Recent evidence suggests that yawning is a
thermoregulatory behavior. To explore this
possibility further, the frequency of contagious
yawning in humans was measured while outdoors in
a desert climate in the United States during two
distinct temperature ranges and seasons (winter:
22t; early summer: 3TC). As predicted, the
proportion of pedestrians who yawned in response
to seeing pictures of people yawning differed
significantly between the two conditions
(winter: 45%; summer: 24%). Across conditions
yawning occurred at lower ambient temperatures,
and the tendency to yawn during each season was
associated with the length of time spent outside
prior to being tested. Participants were more
likely to yawn in the milder climate after
spending long periods of time outside, while
prolonged exposure to ambient temperatures at or
above body temperature was associated with
reduced yawning. This is the first report to
show that the incidence of yawning in humans is
associated with seasonal climate variation,
further demonstrating that yawn-induced
contagion effects can be mediated by factors
unrelated to individual social characteristics
or cognitive development.
INTRODUCTION
Numerous hypotheses have been proposed to
explain why vertebrates yawn, and the two
prevailing hypotheses favor either physiological
or social function (Guggisberg et al., 2010).
Physiological hypotheses predict that yawning
acts to aid in the regulation of a given body
state (e.g., brain temperature or arousal),
while the social hypothesis predicts that
yawning functions to synchronize group behavior
by communicating unpleasant mental and physical
states. While experimental and observational
evidence of contagious yawning in humans (e.g.,
Provine, 1986; Platek et al., 2003), a few
select non-human primate species (chimpanzees,
Pan troglodytes; stumptail macaques, Macaca
arctoides; gelada baboons, Theropithecusgelada;
Anderson et al., 2004; Paukner and Anderson,
2006; Campbell et al., 2009; Palagi et al.,
2009), and dogs (Joly-Mascheroni et al., 2008;
but see Harr et al., 2009 and O'Hara and Reeve,
2011) provides support that yawning may have a
social role, tests of the specific predictions
of the social model are lacking and it is
unknown how yawning could reliably transmit
specific information during varying contexts
(Gallup, 2011). Furthermore, the ubiquity of
non-social yawning across vertebrate classes
(e.g., Baenninger, 1987) suggests that it has an
underlying physiological significance, and thus
may have multiple functional outcomes across
species.
Although it is still commonly believed that
yawning functions to equilibrate 02 and CO2
levels in the blood, there is no support for
this hypothesis and it has been concluded that
yawning and breathing operate by different
mechanisms (Provine et al., 1987). On the other
hand, one of the physiological hypotheses
receiving growing support proposes a role of
yawning in brain thermoregulation (Gallup and
Gallup, 2007, 2008). Recent evidence for this
model comes from prelimbic brain temperature
recordings in rats (Rattus norvegicus), showing
that yawning
is preceded by rapid increases in brain
temperature and followed by corresponding
decreases in brain temperature (ShoupKnox et
al., 2010). According to this model, cooling is
primarily the result of enhanced cerebral blood
flow and countercurrent heat exchange with
ambient air. Accordingly, the temperature of the
ambient air is what gives a yawn its utility.
Thus yawning should be counterproductive - and
therefore suppressed in ambient temperatures at
or exceeding body temperature, as taking a deep
inhalation of air would no longer promote
cooling. In other words, there should be a
"thermal window" or a relatively narrow range of
ambient temperatures in which to expect highest
rates of yawning (Gallup and Gallup, 2007).
Experimental studies on birds (Melopsittacus
undulatus) and rats (Rattus norvegicus) support
this view, showing that changes solely in
ambient temperature are sufficient to influence
yawning frequency (Gallup et al., 2009, 2010,
2011). In particular, yawns become more frequent
during initial increases in ambient temperature,
but then decrease as temperatures approach body
temperature.
The current study explored this relationship
in humans by measuring the incidence of
contagious yawning while outdoors during two
distinct periods of temperature and season
(winter and early summer) in Arizona, USA. The
summer condition provided temperatures that
matched or slightly exceeded body temperature
with relatively low humidity, while the
corresponding winter condition included milder
temperatures and slightly higher humidity. It
was predicted that yawning would be less
frequent in summer trials, but that it may be
common just after entering the outside
conditions since adaptive thermoregulatory
responses take time to occur after encountering
sudden climate changes. However, the rate of
yawning should diminish sharply as the amount of
time spent outside increases, since it would no
longer result in a cooling response. Contagious
yawning was used as a proxy for yawning in both
conditions because it is indistinguishable from
spontaneous yawning (aside from the fact that
the triggers differ), and it can be manipulated
using visual stimuli (e.g., Platek et al.,
2003). In other words, a stretching of the jaw
and a deep inhalation of air accompany both
responses, and thus the physiological
consequences should be similar. Furthermore, the
study of contagious yawning provides the
opportunity to determine whether underlying
features related to thermal homeostasis mediate
socially derived aspects of this behavior.
DISCUSSION
As predicted from the thermal window
hypothesis of thermoregulatory model, the
incidence of contagious yawning in humans was
influenced by seasonal variation in climate
conditions. According to this hypothesis, it is
the temperature of the ambient air that gives a
yawn its cooling utility and thus it was
expected that yawning should be diminished when
outdoor temperatures reach or exceed body
temperature. Across seasonal trials yawning was
associated with lower ambient temperatures, and
in particular, yawning was less frequent in the
summer condition when temperatures were higher
and humidity was lower. Furthermore, the
proportion of individuals yawning in the summer
dropped greatly as the length of time spent
outside increased, suggesting that the
expression of social yawning may reflect a
compromise with thermal effects. On the other
hand, there was a positive relationship between
time spent outdoors prior to testing and yawning
in the winter condition. Since all trials were
conducted in direct sunlight (where temperature
exceeded that recorded in the shade), it seems
likely that thermoregulatory responses will
increase over time under these conditions, thus
explaining this relationship.
The findings of this report are consistent
with previous research suggesting that the
triggers for spontaneous yawning are sensitive
to ambient air temperature and mechanisms of
brain thermoregulation. Recent experimental and
observational research has shown a connection
between yawning and ambient temperature
manipulation/variation in other animals
(Deputte, 1994; Campos and Fedigan, 2009; Gallup
et al., 2009, 2010, 2011). Due to inherent
limitations of field research, future studies
should experimentally investigate the
association between human yawning and more
refined ambient temperature ranges in the
laboratory. In addition, research should
investigate the
frequency of yawning in extreme cold
climates since yawning in severe cold
temperatures would be expected to have adverse
effects on brain thermoregulation, and thus
should be inhibited. Moreover, considering
yawning or yawn-like behaviors are ubiquitous
across vertebrate classes, research should
explore the relationship between yawning and
seasonal climate variation in
poikilotherms.
This study is the first to show that the
expression of yawning in response to contagious
stimuli can be altered by variation in seasonal
climatic conditions. Furthermore, while previous
research has shown that specific individual
social characteristics and cognitive
developmental factors are involved with the
susceptibility to yawning contagiously in humans
(e.g., Anderson and Meno, 2003; Platek et al.,
2003; Senju et al., 2007; Millen and Anderson,
2010), this study further indicates that
yawn-induced contagion effects can also be
mediated by non-social factors (e.g., ambient
temperature). These findings extend the logic of
the thermal window hypothesis to humans,
demonstrating a highly conserved, comparative
aspect to the expression of this behavior.
Consistent with the thermoregulatory model,
these results dovetail with recent research
showing that methods of behavioral brain cooling
(nasal breathing and forehead cooling) inhibit
contagious yawning in humans (Gallup and Gallup,
2007). Taken together, future studies of
contagious yawning should be assessed under
conditions where thermal effects are essentially
neutral, or at least consistent, across
conditions.
In summary, while the utility of yawning as
a contagious behavior is still under debate, the
current findings suggest the underlying
mechanism for this response may be involved with
thermoregulatory physiology, further challenging
the view that the origin of yawning is social
(Guggisberg et al., 2010).
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