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mise à jour du
31 mai 2015
Anim Cogn
2015;18(5):1051-158
Experimental evidence of contagious yawning in budgerigars (Melopsittacus undulatus).
 
Gallup AC, Swartwood L, Militello J, Sackett S.
 
Psychology Department, State University of New York at Oneonta, USA

Chat-logomini

Abstract
 
Experimental evidence of contagious yawning has only been documented in four mammalian species. Here, we report the results from two separate experimental studies designed to investigate the presence of contagious yawning in a social parrot, the budgerigar (Melopsittacus undulatus). In Study 1, birds were paired in adjacent cages with and without visual barriers, and the temporal association of yawning was assessed between visual conditions. In Study 2, the same birds were exposed to video stimuli of both conspecific yawns and control behavior, and yawning frequency was compared between conditions. Results from both studies demonstrate that yawning is contagious. To date, this is the first experimental evidence of contagious yawning in a non-mammalian species. We propose that future research could use budgerigars to explore questions related to basic forms of empathic processing.

Andrew C. Gallup. Yawning and the thermoregulatory hypothesis
 
A comment on Newscientist

budgerigar
Introduction
Yawning is characterized by a powerful gaping of the jaw with inspiration, a brief period of peak muscle contraction, and a passive closure of the jaw with shorter expiration (Barbizet 1958). Nonsocial yawning, also known as spontaneous yawning, is believed to be relatively widespread among vertebrates (Baenninger 1987) and may function in promoting cortical arousal (Baenninger 1997) and/or state change (Provine 1986, 1996, 2005) by decreasing brain temperature (Eldakar et al. in press; Gallup and Gallup 2007, 2008; Gallup and Eldakar 2012; Massen et al. 2014; Shoup-Knox et al. 2010). Contagious yawning, which can be elicited by sensing or thinking about the action in others (Provine 2005), appears to be a more recently derived behavior that may function in group coordination and vigilance in social species (Gallup and Gallup 2007; Gallup 2011; Miller et al. 2012a). Introduction
 
Yawning is characterized by a powerful gaping of the jaw with inspiration, a brief period of peak muscle contraction, and a passive closure of the jaw with shorter expiration (Barbizet 1958). Nonsocial yawning, also known as spontaneous yawning, is believed to be relatively widespread among vertebrates (Baenninger 1987) and may function in promoting cortical arousal (Baenninger 1997) and/or state change (Provine 1986, 1996, 2005) by decreasing brain temperature (Eldakar et al. in press; Gallup and Gallup 2007, 2008; Gallup and Eldakar 2012; Massen et al. 2014; Shoup-Knox et al. 2010). Contagious yawning, which can be elicited by sensing or thinking about the action in others (Provine 2005), appears to be a more recently derived behavior that may function in group coordination and vigilance in social species (Gallup and Gallup 2007; Gallup 2011; Miller et al. 2012a).
 
To date, experimental evidence of contagious yawning is restricted to humans (Homo sapiens; e. g., Provine 1986; Platek et al. 2003), chimpanzees (Pan troglodytes) in response to conspecifics (Amici et al. 2014; Anderson et al. 2004; Campbell et al. 2009; Campbell and de Waal 2011; Massen et al. 2012) and human yawns (Campbell and de Waal 2014; Madsen et al. 2013; but see Amici et al. 2014), domesticated dogs (Canis familiaris) in response to human yawns (Joly-Mascheroni et al. 2008; Madsen and Persson 2013; Romero et al. 2013; Silva et al. 2012; but see Harr et al. 2009; O'Hara and Reeve 2011; Buttner and Strasser 2014), and, most recently, a subline of high-frequency yawning Sprague&endash;Dawley rats (Rattus norvegicus; Moyaho et al. 2014). Video-induced yawning has also been reported in stumptail macaques (Macaca arctoides; Paukner and Anderson 2006), but this response also cooccurred with heightened self-directed behaviors and thus appears to be due to social tension or stress rather than contagion. Species that have thus far failed to show contagious yawning in an experimental design include bonobos (Pan paniscus), orangutans (Pongo abelii), and gorillas (Gorilla gorilla) in response to both conspecific and human yawns (Amici et al. 2014), and domesticated dogs and redfooted tortoises (Geochelone carbonaria) in response to conspecifics (Harr et al. 2009; Wilkinson et al. 2011).
 
To date, experimental evidence of contagious yawning is restricted to humans (Homo sapiens; e. g., Provine 1986; Platek et al. 2003), chimpanzees (Pan troglodytes) in response to conspecifics (Amici et al. 2014; Anderson et al. 2004; Campbell et al. 2009; Campbell and de Waal 2011; Massen et al. 2012) and human yawns (Campbell and de Waal 2014; Madsen et al. 2013; but see Amici et al. 2014), domesticated dogs (Canis familiaris) in response to human yawns (Joly-Mascheroni et al. 2008; Madsen and Persson 2013; Romero et al. 2013; Silva et al. 2012; but see Harr et al. 2009; O'Hara and Reeve 2011; Buttner and Strasser 2014), and, most recently, a subline of high-frequency yawning Sprague&endash;Dawley rats (Rattus norvegicus; Moyaho et al. 2014). Video-induced yawning has also been reported in stumptail macaques (Macaca arctoides; Paukner and Anderson 2006), but this response also cooccurred with heightened self-directed behaviors and thus appears to be due to social tension or stress rather than contagion. Species that have thus far failed to show contagious yawning in an experimental design include bonobos (Pan paniscus), orangutans (Pongo abelii), and gorillas (Gorilla gorilla) in response to both conspecific and human yawns (Amici et al. 2014), and domesticated dogs and redfooted tortoises (Geochelone carbonaria) in response to conspecifics (Harr et al. 2009; Wilkinson et al. 2011).
 
Observational evidence for contagious yawning to conspecifics has been reported in bonobos (Demuru and Palagi 2012; Palagi et al. 2014), gelada baboons (Theropithecus gelada; Palagi et al. 2009), budgerigars (Melopsittacus undulatus; Miller et al. 2012b), and wolves (Canis lupus lupus; Romero et al. 2014).
 
Research suggests that contagious yawning is triggered by mechanisms that differ from those involved in other involuntary actions (Amici et al. 2014). In particular, contagious yawning is thought to represent a basic form of empathy rooted in a perception&endash;action mechanism known as state matching or emotional contagion (Preston and de Waal 2002). Consistent with this view, previous research has documented a strong association between contagious yawning and empathy (for a discussion, see Campbell and de Waal 2014). For example, in humans, contagious yawning is more common among participants who score high on empathy measures (Platek et al. 2003; but see Bartholomew and Cirulli 2014), and thinking about yawning has been shown to activate brain areas implicated in empathic processing (e.g., Platek et al. 2005; Nahab et al. 2009). Comparative studies investigating the developmental onset and decline of contagious yawning also generally support this view (Anderson and Meno 2003; Bartholomew and Cirulli 2014; Giganti et al. 2012; Madsen et al. 2013; Madsen and Persson 2013; Massen et al. 2014), since empathy-related capacities in humans emerge in early childhood and decline in old age (Bailey and Henry 2008; Perner and Lang 1999). Growing comparative research also demonstrates a positive relationship between contagious yawning and group affiliation or social closeness/bonding (Campbell and de Waal 2011; Demuru and Palagi 2012; Norscia and Palagi 2011; Palagi et al. 2009; Romero et al. 2013, 2014; Silva et al. 2012), which supports a connection with empathic processing. For example, an initial study on chimpanzees provided evidence for an ingroup bias for contagious yawning (Campbell and de Waal 2011). In particular, captive chimpanzees shown video stimuli of other chimpanzees yawning demonstrate contagion to ingroup members but not to unfamiliar conspecifics. Subsequent studies, however, have failed to demonstrate a familiarity bias for chimpanzees viewing human yawns (Campbell and de Waal 2014; Madsen et al. 2013), and at least one study provided evidence that relationship quality among chimpanzees did not predict yawn contagion (Massen et al. 2012). There has also been mixed support for domesticated dogs to yawn more in response to yawns from familiar humans (Madsen and Persson 2013; O'Hara and Reeve 2011).
 
Since contagious yawning may represent a primitive form of empathy, unequivocally demonstrating the presence of this behavior in a laboratory animal, with the ability to manipulate it experimentally, could be important for exploring basic questions related to this cognitive capacity. For example, budgerigars (M. undulatus), a species of social parrot indigenous to Australia, represent a good candidate species because these birds form lasting bonds with breeding pairs and interact within coordinated flocks throughout the year (Wyndham 1980). Furthermore, previous research has demonstrated that these birds show automatic imitation to video stimuli (Mui et al. 2008), whereby the sight of another's action tends to elicit the same action in the observer (Sturmer et al. 2000). Using a naturalistic approach, Miller et al. (2012b) initially examined this species and revealed that yawns were temporally clustered in an undisturbed, established flock of captive budgerigars. These findings suggest yawning is contagious, similar to the other aforementioned observational studies; however, such methods cannot completely account for circadian physiological synchrony and/or collectively sensed environmental stimuli (both of which influence the expression of yawning, see Baenninger 1997).
 
Here, we describe two separate experimental studies designed to investigate the presence of contagious yawning in budgerigars in a controlled laboratory setting. Study 1 paired birds in adjacent cages with and without visual barriers, and the frequency of potentially contagious yawns (i.e., those occurring within a restricted temporal proximity) was compared based on the opportunity for visual information transfer. Given that in the wild, the group size and composition of budgerigars can fluctuate depending upon the season (Wyndham 1983) and that both sexes within this species show vocal call convergence to ingroup members when housed in captivity (Farabaugh et al. 1994; Hile et al. 2000), pairs of familiar and unfamiliar birds were tested together in this experiment to assess the potential for a familiarity bias in this response. Unlike chimpanzees or wolves, however, in which observing unfamiliar conspecifics may elicit hostility and familiarity biases for contagious yawning have been reported (Campbell and de Waal 2011; Romero et al. 2014), budgerigars show more fluid flocking and thus we did not expect a strong bias for contagious yawning. Since previous research has demonstrated that budgerigars respond to video displays of real and virtual conspecifics (Mui et al. 2008; Moravec et al. 2010; Mottley and Heyes 2003), Study 2 compared the yawn frequency of the same birds from Study 1 during exposure to video presentations of yawns versus control behaviors.
 
Discussion
Yawning in response to sensing or thinking about the action in others may represent a primitive form of empathy. Despite the potential importance of identifying various non-human species showing this capacity, comparative investigations of contagious yawning have been limited. These two experimental studies reveal the presence of contagious yawning in budgerigars in a controlled laboratory setting, corroborating a previous observational report assessing the temporal distribution of yawns in an undisturbed flock (Miller et al. 2012b). The experiment in Study 1 provides an ecologically valid measure of social contagion utilizing the signaling of a live demonstrator producing real yawns (improving upon Wilkinson et al. 2011). Temporally classified contagious yawns during these trials (i.e., those occurring within 5 min of a yawn from the matched pair) occurred more than three times as often when the birds could see one another, whereas there was no difference in the frequency of spontaneous yawning across visibility conditions. The experiment in Study 2 used a more traditional laboratory-based methodology for testing contagious yawning (e.g., Anderson et al. 2004), by presenting small groups of birds with repeated video clips of conspecific yawns and control behavior. In comparison with matched control stimuli, budgerigars in this experimental condition yawned more than twice as often and this response was not linked with indicators of stress or anxiety (i.e., self-directed behaviors). It is important to note, however, that this represents a modest effect given the magnitude of the video stimulus (over 150 yawns were displayed during the 10-min experimental session).
 
We found no evidence of an ingroup bias for contagious yawning in budgerigars. That is, yawns appeared similarly contagious between birds housed within the same aviary and across outgroup pairs. Previous experiments on chimpanzees and domesticated dogs have demonstrated mixed support for a familiarity bias in contagious yawning (Campbell and de Waal 2011; Romero et al. 2013; Silva et al. 2012; but see Madsen et al. 2013; Madsen and Persson 2013), while observational studies on primates (human and non-human) and wolves have shown a positive association with social closeness and affiliation (Demuru and Palagi 2012; Norscia and Palagi 2011; Palagi et al. 2009, 2014; Romero et al. 2014). There may be reasons to suspect that budgerigars would be less sensitive to familiarity or social closeness for various forms of state matching since they naturally live in much larger, more fluid groups of unrelated individuals than the abovementioned species and can form flocks of over 1000 coordinated members in the wild (Wyndham 1980).
 
Conversely, we have recently discovered evidence of an ingroup bias for stretching in this species (unpublished data), a more overt behavior directly relevant to flocking. It remains possible that limitations in the current study do not permit a true comparison to the documented ingroup/outgroup effects of contagious yawning in other species. For example, since all of the budgerigars were housed in the same room, this permitted vocal communication between the two groups and perhaps created some degree of familiarity or social affiliation prior to testing. Previous research has demonstrated that vocal call convergence occurs among budgerigars housed in captivity (Farabaugh et al. 1994; Hile et al. 2000), though in our study, vocalizations between the pairs were uncommon to nonexistent. Another limitation to the current study was that the degree of social closeness between cage mates was not recorded prior to the experiment, so this effect could not be assessed along a continuum.
 
In summary, budgerigars represent the first non-mammalian species, and only the fifth species to date (including humans, chimpanzees, domesticated dogs, and a subline of high-yawning Sprague&endash;Dawley rats), to show contagious yawning in an experimentally controlled setting. These findings provide an example of convergent evolution. Given the association between contagious yawning and empathy, we suggest additional comparative research be conducted to assess the prevalence of contagious yawning in other social vertebrates. Furthermore, since empathic responses have already been demonstrated in avian species (e.g., Edgar et al. 2011; Wascher et al. 2008), and the current findings show that contagious yawns can be experimentally manipulated, we propose that budgerigars represent a good model for exploring primitive forms of empathic processing.