-yawn spacing distribution (Fig. 2a) suggests that yawns were socially influenced (Le., contagious). In other words, long periods of no yawns were broken by a budgerigar's yawn that was then followed by a cascade of yawns among the others. A similar, although less strongly bimodal temporal distribution of stretching was observed. In part, fewer stretches were separated by very long intervals because there were a substantially greater number of stretches than yawns per session (566 yawns versus 1752 stretches) and stretching continued for longer bouts among flock members. Stronger evidence to support the social influence of this behavior comes from stretch-type matching, illustrating that birds were more likely to replicate the specific stretch-type of a previous bird than would be expected by chance. This result is similar to the observational research on gelada baboons (Palagi et al., 2009), showing yawn-type matching. Although no functional distinctions between mono- and bi-lateral stretches were identified, this temporal pairing of identical behaviors suggests that stretches of conspecifics were closely observed and that the form influenced the subsequently stretching bird. It has been suggested that different yawn-types may produce distinct physiological outcomes among chimpanzees (Vick and Paukner, 2010), and thus the matching of different behavioral-types may help coordinate group activity.
An alternative interpretation of the temporal patterns we observed is that flocking birds tend to simultaneously reach the same physiological state (i.e., well-rested, hungry, alerted by outside event, etc.) (Sauer and Sauer, 1967), and this tendency produced more, or less, yawning or stretching among group members. Differences in frequencies across the day would be a reflection of these shared changes, since there are clear diel patterns of yawning in humans and rodents (Anias et al., 1984; Baenninger et al., 1996). If yawning patterns are related to daily rhythms of body temperature, metabolism, and resultant arousal, it is possible that flock members both share a physiological rhythm and respond with some low degree of contagion to another's behavior, thus strengthening the diel pattern and producing higher degrees of clumping. Although plausible, this interpretation seems insufficient. Analyses show that yawning was significantly clustered within sessions, as would be expected by contagion, but when looking across sessions recorded at the same time of day, we notice that both yawns and stretches occurred evenly throughout the videos, and were not repeatedly clustered at a particular time of day. This suggests that a related circadian physiological rhythm experienced by the birds does not explain our results.
The combined temporal patterning and significant "matching" of adjacent stretches suggest that this behavior is contagious and thus a potential social signal in this species. Although the function of stretching is largely unstudied, it is another stereotyped, unlearned behavior that is ubiquitous among tetrapods. Both yawning and stretching are homeostatic behaviors believed to serve a purpose in the maintenance of bodily functions through enhanced circulation (Sauer and Sauer, 1967). Stretching in humans is confined to specific, yet intense state-change, occurring most frequently after waking, but not prior to sleep (Provine et al., 1987). Research on both humans and animals show that yawning also typically occurs during broader state-changes (Provine et al., 1987), and is followed by modified activity or increased locomotion (Baenninger et al., 1996; Giganti et al., 2002; Vick and Paukner, 2010). Taken together with the current results, we suggest that these behaviors may coordinate collective flock behavior, in addition to serving as important preparatory responses to flight. As evidence for this, flight and other movement among perches is often preceded by stretching or yawning in budgerigars (unpublished data). Responding to another's intention-movements has clear adaptive value for any group-moving species. Based on these observations, the study of yawning, stretching and transitions in activity may provide a novel approach to studying collective behavior. When perched, budgerigars sit in close proximity to one another and remain oriented towards adjacent group members, providing a setting where behaviors can spread across a line of birds, coordinating flock movement. Recently we have shown that auditory disturbances enhance both stretching and yawning contagion among budgerigars in small groups (Miller et al., in press), suggesting that the close coupling of these behaviors may be involved in collective response to environmental stimuli. Future research could investigate the role of yawning and stretching contagion in group vigilance, and more specifically how spatial position within a group reflects another bird's information processing, and how birds use local behaviors of nearby conspecifics to infer collective-state (Couzin, 2009).
4. Conclusions
Signals may frequently originate from physiologically relevant behaviors adapted for social purposes. Spontaneous yawning is associated with stress, arousal and thermoregulation in a variety of species, including budgerigars. While the physiological function of stretching is less clear, vertebrates frequently stretch before beginning to move. Stretching also co-occurs with yawning in a variety of species and may therefore be associated with arousal. The observational results presented here suggest that yawning and stretching are at least mildly contagious in budgerigars under semi-natural flock-living conditions. In line with each behavior's presumed physiological function, contagious yawning and stretching may ultimately coordinate mental state and a group's collective movements, but future research needs to test these predictions. While experimental studies are needed to confirm and clarify the degree and precision of contagion, we propose that experiments be designed using live birds as the target stimulus. Nonetheless, the current results provide a strong basis for understanding the functional context of, and inferring an adaptive role for, contagion in coordinated flock-living species.