- Andrew
C. Gallup. Yawning and the thermoregulatory
hypothesis
-
- Recently, Campos and Fedigan (2009)
described some behavioral adaptations to heat
stress and water scarcity in three distinct
groups of white-faced capuchins (Gebus
capueinus) inhabiting the Santa Rosa National
Park in Costa Rica. The authors conclude that at
least one specific self-directed behavior
("tongue out") has a thermoregulatory function.
Evidence for this comes from data showing that
on average, capuchins exposed their tongues more
frequently during hot and dry conditions. In
particular, tongue out behavior occurred at mean
temperatures exceeding the 99% bootstrap
confidence interval (BCI) for temperature and
below the 99% BCI for humidity. Although yawning
met the same criteria (occurring during higher
mean temperatures and lower mean humidity), the
authors do not suggest a thermoregulatory
function for this behavior. Campos and Fedigan
(2009) state, instead, that the observed pattern
is "likely a byproduct of the association
between yawning and resting," and when
considering resting and temperature are
positively correlated, it was concluded that
yawning does not participate in
thermoregulation. I feel the authors are 1)
overly vague when referring to yawning as a
byproduct of resting and 2) too quick to
discount a thermoregulatory value.
Methodological constraints in this study do not
allow for a more convincing examination of the
potential role of yawning in regulating body
temperature.
-
- Recent research suggests the biological
function of yawning among homeotherms is
thermoregulation (for a review see Gallup,
2010). More specifically, it has been proposed
that yawning serves to stimulate cortical
arousal as a brain cooling mechanism (Gallup and
Gallup, 2007). According to this model, yawning
is triggered to maintain brain thermal
homeostasis when other regulatory mechanisms
fail to operate favorably. Brain temperature is
affected by a number of variables, including the
temperature of the blood supplying the brain,
rate of blood flow through the brain, and rate
of metabolic heat production. Yawning
contributes to the first two of these variables.
The deep inhalation of air taken into the lungs
raises blood pressure (Askenasy and Askenasy,
1996) and causes acceleration in heart rate
(Greco and Baenninger, 1991; Guggisberg et al.,
2007). Likewise, the constriction and relaxation
of facial muscles during a yawn increases facial
blood flow and these changes are thought to
increase cerebral blood flow (Zajonc, 1985;
Askenasy, 1989). Together, these processes are
believed to operate like a radiator by removing
hyperthermic blood from specific areas while
introducing cooler blood from the lungs and
extremities, thereby cooling cortical surfaces
through convection. The gaping of the mouth and
deep inhalation of air during a yawn is thought
to cool venous blood draining from the nasal and
oral orifices into the cavernous sinus, which
surrounds the internal carotid artery supplying
blood to the rest of the brain. Recent research
provides strong support for this model showing
that 1) excessive yawning in humans is triggered
during mild hyperthermia and produces
significant decreases in body temperature
(Gallup and Gallup, in press) and 2) spontaneous
yawning in rats is preceded by rapid increases
in brain temperature, which are followed by
corresponding decreases in temperature after a
yawn (Shoup ML et al., unpublished data).
-
- One of the predictions of the brain cooling
hypothesis, other than producing direct brain
cooling effects, is that yawning frequency
should be influenced by variation in ambient
temperature. In particular, it is hypothesized
that yawning should increase as ambient
temperature approaches body temperature. It is
assumed that a rise in ambient temperature
activates thermoregulatory mechanisms that
function to maintain brain and body temperature
within a normal range. This prediction has been
recently tested using budgerigars (Melopsittacus
undulatus) as an avian model (Gallup et al.,
2009). Results showed that yawning frequency in
budgerigars increased during rising ambient
temperature, as opposed to when temperatures
were held constant. A more recent study
manipulated ambient temperature in both
directions and confirmed that yawning occurred
more often during high-increasing temperatures
compared with decreasing temperatures (Gallup et
al., in press). In addition, yawning was
positively correlated with ambient temperature
and occurred more often in tandem with other
thermoregulatory behaviors.
-
- The results of Campos and Fedigan (2009) are
in accord with these studies showing that
yawning occurred at higher ambient temperatures
and thus was more likely to have also occurred
alongside tongue out behavior. By investigating
the temporal relationship between yawning and
tongue protrusion, it would be possible to
provide a more convincing justification for
whether to couple or disentangle these two
behaviors. The reports of Campos and Fedigan
(2009) and Gallup et al. (2009) show that
yawning occurs at roughly the same average
temperatures (30-32°C) across both species.
One difference is that budgerigars do not rest
more during higher ambient temperatures, whereas
capuchins did. It should be noted, however, that
the assumption of a relationship between yawning
and resting in capuchins was not based on a
formal analysis but rather on the general
association between yawning and sleep. It is
because of this yawn/rest association that
yawning was overlooked as a thermoregulatory
behavior in capuchins. Campos and Fedigan (2009)
imply functionality to yawning when they
describe it as a byproduct of resting but a
specific role was not identified or discussed.
It is well documented in humans that yawning
occurs most often before sleep onset and after
waking (Provine et al., 1987). However, it is
important to realize that sleep and body
temperature vary inversely, and yawning
frequently occurs in the evening, when brain
temperature is at its peak, and upon waking,
when brain temperature begins increasing from
its lowest point (Landolt et al., 1995). It
would have been interesting to compare the rates
of yawning among capuchins during resting
periods of varying ambient temperatures.
-
- In combination with existing evidence
supporting a strong connection between yawning
and changes in internal and external
temperatures, it seems reasonable that both
yawning and tongue protrusion are methods of
behavioral thermoregulation in capuchins. Among
homeotherms, ecological factors such as the
relative need for water conservation could
affect the way yawning is used to alleviate
thermal stress, as has been suggested for
budgerigars (Gallup et al., 2009). For instance,
there could be differences in yawning between
homeothermic species selected to different
degrees for cooling abilities in challenging
thermal environments. Thus, yawning may not be
highly involved in behavioral thermoregulation
across all primates. Similar to budgerigars,
however, capuchins serve as an intriguing model
for studying yawning and thermoregulation
because they also live in hot, dry climates. It
would be interesting to know whether yawning
rates in capuchins vary as a function of
increasing, decreasing, or constant ambient
temperatures.
-
- In summary, comparative research from birds,
rats, and humans suggests that yawning reduces
brain and body temperature, is influenced by the
range and direction of ambient temperature
change, and is inhibited by methods of
behavioral cooling (Gallup, 2010). The data
presented by Campos and Fedigan (2009) are
consistent with the view that yawning may also
be a thermoregulatory behavior in white-faced
capuchins, yet more focused analyses are
required to reach an informed conclusion.
Although yawns are observed in all classes of
vertebrates (Baenninger, 1987), researchers are
only beginning to critically study this behavior
in a comparative nature, and due to the
potential multifunctionality of yawning, much
more research is needed. Recently, Vick and
Paunker (2009) have investigated the
physiological role of yawning in primate
behavior, providing thorough analysis of the
variation and context of yawning in chimpanzees
(Pan troglodytes). In addition, Palagi et al.
(2009) have studied the social nature of
yawning, providing support for a role of empathy
in yawning contagion among gelada baboons
(Theropithecus gelada). Hopefully, these efforts
will pave the way for future comparative studies
highlighting the importance of this
evolutionarily conserved behavior.
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