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.
6. References
1. Walusinski O, Deputte BL (2004) Le
bâillement: phylogenèse,
éthologie, nosogénie. Revue
Neurologique 160: 1011-1021.
2. Barbizet J (1958) Yawning. Journal of
Neurology Neurosurgery and Psychiatry 21:
203209.
3. Deputte BL (1994) Ethological study of
yawning in primates 1. Quantitative-analysis and
study of causation in 2 species of old-world
monkeys (Cerbocebus-albigena and
Macaca-Fascicularis). Ethology 98: 221-245.
4. Baenninger R (1987) Some comparative
aspects of yawning in Betta splendens, Homo
sapiens, Panthera leo and Papio sphinx. Journal
of Comparative Psychology 101: 349354.
5. Guggisberg AG, Mathis J, Schnider A, Hess
CW (2010) Why do we yawn? Neuroscience and
Biobehavioral Reviews 34: 1267-1276.
6. Greco M, Baenninger R, Govern J (1993) On
the context of yawning - When, where and why.
Psychological Record 43: 175-183.
7. Giganti F, Hayes MJ, Cioni G, Salzarujo P
(2007) Yawning frequency and distribution in
preterm and near term infants assessed
throughout 24-h recordings. Infant Behavior
& Development 30: 641-647.
8. Zilli I, Giganti F, Salzarulo P (2007)
Yawning in morning and evening types. Physiology
& Behavior 91: 218-222.
9. Siqueira LD (2009) Yawning and
thermoregulation in budgerigars: lack of support
from results. Animal Behaviour 78: E1-E2.
10. Eguibar JR, Barajas M, Moyaho A (2004)
Genotype-dependent effect of ACTH(l -24) on
grooming and yawning in two inbred strains of
rats. Neuropeptides 38: 283-288.
11. Beerda B, Schilder MBH, van Hooff J, de
Vries HW, Mol JA (1998) Behavioural, saliva
cortisol and heart rate responses to different
types of stimuli in dogs. Applied Animal
Behaviour Science 58: 365-381.
12. Maestripieri D, Schino G, Aureli F,
Troisi A (1992) A modest proposal - Displacement
activities as an indicator of emotions in
primates. Animal Behaviour 44: 967-979.
13. Tinbergen N (1952) Derived activities:
their causation, biological significance,
origin, and emancipation during evolution. The
Quarterly Review of Biology 27: 1-32.
18. Mills DS (2005) Repetitive movement
problems in the horse. In: McDonnell DSMaSM,
editor. The Domestic Horse, The Origins,
Development and Management of its Behaviour.
Cambridge: Cambridge University Press. pp.
212-227.
19. Waring G (2003) Horse Behavior, second
edition. Norwich, New York: Noyes
Publications/William Andrew Publishing. 442
p.
20. McGreevy PD, Cripps PJ, French NP, Green
LE, Nicol CJ (1995) Management factors
associated with stereotypic and redirected
behavior in the thoroughbred horse. Equine
Veterinary Journal 27: 86-91.
21. Cooper JJ, McDonald L, Mills DS (2000)
The effect of increasing visual horizons on
stereotypic weaving : implications for the
social housing of stabled horses. Applied Animal
Behaviour Science 69: 67-83.
22. Hausberger M, Gautier E, Muller C, Jego
P (2007) Lower learning abilities in stereotypic
horses. Applied Animal Behaviour Science 107:
299-306.
23. Hausberger M, Gautier E, Biquand V,
Lunel C, Jego P (2009) Could work be a source of
behavioural disorders? A study in horses. PbS
ONE 4: e7625.
24. Altmann J (1974) Observational study of
behaviour: sampling methods. Behaviour 49:
227-267.
25. Siegel S, Castellan J (1988)
Nonparametric statistics for the behavioral
sciences, second edition. New York:
McGraw-Hill.
26. Bergeron R, Badnell-Waters AJ, Lambton
S, Mason G (2006) Stereotypic oral behaviour in
captive ungulates: foraging, diet and
gastrointestinal functions. In: Mason G, Rushen
J, editors. Stereotypic animal behaviours -
Fundamentals and applications to welfare 2nd
edition. Wallingford, Oxford: CABI. pp.
19-57.
27. Holmgren B, Budelli R, Urbaholmgren R,
Eguibar JR, Holmgren M, et al. (1991) Food
anticipatory yawning rhythm in the rat. Acta
Neurobiologiae Experimentalis 51: 97105.
28. Mormede P, Andanson S, Auperin B, Beerda
B, Guemene D, et al. (2007) Exploration of the
hypothalamic-pituitary-adrenal function as a
tool to evaluate animal welfare. Physiology
& Behavior 92: 317-339.
29. Ôdberg F. Abnormal behaviours:
stereotypies. In: Garci, editor; 1978; Madrid.
Industrias Graficas Espana. pp. 475-480.
30. Rushen J, Mason G (2006) A
decade-or-mor&s progress in understanding
stereotypic behaviour. In: Rushen J, Mason G,
editors. Stereotypic animal behaviours
Fundamentals and applications to welfare 2nd
edition. Wallingford, Oxford: CABI. pp.
1-17.
31. Troisi A, Aureli F, Schino G, Rinaldi F,
Deangelis N (1990) The influence of age, sex,
and rank on yawning behavior in 2 species of
macaques (Macaca-fascicularis and M Fuscata).
Ethology 86: 303-3 10.
