mystery of yawning
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Yawning: its cycle, its role
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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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mise à jour du
8 mai 2011
 
International Scholarly Research Network
ISRN Zoology
Volume 2011
Article ID 271209
Co-occurrence of yawning and stereotypic behaviour in horses Equus caballus
 
Fureix Carole, Gorecka-Bruzda Aleksandra, Gautier Emmanuel, Hausberger Martine
 
Université Rennes, Ethologie Animale et Humaine
Polish Academy of Sciences, Department of Animal Behaviour
 
Equine Colic
Horses's stretching
Investigating determinants of yawning in the domestic (Equus caballus) and Przewalski (Equus ferus przewalskii) horses
Górecka-Bruzda A, Fureix C, et al.

Chat-logomini

ABSTRACT
 
Determinants of yawning are still uncertain. As yawning seems to be triggered by stress and emotional contexts, we investigated specific correlates of yawning and stereotypic behaviours in horses. Study 1 investigated correlations in time between yawning and stereotypic behaviour in stereotypic horses from a same facility; study 2, involving riding school horses, investigated co-occurrence of yawning and stereotypic behaviour at the individual level and in response to environmental factors (feeding time). Results showed that 1) stereotypic horses yawned more than the non-stereotypic horses, 2) yawning increased at the same time periods as stereotypic behaviours did and 3) yawning frequency was positively correlated with stereotypic behaviour frequencies (studyl). Different hypotheses are discussed: direct / indirect causal relationship, other factors susceptible to trigger both yawning and stereotypies. This study, underlining for the first time a co-occurrence of yawning and stereotypic behaviour, opens a promising line of investigation of this puzzling behaviour.
 
1. Introduction
 
A yawn is an involuntary sequence consisting in mammals of mouth opening, deep inspiration, brief apnoea and slow expiration [1], and is especially frequent in humans and carnivores e.g. [2,3]. However, studies of behaviour have neglected yawning [4] and, although a number of hypotheses attempt to explain its causality, experimental data are relatively scarce compared to the abundance of theoretical considerations (reviewed by [5]).
 
Determinants of yawning are still uncertain. The fact that yawning is involved in behavioural state changes is well established, especially in quiet contexts of motor relaxation such as before or just after sleep (e.g. [1,2,3,6,7,8]). However, yawning can also be triggered by stress and emotional contexts (e.g. agonistic social interactions in primates: [1,3]; potential heat stress in budgerigars: [9]). Thus, intracerebroventricular administration of the synthetic adrenocorticotropic hormone ACTH 1-24 increases the frequency of yawning in rats (e.g. [10]) and dogs [6]. Co-occurrence of yawning and changes of behaviour associated with stress (e.g. restlessness, lowered posture) has been reported in dogs [11]. Yawning has been proposed to be a "displacement activity" in primates [12], i.e. a behavioural pattern apparently irrelevant to the animal's ongoing activity, thought to occur in stressful situations [13]. Clinical approaches of yawning reveal that, among numerous pathologies (such as schizophrenia, multiple sclerosis, epilepsy, migraine headache), being under stress is conducive of yawning in humans e.g. [14,15]. Recently, Reamer et al. [16] exploring correlates of self-directed behaviour and "abnormal" stereotypic behaviour, prevalent in stress-inducing environments (e.g. [17]) in captive red-capped mangabeys (Cercocebus torquatus torquatus), failed to evidence a relationship between yawning and stereotypic behaviour. Unfortunately, their analysis did not separate yawning from other self-directed behaviours (i.e. self-scratching, self-grooming and body shaking).
 
Here, we investigated specific correlates of yawning and stereotypic behaviours in horses. Horses can be informative models, as a variety of stereotypies has been well described [18] and this species is known to yawn [1,19], a case rare amongst ungulates. We report two studies, both involving equestrian facilities where horses were kept in social isolation (i.e. in boxes) and experienced time-restricted feeding practices, two factors known to trigger stereotypies [20,21]. These two studies are complementary: study 1, considering only stereotypic horses in a facility where all horses were kept under the same conditions (same practices, same food, same sex, mostly same breed), investigated correlations in time between yawning and stereotypic behaviour; study 2, performed in an ordinary mixed-sex riding school population, investigated potential sex effects and potential co-occurrence of yawning and stereotypic behaviour at the individual level and in response to environmental factors (ii e. feeding time). Observations of these horses in their box revealed clear co-occurrence of yawning and stereotypic behaviour and even, in study 1, correlation between times performing both behaviours at the individual level. This co-occurrence of yawning and stereotypic behaviour opens a promising line of investigation, potentially broaching different functions of this puzzling behaviour.
 
4. Discussion
 
We observed in horses clear co-occurrences of yawning and stereotypic behaviours in two different situations: a one place - one sex situation and ordinary mixed-sex riding school populations. Horses presenting stereotypic behaviour yawned more than the non-stereotypic horses. Yawning increased at the same time periods as stereotypic behaviours did and its frequency was, in the first study, correlated with stereotypic behaviour frequencies: the more frequent their stereotypic behaviours, the more horses yawned. Interestingly, type of stereotypic behaviour (oral / motor) did not influence this correlation. Frequencies of occurrence as well as proportions of horses yawning did not differ between the two studies. No effects of age or of sex could be evidenced for either type of stereotypic behaviour.
 
Our results underline for the very first time a clear relationship between yawning and behavioural disorders (Le. stereotypies), using an original model, the horse. To our knowledge, only one previous study broached this issue, but it failed to evidence correlates between yawning and stereotypic behaviours in captive red-capped mangabeys [16]. However, Reamer et al.'s analysis did not separate yawning from other self-directed behaviours (SDB), and the authors argued that the hygienic function of some of these SDB (e.g. self-grooming) could have masked variations in rates of SDB linked to emotional states.
 
Three lines of hypotheses can be considered to explain the relationship between yawning and stereotypic behaviours in our study. Firstly, a direct causal relationship (L e. one behaviour triggers the other) may be involved. However, the kind of physiological and / or behavioural mechanism underlying such a direct causal relationship between yawning and stereotypies is not clear, and remains to be investigated. Moreover, temporal analysis of our data revealed that yawning did not occur more frequently after or before stereotypic behaviours than after or before other behaviours (Fureix et al, unpublished data).
 
More interesting is the hypothesis that one of the behaviours may trigger the other indirectly through another factor (Le. an indirect causal relationship). Interestingly, stereotypic horses have been reported to lie down and sleep less than non-stereotypic horses, maybe because of being focused on their stereotypic behaviours [22]. This may induce tiredness (because of less sleep and more energy spent performing repetitive movements), and drowsiness is a factor commonly reported to trigger yawning e.g. [1,2,3,6,7,8]. Moreover, according to the brain cooling hypothesis, excessive yawning appears to be symptomatic of conditions that increase brain and/or core temperature (see [14]), and these conditions include sleep deprivation. Additionally, the energy spent in repetitive movements and / or mental activity in relation to stereotypic behaviours may promote an increase in brain temperature in stereotypic horses, which could trigger compensatory yawning according to Gallup and Gallup's [14] brain cooling hypothesis.
 
The third hypothesis predicts that other factors, among which gastrointestinal dysfunctions (common in domestic ungulates, [26]) can be mentioned, trigger both yawning and stereotypies. Indeed, gastric diseases can be accompanied by yawning [4] and co-occurrence of stereotypy performance and gastrointestinal acidity has led to suggestions that oral stereotypic behaviours are a response to gut health (perhaps having some beneficial effects, for instance by generating saliva that helps to rectify gastrointestinal pH) [26]. However, the relationship we observed between yawning and stereotypic behaviours seems to be independent of type of stereotypy (L e. oral but also motor), and all but one (in ENE horses) or two (in riding school horses) stereotypic behaviours were linked with, or increased at the same time periods as yawning. Thus these results suggest that, even if possibly involved, gastrointestinal dysfunctions are not the only mechanism at stake.
 
Interestingly, the riding school horses yawned and displayed stereotypic behaviours more often before meals than outside feeding periods, in accordance with previous studies focusing independently on yawning (e.g. [2,4,15,27]) or stereotypic behaviour occurrences (e.g. [26]. Physiological factors such as hunger can trigger yawning (L e. the increase of yawning at the beginning of diabetics' hypoglycaemia, similar to the feeling of hunger in non-diabetics [15]). However, feeding is probably one of the major events in the day of captive animals, and the importance of psychological factors (e.g. frustration) has been suggested by Mason (1971, cited in [28]) who observed that cortisol increased in monkeys when they were not given food (... while their neighbours were), and that this response disappeared when they were given non-nutritive pellets of the same appearance and flavour as their food.
 
Moreover, the frequencies of the stereotypic behaviours of the ENE horses did not increase before meals. This may be due to the fact that they were all given exactly the same food, at the same time, by an automatic feeder, thus creating a less frustrating situation (i.e. no delay between the first and the last horse fed in the stable) compared to the manual distribution of food in the riding schools. However one has to note that co-occurrence between yawning and stereotypic behaviours was observed outside meal periods and both were more frequent in the afternoon than in the morning. Interestingly, no hay was given to the horses in the afternoon (while they were fed hay in the morning), suggesting that these horses may be more frustrated in the afternoon.
 
Here, following the third hypothesis, we argue that frustration may be a common factor triggering both yawning and stereotypic behaviours. Researchers have proposed that yawning is a "displacement activity" (e.g. [12,16]), known to occur in frustration-inducing situations [13], and frustration is the "one common factor to all conditions in which stereotypies develop" [29]. Moreover, motivational explanations of stereotypic behaviours argue that, if sustained, displacement activities resulting from frustration-related stress can develop into stereotypies (e.g. development of pacing by food-frustrated hens repeatedly trying to escape their cage [30]). Our aim here is clearly not to argue that yawning is a stereotypic behaviour, but that individual susceptibility to frustration may be a common mechanism susceptible to explain the co-occurrence of these behaviours in horses kept under suboptimal environmental conditions (confinement, social isolation, time-restricted feeding practices).
 
Moreover, the horses studied here both yawned and displayed stereotypic behaviours more often than do feral horses and horses kept under natural conditions studied in a comparative approach (Górecka et al., in prep). In addition to the clear relationship between yawning and stereotypies, our results reinforce the importance of exploring yawning in relation to welfare issues.
 
In our study, yawning and stereotypic behaviour frequencies were not significantly influenced by the horses' sex, age or breed. Yet yawning has been reported as more frequent in males and in adult than younger males in non human primates, and this has been related to androgen (testosterone) levels and sexual maturity [3,31]. The higher prevalence in sexually mature males is also supported by another study including stallions (Górecka et al., in prep). Thus, the fact that all the males we studied here were adult geldings (i.e. castrated horses) may explain the lack of sex- and age-related differences in our study and reinforces the idea that testosterone levels may be involved.
 
In conclusion, and given the current state of knowledge, yawning has a complex causation, and the relationship between yawning and stereotypies observed in horses offers a promising line of investigation. Amongst the challenging issues is the general problem of distinguishing between an "abnormal" behaviour (e.g. displacement activity) and the same behaviour pattern in a "normal" pattern [12,13]. Thus, it would be interesting to study more precisely the morphology of yawning according to context (e.g. pre-prandial / outside feeding time, displayed by stereotypic / non-stereotypic animals), by taking into account yawning duration and inter-occurrence latencies, preceding / following behaviours, presence / absence of stretching, association with other postural elements. Such an approach should help to identify different kinds of yawning (at rest, emotional...), and potentially different functions of this puzzling behaviour.
 
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