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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

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12 septembre 2010
Animal Behaviour
Handling stress initially inhibits,
but then potentiates yawning in budgerigars
(Melopsittacus undulatus)
Michael L Miller, Andrew C. Gallup, Andrea R. Vogel, Anne B. Clarak
Integrative Neuroscience Program, Department of Psychology
Department of Biological Sciences
Binghamton University


Andrew C. Gallup. Yawning and the thermoregulatory hypothesis
Brain Temperature & Autonomic Nervous System for the study of relaxation
In mammals, yawning is associated with social and physiological stress, as well as thermoregulation, but little is known about why yawning occurs in stressful contexts or how it is integrated with natural stressors. To investigate the stress sensitivity of yawning in birds, we exposed budgerigars (Melopsittacus undulatus) to a handling stressor that simulated a predatory encounter. Each bird was captured, gently held for 4 mm, and then released and videotaped for I h (experimental). On a separate day (±24 h), the undisturbed animal was videotaped for I h (control). The relationship between handling-induced yawning and body temperature was assessed in a separate experiment, in which the underwing temperatures of the same birds were measured at I min intervals during a 4 min holding period. After handling stress, yawning frequency was initially suppressed, then sharply increased within 20 min. Underwing temperature increased during handling, and individuals' final temperatures at minute 4 were negatively correlated with their latencies to yawn after handling. Thus, stress-induced hyperthermia may be responsible for associations between yawns and stress. These results indicate that yawning may offer a sensitive, noninvasive measure of stress in birds.

Yawning is phylogenetically old and ubiquitous among vertebrates (Baenninger 1987), but little is known about its physiological function. It is commonly thought to equilibrate oxygen and carbon dioxide imbalances in the blood, but there is no experimental support for this hypothesis (Provine et al. 1987b). On the other hand, there is strong evidence to suggest that yawning is associated with social (Baenninger 1997) and physiological stress (Gallup & Gallup 2008), including thermal challenges in birds (Gallup et al. 2009). In line with this, yawning may increase brain arousal, and this arousing function may explain the behaviour's association with stress (Baenninger 1997; but see Guggisberg et al. 2007).
Yawning, or behaviour resembling yawning, is associated with stressful events in several nonhuman primates, as well as other mammals. In crested black macaques, Macaca nigra, yawning occurs during intense agonistic interactions and other hostile social situations (Hadidian 1980). Troisi et al. (1990) interpreted yawning by subordinates in this context as a response to stress, and those by dominants as a threat display. In these macaques, yawning also follows abrupt, startling disturbances, such as thunder, that may induce low-level, acute stress (Hadidian 1980). Likewise, in greycheeked mangabeys, Cercocebus albigena, yawning occurs in close temporal proximity to alarm calling in the presence of predators (Deputte 1994). Among primates, similarities between threat displays and yawning confounds interpretations of yawning (Vick & Paukner 2010), making it informative to study yawning in species without open-mouth threat displays. Yawning is also associated with physical stress in laboratory rats (Rattus norvegicus) in that foot-shock strongly increases yawning (Moyaho & Valencia 2002). Taken together, there appears to be a close relationship between stress and yawning in a range of mammals.
In budgerigars (Melopsittacus undulatus), the only birds in which yawning has been experimentally studied, yawning occurs more frequently as ambient temperature increases (22-34'C) towards body temperature (Gallup et al. 2009). In addition, yawning in budgerigars is significantly correlated with other avian thermoregulatory behaviours (e.g. panting, wing venting; Gallup et al. 2010), suggesting that yawning is triggered by the need to decrease elevated body and/or brain temperatures. If temperature regulation is one general function of yawning in homeotherms, stress-associated yawning may be a response to increases in body temperature induced by external stressors (i.e. stress-induced hyperthermia; reviewed in Olivier et al. 2003). For instance, when common eiders, Somateria mollissima, were handled, their body and skin temperatures increased within 4 min following the start of the trial (Cabanac & Guillemette 2001). Stress-induced hyperthermia may produce the intimate relationship between stress, yawning and thermoregulation.
Although yawning is linked to stress across diverse contexts in mammalian species, no experimental studies in birds have evaluated the effect of stress on yawning. Because yawning is an overt, distinguishable behaviour, characterizing its relation to stress may make it a suitable behavioural measure of stress. In this study, we investigated the stress-yawn relationship in budgerigars by inducing acute stress through handling. The degree of handling (i.e. gentle restraint in a gloved hand following a quick capture) was comparable to that experienced by birds during routine measurements in the laboratory and in the field (e.g. Cabanac & Guillemette 2001; Carere & van Oers 2004; Fucikova et al. 2009). We recorded each bird's yawning and stretching frequencies both following brief handling (experimental) and during a similar period with no preceding disturbance (control). We hypothesized that yawning would increase in frequency after the handling session relative to the control period, but would show no temporal pattern during the control period. Because of the temporal association between yawning and stretching among humans and rodents (reviewed in: Baenninger 1997; Provine et al. 1987a), we also recorded stretching. Yawning and stretching in budgerigars are temporally associated in nonexperimental settings (M. L Miller, S. M. Vicario & A. B. Clark, unpublished data). Interestingly, this temporal relationship is decoupled as temperatures increase, presumably when yawns serve a thermoregulatory function that stretching does not (Gallup et al. 2010). Thus, if stress-induced yawning is specifically related to body temperature and brain arousal, stretching should remain unaffected after a simulated predatory encounter.
Yawning and Stretching
We observed 63 yawns in total (42 by the six males, 21 by the four females) during 20 h of observation (10 trials, 2 h/bird). To assess whether the birds' latency to yawn differed between control and experimental conditions, the model included trial condition, trial order and the interaction between these two factors. For this full model, there was no difference in yawning latency between trials categorized by order (F1,8 = 0.62, P = 0.45, partial Tj2 = 0.07) and no interaction between trial condition and trial order (F1,8 = 1.50, P = 0.26, partial j2 = 0.16). After removing trial order from the model, the latency to the first yawn was significantly later in the experimental condition than in the control condition (1322 + 144 s versus 787 ± 189 s; F1,9 = 5.96, P= 0.04, partial 12 = 0.40).
Of the 63 yawns, 34 (3.4 ± 0.54/bird) occurred during the experimental condition and 29 (2.9 + 0.31/bird) occurred during the control condition. To investigate whether there were differences in yawning frequencies between trial conditions and across time intervals, the model included trial condition, time interval, trial order and all interactions between these factors. In the full model, there was no difference in total yawning frequencies between the two trial conditions (F1,8 = 1.02, P = 0.34, partial = 0.11) or between the three 20 min intervals (F2,16 = 0.65, P = 0.54, partial i12 = 0.08). There was also no difference in yawning frequencies between trial orders (F1,8 = 0.02, P = 0.90, partial j2 <0.01), and no interactions between trial order and condition (F1,8 = 2.00, P = 0.20, partial t2 = 0.20), between trial order and time interval (F2,16 = 0.42, P = 0.67, partial = 0.05), or between trial order, time interval and trial condition (F216 = 0.64, P = 0.54, partial i12 = 0.07). After removing trial order from the model, there was a significant interaction between time interval and trial condition (F2,18 = 3.88, P= 0.04, partial Ti 2 = 0.30; Fig. lb). Paired comparisons between the trial conditions within each time interval indicated that yawning frequency was (1) lower in the experimental condition than in the control condition during the first 20 min (t9 = 2.23, P = 0.05), (2) greater in the experimental condition than in the control condition during the second 20 min interval (t9 = -2.45, P = 0.04) and (3) not different during the final 20 min interval (t9 = -1.05, P = 0.32).
We observed a total of 69 stretches (41 by males, 28 by females) during the 20h of observation. The same set of analyses was run to investigate whether latency to stretch differed between control and experimental conditions. Unlike yawning, there was no difference in latencies to the first stretch between the experimental and control conditions (1913 ± 307 s versus 1931 +403 s; F1,8 = 0.00, P = 0.97, partial t2 = 0.00). In addition, there was no difference in stretching latency between trial orders (F1,8 = 0.31, P = 0.59, partial = 0.04), and no interaction between trial condition and trial order (F1,8 = 1.34, P = 0.28, partial j2 = 0.14).
To investigate whether stretching frequencies differed between conditions and across intervals, the full model included trial condition, time interval, trial order and interactions between these factors. For this model, stretching frequencies did not differ between trial conditions (F1,8 = 0.03, P=0.86, partial <0.01) or trial orders (F1,8 = 0.79, P = 0.40, partial = 0.09), and there was no interaction between trial order and condition (F1,8 = 0.17, P = 0.69, partial t2 = 0.02), or between trial order and time interval (F2,16 = 0.45, P = 0.64, partial 2 = 0.05). Unlike yawning, there was no significant interaction between time interval and trial condition (F2,16 = 2.05, P = 0.16, partial 2 = 0.20). There was also no interaction between trial condition, time interval and trial order (F2,16 = 0.35, P = 0.71, partial 2 = 0.04). When removing trial order from the model, stretching differed significantly across the three time intervals (F2,18 = 4.31, P = 0.03, partial î2 = 0.32). Post hoc corrections showed no significant pairwise comparisons (all Ps > 0.05).
Temperature Changes with Handling
During the temperature assessment session, budgerigar body temperature steadily increased during the handling session (Fig. 2a). Average temperature differed across the four I min intervals (Friedman's test: = 18.04, P <0.01). All pairwise comparisons between time intervals showed a significant increase from one interval to the next (Ps < 0.05), except between the second and third minute, which was nearly significant (P = 0.06). A budgerigar's previously recorded behaviour (yawns or stretches) was then correlated with this individual's underwing temperature. Underwing temperatures at the end of the handling sessions were strongly and negatively correlated with the latency to first yawn (Kendall's tau correlation: b = -0.62, P = 0.03; Fig. 2b). This indicates that birds with higher body temperatures following handling yawned sooner during the experimental condition. Underwing temperatures at the fourth minute were not correlated with an individual's total yawn frequency (b = 0.15, P = 0.61) or with the number of yawns during any one of the three 20 min intervals (all Ps > 0.05). Increases in temperature (i.e. difference between the final and first minute) were not correlated with (1) yawn latency (b = -0.18, P = 0.53), (2) total yawning frequencies (b = 0.42, P = 0.16) or (3) yawning frequencies across each 20 min interval (all Ps > 0.05). Unlike yawning, stretching by individuals was not correlated with either temperature at the fourth minute or change in temperature (Ps > 0.05).
These results illustrate that yawning in budgerigars is affected by handling stress. Yawns were initially suppressed, but then increased in frequency after 20 min. As handling may simulate escape from a predator, initially suppressing yawns may adaptively reduce attention-getting movements and/or reduce conflict with other antipredatory behaviours. Because acute stress increases body temperature (e.g. Cabanac & Guillemette 2001), a spike in yawning after 20 min is adaptive, since research suggests yawning is a thermal-stabilizing mechanism that decreases brain and/or body temperature (e.g. Gallup & Gallup 2007, in press: Gallup et al. 2009). This interpretation is supported by the strong negative correlation between individuals' body temperatures after handling and their latencies to first yawn (see Fig. 2b), indicating that higher body temperatures may trigger birds to yawn sooner. In contrast to yawning, stretching did not change in frequency after the stressor. Stretching frequencies were also unrelated to the individuals' body temperatures, suggesting that stretching lacks a thermoregulatory role (Gallup et al. 2009).
These results are consistent with previous findings in other species that demonstrate a temporal association between yawning and stress. For instance, in South African ostriches, Struthio camelus australis, yawning did not occur during intense activity, but did occur when startling stimuli were recognized as innocuous, presumably sometime after the stressor (Sauer & Sauer 1967). When rats were exposed to a novel environment, yawning gradually increased, peaking after 30 min (Moyaho & Valencia 2002). Similarly, when rats were foot-shocked at fixed, 10 min intervals, yawning was initially low, but then gradually increased and peaked by 40 min. On the other hand, increases in yawning were less pronounced when rats were foot-shocked at random intervals (Moyaho & Valencia 2002). This is consistent with the budgerigar data, because it shows that yawning occurs during a recovery period following a stressor: when foot-shocked at known intervals, rat yawning dramatically increases, but when randomly footshocked, yawning does not increase as dramatically, presumably because the stress state persists. These data suggest that yawning is related to the recovery period following a stressor and may be an adaptive response that increases vigilance as the environment becomes more predictable (see Greco et al. 1993).
The appearance of yawns during the second 20 min interval is in accord with the view that yawning is a thermoregulatory behaviour in budgerigars (Gallup et al. 2009, 2010). The increased yawns observed during the second 20 min interval may be explained by temperature increases that follow handling stress (Olivier et al. 2003). Similar to the effect of handling on eider ducks (Cabanac & Guillemette 2001), handling increased underwing temperature of budgerigars. This increase in temperature was substantial and rapid, approximating 2 °C within 3-4 min. Cabanac & Guillemette (2001) demonstrated that duck temperature peaked by 10 min of handling, and hyperthermia was maintained for at least 30 min. Therefore, if the time course of body temperature is similar in budgerigars, the spike in yawning during the second interval may have been a compensatory mechanism to reduce brain and/or body temperatures following the simulated capture and escape. Moreover, latency to yawn was negatively correlated with skin temperature measured at the fourth minute. This indicates that birds that responded to stress with greater temperature increases needed to yawn sooner, but not at higher frequencies. In short, increases in metabolic activity following stress inevitably cause increases in body temperature. Whether this increase in temperature is adaptive or a metabolic by-product is unclear: however, yawning may provide a means to regain thermal homeostasis after a stressful event.
Since yawning is an easily distinguishable behaviour, these results suggest that measuring yawns may provide a suitable method to detect and qualitatively measure stress noninvasively. It is difficult to measure stress without disturbing an animal, making accurate assessment of stress difficult. For instance, in laboratory settings, collecting blood to measure corticosterone (CORT) levels inherently produces an emotional response, thereby affecting plasma concentrations of stress hormones, such as CORT (Thanos et al. 2008). To appreciate the application of yawning as a technique to measure stress, it is important to note the sensitivity of this relationship. Although the birds used in this experiment were accustomed to daily human contact over a period of many years,
the flock continues to respond to human entry with increased movement and vocalization (personal observation). In a pilot study, entering the room to turn on a camera was sufficient to inhibit yawns during the first 20 min of the control condition (M. L Miller, J. A. Cusick, D. M. Sutton, A. R. Vogel, A. C. Gallup & A. B. Clark, unpublished data), which is why recordings were remotely started in the control trials. This is not unreasonable, as the heart rates of laboratory mice increase when a technician enters the colony and this effect persists for at least 2 weeks after the first exposure (Kramer et al. 2004). Monitoring yawns may provide a sensitive measure of individual responsiveness to acute stressors.
In summary, these results illustrate a relationship between yawning, stress and thermoregulation in birds. This report provides critical insight into the association between yawning and arousal. It is the first to show that yawning is delayed after a simulated predator's attack and also replicates previous studies, showing that yawns are strongly associated with changing body temperature. These findings also suggest that yawning may provide a noninvasive measurement of stress in field and laboratory settings. Follow up studies should measure other physiological parameters related to stress (e.g. plasma CORT), and then correlate these with yawning.
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Andrew C. Gallup. Yawning and the thermoregulatory hypothesis