Respiratory Physiology & Neurobiology 154 (2006) 302–318
Respiratory cooling and thermoregulatory coupling in reptiles夽
Glenn J. Tattersall ∗ , Viviana Cadena, Matthew C. Skinner
Department of Biological Sciences, Brock University, St. Catharines, Ont., Canada L2S 3A1
Accepted 13 February 2006
Abstract
Comparative physiological research on reptilies has focused primarily on the understanding of mechanisms of the control of
breathing as they relate to respiratory gases or temperature itself. Comparatively less research has been done on the possible link
between breathing and thermoregulation. Reptiles possess remarkable thermoregulatory capabilities, making use of behavioural
and physiological mechanisms to regulate body temperature. The presence of thermal panting and gaping in numerous reptiles,
coupled with the existence of head–body temperature differences, suggests that head temperature may be the primary regulated
variable rather than body temperature. This review examines the preponderance of head and body temperature differences in
reptiles, the occurrence of breathing patterns that possess putative thermoregulatory roles, and the propensity for head and
brain temperature to be controlled by reptiles, particularly at higher temperatures. The available evidence suggests that these
thermoregulatory breathing patterns are indeed present, though primarily in arid-dwelling reptiles. More importantly, however,
it appears that the respiratory mechanisms that have the capacity to cool evolved initially in reptiles, perhaps as regulatory
mechanisms for preventing overheating of the brain. Examining the control of these breathing patterns and their efficacy at
regulating head or brain temperature may shed light on the evolution of thermoregulatory mechanisms in other vertebrates,
namely the endothermic mammals and birds.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Respiratory cooling; Panting; Gaping; Thermoregulation; Countercurrent exchange; Evaporative water loss
1. Introduction
夽 This paper is part of a special issue entitled “Frontiers in Comparative Physiology II: Respiratory Rhythm, Pattern and Responses to
Environmental Change”, guest edited by W.K. Milsom, F.L. Powell
and G.S. Mitchell.
∗ Corresponding author. Tel.: +1 905 688 5550x4815;
fax: +1 905 688 1855.
E-mail address: gtatters@brocku.ca (G.J. Tattersall).
1569-9048/$ – see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.resp.2006.02.011
The subject of reptilian thermoregulation has long
been of interest to comparative physiology. Reptiles, in general, possess a wide array of behavioural
mechanisms for modifying body temperature, including basking, shuttling, postural changes, and eyebulging (Bogert, 1959; Heath, 1970). They also possess numerous physiological mechanisms that appear
to serve as modulators rather than determinants of
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
body temperature, including heart rate and thermal hysteresis, peripheral circulatory adjustments, and even
modest thermogenesis (Seebacher and Franklin, 2005).
Less extensively explored from a physiological perspective is the issue of respiratory cooling in reptiles,
although considerable research has been done on the
total rates of evaporative water loss in reptiles.
Respiratory cooling ultimately manifests from the
evaporative water loss that occurs in the upper airways
and buccal cavity during breathing. This cooling can
result from: (1) a eupneic breathing pattern producing
constitutive cooling of nasal passages; (2) a shallow, but
rapid ventilatory pattern (e.g. panting) which should
induce more extensive cooling of the nasal passages;
(3) an open mouth gaping that increases the surface
area for evaporation and presumably cools the buccal cavity and/or entire upper airways. These latter
breathing patterns are prevalent throughout the reptiles
(Table 1), unfortunately, the control of breathing patterns and neural regulation of ventilation in the context
of body temperature control are poorly understood. A
considerable amount of research into the potential thermoregulatory function of panting and gaping occurred
in the 1970s, with little revisiting of these concepts,
except for a few recent studies (DeNardo et al., 2004;
Borrell et al., 2005; Tattersall and Gerlach, 2005).
In this review, we will outline: (1) the occurrence of
regional temperature differences in reptiles and the circumstantial evidence suggesting that respiratory cooling helps to regulate brain temperature; (2) the types
and prevalence of respiratory patterns that possess
known or probable thermoregulatory function in reptiles; (3) review the known anatomical arrangements
that may help lead to the regulation of brain tempera-
303
ture via respiratory mechanisms; (4) discuss the known
data on respiratory water loss in reptiles and how this
can translate into cooling of the airways and lead to
brain cooling. This review should shed light on whether
the regulated thermoregulatory variable in reptiles is
brain temperature rather than body core or peripheral
temperature. It would appear that in certain reptiles,
panting and gaping are effective cooling mechanisms
that help maintain non-lethal brain temperatures under
heat stress. Furthermore, it is our hope that this review
will stimulate research into the integration of reptilian
respiratory and thermoregulatory physiology.
2. Head–body temperature gradients in reptiles
Reptiles are well known for their thermoregulatory capabilities (Bogert, 1959; Heath, 1964b, 1970;
Templeton, 1971; Huey, 1974), exhibiting numerous
behavioural and physiological mechanisms for regulating relatively precise body temperature. The majority
of thermoregulatory studies, however, have measured
body or cloacal temperature, with less emphasis on
the regulation of head temperature. Measurements of
head or brain temperature have been made simultaneously with body temperatures, although few studies
have manipulated brain temperature in order to examine the role of central thermoreception in physiological or behavioural mechanisms of thermoregulation
(except for Cabanac et al., 1967; Hammel et al., 1967;
Templeton, 1971; Crawford and Barber, 1974). To date,
most reptiles have been demonstrated a temperature
differential between the head and body, particularly
during heating. Little emphasis, however, has been
Table 1
Presence and absence of gaping and panting in reptilian orders (and/or suborders)
Reptilian order/suborder
Prevalencea
Thermoregulatory functiona
References
Testudines
+
−
Moll and Legler (1971)
Squamata
Serpentes
Lacertilia
+
+++
−
+++
Jacobson and Whitford (1971)
Heatwole et al. (1973), Crawford and Kampe (1971),
Firth and Heatwole (1976), Crawford et al. (1977)
Crocodilia
Sphenodonta
++
?
++
?
Spotila et al. (1977)
a Plus sign refers to relative prevalence or strength of response, question sign refers to no known studies, minus sign means there is no known
likely thermoregulatory function.
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placed on examining and comparing head–body temperature differentials under altered thermal regimes,
such as radiant, convective or conductive heating, nor
have there been attempts to compare the nature of these
differentials during heating and cooling. Alligators, for
example, exhibit different rates of head heating versus
body heating, which is dependent on the degree of evaporative cooling from the mouth (Spotila et al., 1977).
Numerous lizards have been shown to have a lower
head temperature than core body temperature at high
ambient temperatures (Webb et al., 1972), although
head and brain temperatures are known to rise initially
more rapidly than body temperature under a constant
heat source (Heath, 1964a, 1966). The tendency is for
brain temperature to reach a critical value during heating, and thereafter show similar or lower values than
body temperature. Webb et al. (1972) found that during artificial heating of three Australian lizards, head
temperature was higher than or similar to body temperature; after panting was initiated, the head temperature
fell below that of the body.
A large literature on internal temperature gradients
comes from snakes (Johnson, 1973, 1975; Hammerson,
1977; Gregory, 1990). For example, in field caught
boas, the slope of the relationship between oral (estimate of head) and cloacal temperature was usually less
than one, indicating regional temperature differences
with cooler head temperatures (Dorcas and Peterson,
1997). At ambient temperatures below preferred body
temperatures, snakes had higher oral temperatures than
body temperatures; however, they possessed lower
oral temperatures when ambient temperatures climbed.
This suggests a combination of behavioural thermoregulation and physiological regulation to achieve regulation of head temperature (Dorcas and Peterson, 1997).
Field and laboratory work on the taipan has shown
that the maximum preferred head temperature was
39 ◦ C, whereas body temperature could reach as high
as 40.5 ◦ C under voluntary conditions (Johnson, 1975).
Similar results have been observed in some Australian
pythons, where intense heating led to faster warming
of the head temperature, after which internal respiratory cooling appeared to lead to a constant esophageal
temperature, in spite of a continually climbing body
temperature (Webb and Heatwole, 1971).
Certain turtles have shown similar capacities for
regional differences in body temperature. Under some
conditions, box turtles have the capacity to keep core
body temperature 10.5 ◦ C below ambient temperature,
through extensive evaporative water loss (Sturbaum
and Riedesel, 1974). In another study, in box turtles
housed at 40 ◦ C, preoptic (i.e. hypothalamic) temperature stabilised at 1–2 ◦ C below ambient temperature, even though cloacal temperature was less than
1 ◦ C different from ambient temperature (Morgareidge
and Hammel, 1975). Spontaneous rises in evaporative water loss (non-respiratory) at constant body temperature, were associated with decreases in preoptic
temperature (Morgareidge and Hammel, 1975), suggesting that in turtles, brain temperature is the primary
regulated variable linked to evaporative cooling. In
two Australian turtles, head temperature was observed
to increase more rapidly than cloacal temperature.
Upon tear formation at higher ambient temperatures,
however, head temperature would fall below that of
cloacal, sometimes by as much as 7 ◦ C (Webb and
Johnson, 1972), suggesting that evaporative water loss
was linked to head temperature regulation. Although
the mode of evaporation might differ among reptiles,
the effect appears to be the same: head and brain temperature can be kept from reaching high and lethal
levels.
The overall significance of respiratory evaporative
cooling and its potential for the regulation of head temperature can be easily observed by a comparison of
the external nasal surface temperature with the external temperature of the head. From our own observations
and from published observations (Tattersall et al., 2004;
Tattersall and Gerlach, 2005), we have observed that
external surface temperature of the nasal region is typically cooler than the head temperature, and more so at
higher temperatures. This simple pattern was observed
in a population of semi-wild tortoises (Geochelone
carbonaria; Fig. 1A; Tattersall and Abe unpublished
observations). In lizards, such as the bearded dragons
(Pogona vitticeps), we observed a slight external respiratory cooling in normoxia (Fig. 1B), with a much
more profound external cooling in hypoxia as lizards
engaged in more pronounced and longer bouts of thermal gaping behaviour, suggestive of a regulated decline
in the so-called body temperature set-point (Tattersall
and Gerlach, 2005). Finally, in rattlesnakes, the external cooling effect is most pronounced, with surface
nasal temperatures in resting animals up to 2 ◦ C lower
than head or body temperature (Fig. 1C). This response
is further accentuated under conditions of high activity
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
305
Fig. 1. External nose temperatures (obtained using infrared thermal imaging) are linearly correlated with head temperature, though at higher
temperatures, there is usually significant respiratory cooling. (A) Semi-wild tortoises (Geochelone carbonaria) exhibit cooler nose temperatures
at high head temperatures (closed circles, slope = 0.82, intercept = 2.94; personal observations, N = 16). (B) Bearded dragons (Pogona vitticeps)
exhibit a similar cooler nose at higher head temperatures. Hypoxia (7% O2 ; open circles, slope = 0.83, intercept = 2.79) leads to an increase in
gaping, leading to colder nose than observed in normoxia (filled circles, slope = 0.74, intercept = 7.48) (N = 14; data from Tattersall and Gerlach,
2005). (C) Rattlesnakes (Crotalus durrisius) exhibit a constitutive respiratory cooling that is augmented when metabolic rate is raised following
a meal (open circles, slope = 0.80, intercept = 2.73), compared to that observed with fasted snakes (filled circles, slope = 0.83, intercept = 2.77)
(N = 12; data from Tattersall et al., 2004). The dotted diagonal line in all three plots is the isothermal line.
(Fig. 2D) or during the post-prandial period when
metabolic rate, heat production and ventilation are all
highly elevated (Figs. 1C and 2C; Tattersall et al.,
2004). Interestingly, in all three species the slope of
the relationship between external nasal temperature and
head temperature was approximately 0.8, meaning that
the nose is typically cooler than the head, and to a
similar extent in the turtles, lizards and rattlesnakes.
Combined with an elevated intercept in all cases, this
suggests that respiratory cooling under normal breathing conditions (i.e. not panting or gaping) is prevalent at
all temperatures, but possibly only significant at higher
ambient temperatures where it would be expected that
respiratory cooing could exert its most physiologically
important role in cooling the brain. At these higher
ambient temperatures, it is still unclear whether respiratory cooling (without the aid of panting or gaping)
is a regulated mechanism or a mere consequence of
elevated ventilation due to a high metabolism. Nevertheless, the presence of a simple but effective countercurrent mechanism for heat exchange in the head
of reptiles (see section below on respiratory countercurrent mechanisms) seems to indicate that respiratory
cooling is, at least partially, a regulated process.
In general, there appears to be a capacity for separate or partially separate regulation of head temperature
from body temperature. The general consensus is that
brain temperature is more precisely regulated than body
temperature, through a combination of behavioural
and physiological processes (Heath, 1964a; Webb et
al., 1972; Johnson, 1973; Gregory, 1990; Dorcas and
Peterson, 1997). At low ambient temperatures, due to
behavioural thermoregulation and a lower thermal inertia of the head, brain temperature can often be seen to
be higher than body temperature, whereas at higher
ambient temperatures, respiratory cooling via panting
or higher total ventilation, may lead to a cooler brain
temperature than body temperature.
3. Thermoregulatory functions of respiratory
patterns
Reptiles, as all ectotherms, exhibit a positive correlation between body temperature and metabolism.
In general, the concomitant higher oxygen demands
imposed by this rise in metabolism are met through an
increase in overall ventilation (Crawford and Kampe,
1971; Frappell and Daniels, 1991). At temperatures
above the preferred range, many lizards (Table 1)
exhibit a drastic increase in breathing frequency in
addition to a decrease in tidal volume, in a pattern that
has been described as panting (Dawson and Templeton,
1966; Frappell and Daniels, 1991). This is accompanied by an open mouth and protruding tongue, which
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Fig. 2. Thermal images (upper 4 panels) of snakes under different conditions (Tattersall and Abe, unpublished observations). The lower 4
panels are outlines of the upper thermal images to provide reference images. (A) Front view of a rattlesnake (Crotalus durrisius) at the end of
a prolonged apnea showing barely perceptible head cooling; (B) front view of the same rattlesnake in (A) 4 s later, at the end of inspiration,
demonstrating the rapid respiratory cooing reaching the external surfaces (temperature scale is similar in A and B); (C) a different rattlesnake
exhibiting significant respiratory cooling under high level of activity (active tail rattling); (D) a python that had previously exhibiting gaping
behaviour, demonstrating whole head cooling from rapid respiratory rates leading to high rates of evaporative water loss (temperature scale is
the same in C and D). The diagonal lines in the outline represent corrugated cardboard paper.
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
enhances evaporative cooling through the respiratory
tract and the oral surfaces (Dawson and Bartholomew,
1958; Crawford, 1972; Heatwole et al., 1973). This
breathing pattern is comparable to that observed in
many panting birds and mammals and is of clear thermoregulatory value. The temperature at which the panting response is initiated has been denoted as the panting
threshold (Table 2).
In some other species of lizards, skinks for example, mouth gaping occurs at nearly lethal temperatures
and is directly preceded or accompanied by uncoordinated body movements and breathing spasms, and
concludes with the cessation of respiration (Veron and
Heatwole, 1970; Webb et al., 1972). In these species,
gaping takes place when death is already imminent and
seems to present no thermoregulatory relevance. Panting and gaping have also been observed in some snakes
(Jacobson and Whitford, 1971), and turtles (Moll and
Legler, 1971), though no role in thermoregulation has
ever been shown in these groups (Table 1).
Gaping can play an important thermoregulatory role
in some reptiles; open mouth breathing has been documented in crocodilians and has been demonstrated to
effectively reduce head temperature as well as heat gain
by the head (Spotila et al., 1977). This strategy allows
for longer basking periods, permitting the body temperature to climb to preferred levels while preventing
the head from overheating. It has also been demonstrated in several lizards that panting has a greater
cooling effect on the head than on the rest of the body
(Crawford et al., 1977). During heating, the chuckwalla
(Sauromalus obesus) was capable of maintaining body
temperatures 1 ◦ C and brain temperatures about 3 ◦ C
below ambient (45 ◦ C) for up to 8 h when allowed to
pant; this gradient was eliminated when the mouth of
307
the panting lizard was taped shut (Crawford, 1972).
In addition, head and body temperatures of the desert
iguana (Dipsosaurus dorsalis) were maintained 6 and
3 ◦ C lower than an ambient temperature of 50 ◦ C for
at least 25 min via evaporative water loss from panting (Dewitt, 1967). Nevertheless, the occurrence of
a head–body temperature differential may not necessarily demonstrate a tighter physiological control over
brain temperature. Instead, it has been argued that this
may reflect differences in the physical thermal characteristics of the head and the body, since the head warms
more quickly than the body (Pough and McFarland,
1976), due to size differences and thermal inertia. However, numerous studies have demonstrated rapid and
substantial changes in brain temperature with little
change in body temperature immediately after the commencement of panting and increased evaporative water
loss (Templeton, 1971; Crawford, 1972; Morgareidge
and Hammel, 1975; Crawford et al., 1977). This would
seem to cast doubt on circumstantial reasons being the
primary explanation for the production of brain temperatures lower than body temperatures.
Gaping and panting are sometimes accompanied
by gular movements. Gular pumping (high amplitude
movements) and gular fluttering (high frequency movements) have been described for varanids and geckos,
respectively and are thought to aid in evaporative cooling by increasing convective heat loss (Webb et al.,
1972; Heatwole et al., 1973). Owerkowicz et al. (1999)
demonstrated that savannah monitors (Varanus exanthematicus) employ gular pumping during locomotion to assist in ventilation. Similar results have been
obtained in varanid lizards where lung inflation can be
largely assisted by buccal pumping (Al-Ghamdi et al.,
2001).
Table 2
Situations that alter or change panting/gaping thresholds in reptiles
Situation
Response
Species
References
Dehydration
Hypoxia
Higher in dehydration
Lower in hypoxia
Circadian
Seasonal
Higher during the day than at night
Higher during the summer than during
the rest of the year
Lower in females than in males
Pogona barbata
Basiliscus vittatus, Iguana iguana,
Pogona sp.
Amphibolurus muricatus
Amphibolurus muricatus
Parmenter and Heatwole (1975)
Dupré et al. (1986), Tattersall and
Gerlach (2005)
Chong et al. (1973)
Heatwole et al. (1975)
Amphibolurus muricatus, Pogona sp.
Heatwole et al. (1973), Tattersall and
Gerlach (2005)
Sex
Threshold is defined as the lowest temperature at which panting or gaping occurs
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The panting response is controlled by both peripheral and central nervous mechanisms but the relative
importance of each of these mechanisms is still a matter
of debate. Although both play an important role in the
onset and inhibition of panting there seems to be considerable variation between reptile species. In the desert
iguana, D. dorsalis, the panting response is primarily
modulated by head temperature. It is necessary for the
cranial fluids and head skin to reach very high temperatures in order for panting to take place. Even at lethal
internal body and skin temperatures (with the exception
of cranial skin) panting will not occur unless the temperature of the head is also relatively high (Templeton,
1971). In S. obesus the panting response is controlled
by a very complex relationship between peripheral
and central nervous thermoreceptors; panting is not
activated unless the appropriate combination of skin,
body and brain temperatures takes place (Crawford and
Barber, 1974). They demonstrated that warming of the
brain, body or skin will all evoke panting, with continuous panting being exhibited under high heat loads.
More significantly, the threshold for inducing panting
in S. obesus was lowest in the brain, followed by the
body, and finally by the skin. This suggests that the most
sensitive thermoreceptors are located centrally, and the
least sensitive are located peripherally. This arrangement is similar to that observed in mammals (Simon
et al., 1986). These thermoreceptors act in a coordinated fashion, since a high brain temperature alone is
not enough to induce panting; body temperature also
has to be above 38 ◦ C before panting can be induced
by brain heating, suggestive of a central integration of
these thermal signals, most likely within the preoptic
region of the hypothalamus.
The role of the pineal complex (consisting of
the parietal and pineal organs) in lizard thermoregulation and in panting in particular has been well
established (Firth and Heatwole, 1976; Firth, 1979).
Removal of the parietal organ (a photoreceptor located
in the dorsal midline of the brain) from Amphibolorus
muricatus significantly reduced the panting threshold during spring and summer, whereas shielding of
the lateral eyes also lowered the panting threshold,
but to a lesser extent (Firth and Heatwole, 1976).
Eye shielded-parietalectomised lizards had even lower
panting thresholds than lizards that had undergone parietalectomy or eye shielding alone (Firth and Heatwole,
1976), suggesting an additive effect on the influence
of the parietal organ and the lateral eyes in the control of panting. In species that do not possess a parietal
organ, such as geckos, the influence of the lateral eyes
in the control of panting is enhanced. It is plausible that
photic information from the environment is transmitted
from these photosensitive organs to the thermoregulatory centers in the hypothalamus (Firth, 1979).
There is also evidence of diel and seasonal variation
in the panting threshold of lizards. The circadian fluctuations follow the environmental temperatures encountered throughout the day, the night values being significantly lower than diurnal ones and noon values being
slightly higher than those of the rest of the day (Chong
et al., 1973). The thermal preferences of lizards are also
of a circadian nature and follow a pattern similar to
that of the panting thresholds. This is evident in thermal gradient experiments where even under constant
light conditions the diurnal selected temperatures significantly exceed night selected temperatures (Cowgell
and Underwood, 1979; Firth et al., 1989). There is also
considerable seasonal variation in the panting thresholds of lizards; higher thresholds being exhibited in the
summer than in the rest of the year (Table 2). Heatwole
et al. (1975) showed that this circannual variation is primarily influenced by photoperiod and thermal acclimation. Animals acclimated to constant light will exhibit
progressively higher panting thresholds with increasing temperature of acclimation. In addition, lizards
acclimated to a 16-h light/8-h dark photoperiod display
significantly higher panting thresholds than those acclimated to 8-h light/16-h dark (Heatwole et al., 1975). As
a result, longer days and higher temperatures like those
present in the summer months lead to higher panting
thresholds, presumably as a result of a seasonal change
in preferred body temperature set-point or its equivalent.
The degree to which certain factors will affect different aspects of the behavioural thermoregulation of a
lizard depends on the environment in which the animal
lives and the adaptations with which it is equipped. The
level of dehydration experienced by a lizard, for example, can be an important source for panting threshold
variation in species from xeric environments but not so
in species living in habitats where water is an abundant
resource. The panting threshold of the desert dwelling
lizard (Pogona barbata), is progressively elevated with
increasing levels of dehydration, with a higher increase
in the panting threshold during the earlier stages of
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
dehydration than during the later ones (Parmenter and
Heatwole, 1975). This adaptation to hot, dry habitats
allows these lizards to conserve water when it is most
needed at the expense of thermoregulatory accuracy,
as well as to sacrifice water balance in a situation
where temperature regulation is imperative. In species
adapted to habitats where water is readily available,
such as A. muricatus, dehydration does not have a significant effect on the panting threshold (Parmenter and
Heatwole, 1975).
Environmental factors such as hypoxia can also alter
different aspects of behavioural thermoregulation. It
has been well established that animals reduce their preferred body temperature under low oxygen conditions
(Wood and Gonzales, 1996). This hypoxic thermoregulatory response serves as a protective mechanism for
vital organs by reducing oxygen requirements during
low availability and thus prolonging the survival of
the animal. Hicks and Wood (1985) tested the preferred temperatures of seven species of lizard in a thermal gradient under different levels of oxygen concentration. Lizards subjected to hypoxic conditions (7%
O2 ) exhibited significantly lower selected temperatures
compared to those tested under normoxic conditions.
Not surprisingly, the thermal threshold for evaporative
cooling through gaping or panting is also lowered with
decreasing concentrations of oxygen. When exposed
to 7% oxygen, basilisks and green iguanas significantly lower the body and skin temperature at which
panting is initiated (Dupré et al., 1986). Tattersall and
Gerlach (2005) tested the effect of hypoxia on the overall gaping time and the magnitude of the gape of the
bearded dragon, P. vitticeps and demonstrated that the
magnitude of the opening of this lizard’s mouth during gaping as well as the overall time employed in
such activity are also significantly affected by inspired
oxygen levels. Progressively heating the animals while
simultaneously exposing them to different oxygen concentrations causes the lizards to spend more time gaping during hypoxia than in normoxia. Tattersall and
Gerlach (2005) also described three types of gape for
the bearded dragon according to the extent of the opening of the lizard’s mouth: Type I, a very small gape;
Type II, a typical gape; Type III corresponded to a wide
open mouth with protruding tongue. When bearded
dragons were exposed to low oxygen concentrations
(10 and 6%) progressively lower temperatures elicited
Types II and III gaping responses when compared to
309
normoxic conditions. All of these respiratory responses
point to a graded and regulated decline in the so-called
body temperature set-point.
Sex is also an important factor when considering the
regulation of panting or gaping thresholds. Tattersall
and Gerlach (2005) showed that female bearded dragons consistently exhibited lower gaping thresholds than
males. This is consistent with the findings of Heatwole
et al. (1973) who found slightly higher, although not
significant, panting thresholds in male Jacky dragons
(A. muricatus) than in females and also consistent
with findings that sex can have subtle, albeit significant effects on behavioural thermoregulation in reptiles
(Lailvaux et al., 2003).
Apparent from the wide array of responses listed
above is that changes in the panting and gaping thresholds, although respiratory in nature, occur for a thermoregulatory purpose (see also Tables 1 and 2). Furthermore, although only briefly outlined here, the panting and gaping responses in reptiles appear to have both
proportional and threshold properties, suggestive of a
central neural integrator and regulator (Simon et al.,
1986; Bligh, 1998). For example, the amount of time a
lizard spends engaged in thermoregulatory panting as
well as the magnitude of the mouth gape increase with
increasing temperature (Tattersall and Gerlach, 2005).
Crawford and Barber (1974) also demonstrated that
the pattern of panting (intermittent versus continuous)
operated in a graded fashion, becoming continuous
whenever the thermal drive was high. Interestingly,
that thermal drive could be derived from brain, body,
or skin thermoreceptors. Combined, these two studies
both suggest the existence of a proportional control in
the nature of the panting and gaping responses. In other
words, the degree to which these respiratory responses
manifest is proportional to the magnitude of the deviation from the preferred or set-point temperature. This
is a hallmark feature of a thermoregulatory effector
response.
4. Cephalic blood flow and cardiovascular
control of head temperature
As discussed earlier, it has been repeatedly observed
that when reptiles are basking or exposed to a high heat
stress environment, a head–body temperature gradient
develops (Dorcas and Peterson, 1997). This head–body
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temperature gradient can be attributed to a combination
of physical differences, behavioural thermoregulation,
or physiological control (Dorcas and Peterson, 1997),
as outlined above. This section will focus on the cardiovascular mechanisms found within the cephalic region
that may aid in the regulation of brain temperature. It
should be pointed out, however, that it is currently not
clear how cephalic blood flow regulation is linked to
respiratory cooling.
Early work suggested that the reptilian brain exhibits
centrally thermosensitive neurons with a putative cardiovascular role (Rodbard et al., 1950), suggesting, at
the time, that ectotherms possess similar central regulatory mechanisms to endotherms. Subsequently, Heath
(1964a) observed that during basking in the horned
lizard (Phrynosoma coronalum), the head warmed
up faster than the body, resulting in a head–body
temperature gradient of approximately 2–4 ◦ C. This
was thought to be largely due to the larger surface
area to volume ratio (Heath, 1964a, 1966; Pough and
McFarland, 1976). Differential head and body heating rates and at least transiently, head–body temperature gradients, can be developed and maintained by a
countercurrent heat exchanger. Similar to countercurrent heat exchangers found in the extremities of many
marine animals, there is a cranial countercurrent heat
exchanger located in the head of reptiles (Heath, 1966).
In this unique reptilian exchange system, there is heat
exchange between the internal jugular vein and the
internal carotid artery controlled by the internal jugular
constrictor muscle (Fig. 3). During basking, the internal jugular carries warm blood away from the head, and
due to its close proximity to the internal carotid artery,
heat is transferred to the cooler carotid artery blood,
thus retaining heat in the head (Oelrich, 1956; Heath,
1964a, 1966). Interestingly, when the body temperature was increased to 30 ◦ C in P. coronalum, an eyebulging phenomenon repeatedly occurred, resulting in
the diminishing of the head–body temperature gradient.
This was followed by an increase in the heating rate of
Fig. 3. Cephalic blood supply in lizards that are involved in thermoregulation. Cranial venous supply in the lizard (Lacerta agilis) is shown
on the left, in (A) (from Bruner, 1907), with small black arrows indicating heat flow. Heath (1966) proposed (B, on right) that the jugularis
constrictor muscle contracts, increasing venous pressure and causing a build-up of blood in the cephalic venous sinuses (C.V.S.), eventually
forcing blood to drain the head through the lateral commisure (L.C.), the external jugular (E.J.) vein and the vertebral vein (V.V.). As a result, the
countercurrent exchange between the internal jugular (I.J.) vein and the internal carotid artery is by-passed, and brain heating can be diminished.
Small arrows indicate direction of heat exchange.
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
the body and a concurrent decrease in the rate of heating in the head (Heath, 1964a). Eye-bulging indicates
that there has been an alteration in circulatory blood
flow within the cephalic region (Fig. 3; Bruner, 1907;
Heath, 1964a; Crawford, 1972), and Heath (1964a)
suggested that the internal jugular constrictor muscle transiently flexes at higher head temperatures. The
result of this contraction is that blood now fills the
cephalic venous sinuses increasing the cephalic venous
pressure, manifesting externally as eye-bulging. The
increase in pressure initiates the opening of cephalic
shunts, where blood flows through the external jugular
vein and vertebral veins, by-passing the normal flow
through the internal jugular vein. Consequently, there
is no heat exchange between the internal jugular vein
and the internal carotid artery. The elimination of the
countercurrent heat exchange system allows for heat
transfer from the head to the body, causing an increase
in the body heating rate and a decrease in the heating
rate within the head; this diminishes the head–body
temperature gradient during the later phase of a basking
bout (Heath, 1964a, 1966). Dewitt (1967) also noticed
similar eye protrusion behaviour in D. dorsalis, and
when eye-bulging occurred there was also a decline in
the head–body temperature gradient (i.e. a trend toward
the head temperature becoming equal to or less than
body temperature), suggesting a similar cardiovascular mechanism to control the head–body temperature
gradient.
A physiological countercurrent heat exchanger system is advantageous in the cranium of reptiles in that
it allows for the brain to be quickly warmed up after
a cool period; when the optimal temperature has been
surpassed, however, the temperature sensitive brain can
be cooled or its heating rate slowed, by disabling the
countercurrent heat exchanger and dumping its heat to
the body (Heath, 1966). The topic of thermoregulatoryrelated countercurrent exchange mechanisms will be
addressed in the following section.
5. Respiratory countercurrent mechanisms
Many vertebrates have evolved physiological mechanisms to dissipate heat and cool the temperature sensitive brain during high heat stress. One mechanism
that tends to be consistent across mammalian, avian
and possibly reptilian species is the countercurrent
311
heat exchange system found within the respiratory
passages. Within the nasal passages of mammals and
birds there are complex structures called turbinates.
These turbinates can be described as one or more
pairs of coiled cartilage, covered with moist mucociliated epithelium (Hillenius, 1992, 1994; Geist, 2000;
Hillenius and Ruben, 2004). Unlike mammals and birds
that have relatively more complex turbinate structures,
most reptile species have relatively simple formations.
The formations are termed conchae consisting of only
a few coiled cartilaginous processes (Hillenius, 1992,
1994; Hillenius and Ruben, 2004). In D. dorsalis and
other species, the conchae contain a salt gland (Murrish
and Schmidt-Nielsen, 1970; Schmidt-Nielsen et al.,
1970; Schmidt-Nielsen, 1972). Crocodilians have a
more complex nasal passage than the rest of the reptilian orders, having three conchae in succession down
the nasal passages (Hillenius, 1992, 1994).
To understand how respiratory nasal passages could
be utilised to cool the brain it is first useful to grasp
how the nasal passages and turbinates function in
endotherms. The countercurrent heat exchangers found
in the nasal passages are analogous in function but
not in flow to vascular heat exchangers. In vascular
heat exchangers, blood flows in opposite directions and
heat transfer occurs between the parallel arteries and
veins. This process is referred to as spatial separation
due to the close proximity of the two vessels (Jackson
and Schmidt-Nielsen, 1964; Schmidt-Nielsen, 1972).
However, in the nasal passages there is only temporal
separation that can be simply described as air flow that
moves in and out within one functional tube (Jackson
and Schmidt-Nielsen, 1964; Schmidt-Nielsen, 1972).
During inspiration, the dry, cooler ambient air comes in
contact with the coiled nasal turbinates which heat and
saturate the incoming air. As the incoming air passes
over the mucosal surfaces heat is lost from the moist
surface and is gained by the air. This creates a cooler
mucosal surface which often falls below body temperature (Jackson and Schmidt-Nielsen, 1964). Consequently, due to evaporation, there is also water loss
from the nasal surface humidifying the passing air. Following inspiration, the incoming air is now at body
temperature and fully saturated within the lungs. Upon
expiration, the now warmed and humidified air in turn
warms the cool mucosal surface created during inspiration. As a result the warm air from the lung passes
over the cool mucosal surfaces which regain the heat
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G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
from the exhaled air that was lost during prior inspiration. Given that the air leaving the nasal passage is
below body temperature, water is conserved through
condensation on the mucosal surface, and thus the air
leaving the nasal passage is no longer fully saturated
(Hillenius, 1992).
Although the preceding described how the nasal passages and turbinates function in endotherms, it also
demonstrated how heat and water can be conserved.
When mammals, birds, and reptiles are exposed to high
temperatures that may result in the overheating of the
brain, however, respiratory mechanisms may instead
be utilised to dissipate heat rather than conserve it,
through the stimulation of panting, gaping, and/or altering cranial shunts, and thus by-passing respiratory and
cardiovascular countercurrent mechanisms.
Mammals, such as artiodactyls, utilise respiratory
cooling along with vascular heat exchange systems
to cool the brain. Taylor and Lyman (1972) demonstrated that gazelles were able to keep the brain 2.7 ◦ C
cooler than that of the body after body temperature
was raised by exercise. This was achieved by blood
vessels in the mucosa being cooled by evaporation in
the nasal passageways. The cooled venous blood then
passes through the carotid rete which consists of a series
of arterioles located inside the cranial cavity. This is
where the heat exchange occurs cooling the warm arterial blood that is being directed to the brain (Baker,
1979, 1982; Jessen, 1998, 2001; Mitchell et al., 2002).
Carotid retes are most prominent in artiodactyls and
felids and their cooling capacity on the brain is somewhat limited. Generally in artiodactyls, the degree to
which the brain can be cooled by this means is less than
1 ◦ C (Mitchell et al., 2002). Analogous to mammals,
birds also use a combination of vascular countercurrent heat exchange system. Similar to the mammalian
carotid rete, birds utilise an opthalmic rete to aid in
brain cooling (Baker, 1982; Mitchell et al., 2002). Like
the carotid rete, the opthalmic rete is a collection of
small arteries developed from the carotid artery and
is interwoven with the veins that drain the cool blood
form buccopharyngeal surfaces and the beak (Baker,
1982; Fuller et al., 2003). Blood from the buccopharyngeal mucosa and turbinates in the beak would be
cooled by evaporation during panting or gular fluttering (Zurovsky and Laburn, 1987).
Comparable to mammals and birds, but not as complex, reptiles also use a vascular countercurrent heat
exchange system in combination with respiratory passageways. Crawford (1972) recorded that when panting
is initiated in S. obesus, a brain temperature 2.7 ◦ C
below that of the body can be sustained during high
heat stress (discussed in Sections 2 and 3). In S. obesus, the carotid arteries are in close proximity to the
surface of the pharynx and are exposed to air movement when panting. During panting the carotid artery is
cooled, thus simultaneously cooling the blood directed
for the head. Webb et al. (1972) also noted that during
open mouth gaping and gular fluttering (300 min−1 )
in geckos, the orbital sinuses were clearly engorged
with blood, suggesting that heat can be removed from
the vascular system directly through evaporation from
the inner surfaces of the mouth near the blood sinuses.
Although there are no reports of reptiles with retia
found near the carotid artery, there is a shunt system
that occurs in the cranium (previously discussed). With
both the vascular countercurrent heat exchange system and respiratory mechanism working together, the
brain of some reptiles can be efficiently cooled during
high environmental temperatures. Through the combined efforts of the constriction of the internal jugular
constrictor muscle and panting, the brain may not only
lower its rate of heating when reptiles are basking, but
actually begin to cool at extreme temperatures. Due to
the fact that the head warms faster than the body (Pough
and McFarland, 1976), it is entirely plausible that a
countercurrent heat exchange mechanism has evolved
to regulate the temperature sensitive brain in reptiles
(Heath, 1964a), particularly in those that are exposed
to warm ambient temperatures and intense solar radiation that leads to high or lethal body temperatures.
6. Respiratory evaporative water loss
The literature comparing standardised respiratory
water losses in reptiles is not very extensive, with most
evaporative water loss estimates being based primarily on whole body assessments. In a few instances, it
has been possible to dissociate respiratory water loss
from total cutaneous water loss (see Table 3). To facilitate comparisons of water loss from the respiratory
tracts, the ratio of respiratory evaporative water loss
rate to metabolic rate (Respiratory Water Extraction
Coefficient = RWEC; mg H2 O/mL O2 ) can be used. It
gives an indication of the ability of the respiratory
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
313
Table 3
Respiratory water extraction coefficient (mg H2 O/mL O2 ) in two different species of mammals and 4 different species of lizards
Species
Tb (◦ C)
RWEC (mg H2 O/mL O2 )
References
Kangaroo rat (Diplodomys spectabilis)
Albino rat (Rattus norvegicus)
38a
38a
0.57
0.94
Schmidt-Nielsen and Schmidt-Nielsen (1950)
Schmidt-Nielsen and Schmidt-Nielsen (1950)
Pristidactylus torquatus
25
30
8.66b
9.43b
Labra and Rosenmann (1994)
Pristidactylus volcanensis
25
30
6.93b
7.56b
Labra and Rosenmann (1994)
Varanus sp.
25
38
0.26
0.93c
Thompson and Withers (1997)
Chuckwalla (Sauromalus obesus)
26
35
40
0.61
0.70
1.24
Crawford and Kampe (1971)
a
b
c
Estimated values based on approximate mammalian body temperature.
Values calculated from data reported in the study of Labra and Rosenmann (1994).
38 ◦ C value extrapolated from 25 ◦ C based on a Q10 of 2.6 observed between 20 and 25 ◦ C.
system to recover moisture derived from lung ventilation, while standardizing for the influence of metabolic
rate (Schmidt-Nielsen and Schmidt-Nielsen, 1950).
The value has been extensively measured in mammals,
with values ranging from 0.4 in desert mammals to 1.0
in other mammals, including humans. The RWEC can
be as low as 0.7–0.93 (Table 2) in some lizards, a value
that is higher than the values of 0.4 observed by kangaroo rats (Schmidt-Nielsen and Schmidt-Nielsen, 1950),
desert mammals that possess countercurrent exchange
mechanisms and elaborate respiratory turbinates. The
RWEC of 0.7–0.93, however, is not dissimilar from
non-desert mammals with turbinates. Other reptilian
values range from 0.8 up to 10 (Table 3), suggesting
a wide range of values in the few reptiles where this
has been measured. It is apparent from the few studies that exist, that although the RWEC varies greatly
in reptiles, some values are at par with the standard
mammalian values, particularly in desert dwelling reptiles. The reasons for the similar values between some
reptiles and some endotherms is unclear at present, particularly because the absence of respiratory turbinates
in reptiles is thought to result in relatively high rates of
respiratory evaporative water loss (Hillenius, 1992). It
is clear, however, from studies on mammals that possess respiratory turbinates, that cooling of respiratory
passages occurs, primarily for the purposes of recovering heat and moisture. Nevertheless, it is plausible
that a cool respiratory passage would also serve to cool
the brain if the appropriate circulatory arrangements
exist.
Except for Murrish and Schmidt-Nielsen (1970), it
has been tacitly assumed that since most ectotherms
have body temperatures close to ambient, they would
have little need for recovering heat or moisture in
the respiratory passages. However, it would be prudent to consider the role of respiratory cooling as
a possible moisture recovery mechanism, in addition
to any thermoregulatory role. Preliminary data (Tattersall and Andrade, unpublished observations) from
the South American rattlesnake, Crotalus durissus,
show that nasal air temperatures and head temperature
change dramatically during inspiration and expiration
in animals equilibrated under different thermal regimes
(Fig. 4). At lower temperatures of 26 ◦ C, head temperature is nearly identical to ambient temperature. At
higher ambient temperatures, the deviation between
head and ambient grows larger, being approximately
0.2–0.4 ◦ C lower at 30 ◦ C and over 1.5 ◦ C lower at an
ambient temperature of 34 ◦ C. These modest changes
occurred at relative humidities between 40 and 70%. At
10% relative humidity, the deviation between head and
ambient temperature can be as large as 2 ◦ C at a moderate ambient temperature of 30 ◦ C due to the greater
capacity for evaporation, similar to that observed by
Borrell et al. (2005). The dynamic response resulting in this deviation in head temperature is the act
of breathing. During inspiration, the nasal passage
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G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
cools to a value that can be up to 6 ◦ C lower than
ambient temperature, indicating significant evaporation within the airways and cooling of the respiratory
walls. The shallower, more distal temperatures also
fall, though only to a fraction of that of the deeper
airways. During non-ventilatory periods, the deep airways slowly and passively warm up toward ambient
temperature, whereas the shallow airways remain fairly
constant. The entire airway, however, tends to remain
cooler than ambient or head temperature throughout the non-ventilatory period. Continuous evaporation inside the airways is reduced once airflow has
stopped, particularly as the airway humidity would be
elevated due to evaporation that occurred during inspiration. Upon initiation of expiration in the subsequent
breath, both deep and shallow airways warm up toward
head temperature, which is slightly below ambient
temperature.
Fig. 4. Deep (solid black line) and shallow (dark grey line) nasal temperatures recorded in a rattlesnake (Crotalus durissius) at different ambient
temperatures (dotted line) (Tattersall and Andrade, unpublished observations). (A) Ta is approximately 26 ◦ C and relative humidity of 50%; (B)
Ta is approximately 30 ◦ C and relative humidity of 50%; (C) Ta is approximately 34 ◦ C and relative humidity of 50%; (D) Ta is approximately
30 ◦ C with a low relative humidity of <10%. In (A–C) the breathing trace recorded by impedance is shown, with inspiration upwards and
expiration downwards. Dotted vertical lines indicate the onset of inspiration. Note the larger gradient between head temperature (light grey line)
and Ta at higher breathing frequencies (which occur at higher Ta ) and at low relative humidity.
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
During the entire breathing period, airway temperature is always lower than head or ambient temperature,
suggesting either continual evaporation during periods
of respiratory silence, or thermal inertia and sustained
cooler temperatures due to the lack of air flow. The latter seems more likely, particularly given the subsequent
rapid increase in airway temperature during expiration.
Furthermore, there is a strong influence of depth in the
nares on ambient temperature changes, suggesting a
spatial thermal gradient as well as the temporal gradient. This gradient may be crucial to the conservation of
water in many reptiles. This methodological approach
warrants a more systematic approach in the future when
examining the water conservation strategies of reptiles, particularly given the preliminary nature of these
data. Although respiratory turbinates are absent in most
reptiles, it is possible that a slow and deep breathing
pattern can lead to the conditions necessary for significant water recovery during normal breathing, as well
as leading to some degree of brain temperature regulation coupled to respiratory cooling. Experiments that
simultaneously manipulate relative humidity and ambient temperature, as in Borrell et al. (2005) might be able
to discern whether changes in breathing patterns play
a specific role in thermoregulatory control of head or
body temperature.
On an evolutionary timescale, we would predict that
the greatest propensity for respiratory-induced cooling should occur in desert dwelling or xeric adapted
reptiles, particularly lizards, as seen from the fact that
panting and gaping appear to be most common in these
reptiles (Table 1) and are effective at regulating head
or body temperature (Templeton, 1971; Crawford and
Barber, 1974). Murrish and Schmidt-Nielsen (1970)
estimated that the desert iguana (Iguana iguana) recovers 31% of the respiratory water that would have been
lost if no respiratory cooling existed. It is obvious
that although evaporation occurs in the respiratory passages, not all moisture is lost to the atmosphere. Evaporation occurs primarily during inspiration and provides
for additional cooling of the airways, and can serve the
purpose of allowing for respiratory water to condense
during expiration, as it does in mammalian turbinates.
This is somewhat speculative, and thus the critical point
for future research would be to firmly establish the
link between respiratory cooling, respiratory pattern
changes, and the potential for regulation of brain temperature.
315
7. Concluding remarks
Many reptiles appear to possess rather exquisite regulation of brain temperature, particularly in the face
of high ambient temperatures. Although the best precision seems to be restricted to certain lizards, in
general, reptiles have acquired the necessary neurological pathways for sensing and regulating temperature in the body (Bogert, 1959; Crawford and Barber,
1974; Morgareidge and Hammel, 1975; Grigg et al.,
2004). Indeed, it may even be the case that behavioural
and physiological thermoregulation are aimed primarily at the maintenance or regulation of brain temperature rather than body temperature, as has been
widely assumed (Webb et al., 1972; Webb and Johnson,
1972; Hammerson, 1977; Gregory, 1990; Dorcas and
Peterson, 1997). From a sensory perspective, brain,
body and skin thermoreceptors can all activate panting
in certain reptiles, although brain temperature is the
most sensitive regulator, evoking panting at lower temperatures than body or skin thermoreceptors (Crawford
and Barber, 1974). This pattern of activation is quite
similar to how mammalian thermoreceptors respond to
changing temperature and effect heat loss mechanisms
(Richards, 1970). As Crawford and Barber (1974)
pointed out, it appears that reptiles possess the necessary regulatory mechanisms, but not necessarily the
capacity for robust regulation of core body temperature,
as seen in the endothermic vertebrates. Continuously
maintaining large temperature gradients between themselves and their environment is prohibitively expensive
from an osmoregulatory perspective, and thus respiratory cooling may only reasonably be expected to cool
the brain.
We speculate, therefore, that respiratory cooling can
be imparted to the brain through vascular mechanisms
or simply via conductive heat transfer. In some reptiles,
panting and gaping operates as an ambient temperaturedependent switch that is induced prior to high, lethal
temperature exposure, often in a graded and regulated
fashion. It has not escaped our notice that a profound respiratory cooling could be most pronounced
in slower breathing, larger tidal volume reptiles, like
snakes (Stinner, 1982; Andrade et al., 2004), since the
low air velocity will ensure adequate time for heat
exchange and phase changes of water to occur between
tissue and air. In addition, the long non-ventilatory periods will further support the capacity for cool airways
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G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
to play a role in cooling the brain. At present, the possible role for changes in the eupneic breathing pattern
(i.e. non-panting or gaping) that could produce greater
or lesser respiratory cooling leading to the maintenance
of head temperature would be speculative, but certainly
warrants future investigation.
Acknowledgements
We would like to acknowledge Denis Andrade and
August Abe for providing access to the rattlesnakes
and tortoises. We would like to extend our gratitude
to Dimitri Skandalis for critically proofreading the
manuscript, and significantly improving the final version. The authors’ research was funded by the Natural
Sciences and Engineering Research Council of Canada,
the Canadian Foundation for Innovation, and by a Premier’s Research Excellence Award to G.J.T.
References
Al-Ghamdi, M.S., Jones, J.F., Taylor, E.W., 2001. Evidence of a
functional role in lung inflation for the buccal pump in the
agamid lizard, Uromastyx aegyptius microlepis. J. Exp. Biol. 204,
521–531.
Andrade, D.V., Tattersall, G.J., Brito, S.P., Soncini, R., Branco, L.G.,
Glass, M.L., Abe, A.S., Milsom, W.K., 2004. The ventilatory
response to environmental hypercarbia in the South American
rattlesnake, Crotalus durissus. J. Comp. Physiol. B 174, 281–
291.
Baker, M.A., 1979. A brain-cooling system in mammals. Sci. Am.
240, 130–139.
Baker, M.A., 1982. Brain cooling in endotherms in heat and exercise.
Ann. Rev. Physiol. 44, 85–96.
Bligh, J., 1998. Mammalian homeothermy: an integrative thesis. J.
Therm. Biol. 23, 143–258.
Bogert, C.M., 1959. How reptiles regulate their body temperature.
Sci. Am. 200, 105–120.
Borrell, B.J., LaDuc, T.J., Dudley, R., 2005. Respiratory cooling in
rattlesnakes. Comp. Biochem. Physiol. A 140, 471–476.
Bruner, H.L., 1907. On the cephalic veins and sinuses of reptiles,
with description of a mechanism for raising the venous bloodpressure in the head. Am. J. Anat. 7, 1–117.
Cabanac, M., Hammel, T., Hardy, J.D., 1967. Tiliqua scincoides: temperature-sensitive units in lizard brain. Science 158,
1050–1051.
Chong, G., Heatwole, H., Firth, B.T., 1973. Panting thresholds of
lizards-II. Diel variation in panting threshold of Amphibolurus
muricatus. Comp. Biochem. Physiol. 46, 827–829.
Cowgell, J., Underwood, H., 1979. Behavioral thermoregulation in
lizards: a circadian rhythm. J. Exp. Zool. 210, 189–194.
Crawford, E.C., 1972. Brain and body temperatures in a panting
lizard. Science 177, 431–433.
Crawford, E.C., Barber, B.J., 1974. Effects of core, skin, and brain
temperature on panting in lizard Sauromalus obesus. Am. J. Physiol. 226, 569–573.
Crawford Jr., E.C., Kampe, G., 1971. Physiological responses of the
lizard Sauromalus obesus to changes in ambient temperature.
Am. J. Physiol. 220, 1256–1260.
Crawford, E.C., Palomeque, J., Barber, B.J., 1977. Physiological
basis for head–body temperature differences in a panting lizard.
Comp. Biochem. Physiol. A 56, 161–163.
Dawson, W.R., Bartholomew, G.A., 1958. Metabolic and cardiac
responses to temperature in the lizard Dipsosaurus dorsalis.
Physiol. Zool. 31, 100–111.
Dawson, W.R., Templeton, J.R., 1966. Physiological responses to
temperature in the alligator lizard Gerrhonotus multicarinatus.
Ecology 47, 759–765.
DeNardo, D.F., Zubal, T.E., Hoffman, T.C.M., 2004. Cloacal evaporative cooling: a previously undescribed means of increasing evaporative water loss at higher temperatures in a desert
ectotherm, the Gila monster Heloderma suspectum. J. Exp. Biol.
207, 945–953.
Dewitt, C.B., 1967. Precision of thermoregulation and its relation
to environmental factors in desert iguana Dipsosaurus dorsalis.
Physiol. Zool. 40, 49–66.
Dorcas, M.E., Peterson, C.R., 1997. Head–body temperature differences in free-ranging rubber boas. J. Herpetol. 31, 87–
93.
Dupré, R.K., Hicks, J.W., Wood, S.C., 1986. The effect of hypoxia
on evaporative cooling thresholds of lizards. J. Therm. Biol. 11,
223–227.
Firth, B.T., 1979. Panting thresholds of lizards - role of the eyes in
panting in a gecko, Oedura tryoni. Comp. Biochem. Physiol. A
64, 121–123.
Firth, B.T., Heatwole, H., 1976. Panting thresholds of lizards—role
of pineal complex in panting responses in an Agamid,
Amphibolurus muricatus. Gen. Comp. Endocrin. 29, 388–
401.
Firth, B.T., Turner, J.S., Ralph, C.L., 1989. Thermoregulatory behavior in 2 species of iguanid lizards (Crotaphytus collaris and
Sauromalus obesus) - Diel variation and the effect of pinealectomy. J. Comp. Physiol. B 159, 13–20.
Frappell, P.B., Daniels, C.B., 1991. Temperature effects on ventilation and metabolism in the lizard, Ctenophorus nuchalis. Resp.
Physiol. 86, 257–270.
Fuller, A., Kamerman, P.R., Maloney, S.K., Mitchell, G., Mitchell,
D., 2003. Variability in brain and arterial blood temperatures in
free-ranging ostriches in their natural habitat. J. Exp. Biol. 206,
1171–1181.
Geist, H.R., 2000. Nasal respiratory turbinate function in birds. Physiol. Biochem. Zool. 73, 581–589.
Gregory, P.T., 1990. Temperature differences between head and
body in garter snakes (Thamnophis) at a den in central British
Columbia. J. Herpetol. 24, 241–245.
Grigg, G.C., Beard, L.A., Augee, M.L., 2004. The evolution of
endothermy and its diversity in mammals and birds. Physiol.
Biochem. Zool. 77, 982–997.
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
Hammel, H.T., Caldwell, F.T., Abrams, R.M., 1967. Regulation
of body temperature in blue-tongued lizard. Science 156,
1260–1262.
Hammerson, G.A., 1977. Head–body temperature differences monitored by telemetry in snake Masticophis flagellum piceus. Comp.
Biochem. Physiol. A 57, 399–402.
Heath, J.E., 1964a. Head–body temperature differences in horned
lizards. Physiol. Zool. 37, 273–279.
Heath, J.E., 1964b. Reptilian thermoregulation: evaluation of field
studies. Science 146, 784–785.
Heath, J.E., 1966. Venous shunts in the cephalic sinuses of horned
lizards. Physiol. Zool. 39, 30–35.
Heath, J.E., 1970. Behavioural thermoregulation of body temperature
in poikilotherms. Physiologist 13, 399–410.
Heatwole, H., Firth, B.T., Stoddart, H., 1975. Influence of season,
photoperiod and thermal acclimation on panting threshold of
Amphibolurus muricatus. J. Exp. Zool. 191, 183–192.
Heatwole, H., Firth, B.T., Webb, G.J.W., 1973. Panting thresholds of
lizards-I. Some methodological and internal influences on panting threshold of an Agamid, Amphibolurus muricatus. Comp.
Biochem. Physiol. 46, 799–826.
Hicks, J.W., Wood, S.C., 1985. Temperature regulation in lizards:
effects of hypoxia. Am. J. Physiol. 248, R595–R600.
Hillenius, W.J., 1992. The evolution of nasal turbinates and mammalian endothermy. Paleobiology 18, 17–29.
Hillenius, W.J., 1994. Turbinates in therapsids—evidence for late
permian origins of mammalian endothermy. Evolution 48,
207–229.
Hillenius, W.J., Ruben, J.A., 2004. The evolution of endothermy
in terrestrial vertebrates: Who? when? why? Physiol. Biochem.
Zool. 77, 1019–1042.
Huey, R.B., 1974. Behavioural thermoregulation in lizards: importance of associated costs. Science 184, 1001–1003.
Jackson, D.C., Schmidt-Nielsen, K., 1964. Countercurrent heat
exchange in the respiratory passages. Proc. Natl. Acad. Sci. 51,
1192–1197.
Jacobson, E.R., Whitford, W.G., 1971. Physiological responses to
temperature in the patch-nosed snake, Salvadora hexalepis. Herpetologica 27, 289–295.
Jessen, C., 1998. Brain cooling: an economy mode of temperature
regulation in artiodactyls. News Physiol. Sci. 13, 281–286.
Jessen, C., 2001. Selective brain cooling in mammals and birds. Jpn.
J. Physiol. 51, 291–301.
Johnson, C.R., 1973. Thermoregulation in pythons II. Head–body
temperature differences and thermal preferenda in Australian
pythons. Comp. Biochem. Physiol. A 45, 1064–1087.
Johnson, C.R., 1975. Head–body thermal control, thermal preferenda, and voluntary maxima in Taipan, Oxyuranus scutellatus
(Serpentes: Elapidae). Zool. J. Linn. Soc. 56, 1–12.
Labra, M.A., Rosenmann, M., 1994. Energy metabolism and evaporative water loss of Pristidactylus lizards. Comp. Biochem.
Physiol. A 109, 369–376.
Lailvaux, S.P., Alexander, G.J., Whiting, M.J., 2003. Sex-based
differences and similarities in locomotor performance, thermal preferences, and escape behaviour in the lizard Platysaurus
intermedius wilhelmi. Physiol. Biochem. Zool. 76, 511–
521.
317
Mitchell, D., Malhoney, S.A., Jessen, C., Laburn, H.P., Kamerman,
P.R., Mitchell, G., Fuller, A., 2002. Adaptive heterothermy and
selective brain cooling in arid-zone mammals. Comp. Biochem.
Physiol. B 131, 571–585.
Moll, E.O., Legler, J.M., 1971. The life history of a neotropical slider
turtle Pseudemys scripta (Schoepff), in Panama. Bull. Los Angelos County Mus. Nat. Hist. 11, 1–102.
Morgareidge, K.R., Hammel, H.T., 1975. Evaporative water loss in
box turtles: effects of rostral brainstem and other temperatures.
Science 187, 366–368.
Murrish, D.E., Schmidt-Nielsen, K., 1970. Exhaled air temperature
and water conservation in lizards. Resp. Physiol. 10, 151–158.
Oelrich, T.M., 1956. The anatomy of the head of Ctenosaura pectinata (Iguanidae). Mus. Zool. Univ. Mich. Misc. Publ. 94, 1–122.
Owerkowicz, T., Farmer, C.G., Hicks, J.W., Brainerd, E.L., 1999.
Contribution of gular pumping to lung ventilation in monitor
lizards. Science 284, 1661–1663.
Parmenter, C.J., Heatwole, H., 1975. Panting thresholds of lizards. 4.
Effect of dehydration on panting threshold of Amphibolurus barbatus and Amphibolurus muricatus. J. Exp. Zool. 191, 327–332.
Pough, F.H., McFarland, W.N., 1976. Physical basis for head–body
temperature differences in reptiles. Comp. Biochem. Physiol. A
53, 301–303.
Richards, S.A., 1970. The biology and comparative physiology of
thermal panting. Biol. Rev. Camb. Philos. Soc. 45, 223–264.
Rodbard, S., Samson, F., Ferguson, D., 1950. Thermosensitivity of
the turtle brain as manifested by blood pressure changes. Am. J.
Physiol. 160, 402–408.
Schmidt-Nielsen, B., Schmidt-Nielsen, K., 1950. Pulmonary water
loss in desert rodents. Am. J. Physiol. 162, 31–36.
Schmidt-Nielsen, K., 1972. Recent advances in the comparative
physiology of desert animals. Symp. Zool. Soc. Lond. 31,
371–382.
Schmidt-Nielsen, K., Hainsworth, F.R., Murrish, D.E., 1970.
Counter-current heat exchange in the respiratory passages: effect
on water and heat balance. Respir. Physiol. 9, 263–276.
Seebacher, F., Franklin, C.E., 2005. Physiological mechanisms of
thermoregulation in reptiles: a review. J. Comp. Physiol. B 175,
533–541.
Simon, E., Pierau, F.K., Taylor, D.C., 1986. Central and peripheral
thermal control of effectors in homeothermic temperature regulation. Physiol. Rev. 66, 235–300.
Spotila, J.R., Terpin, K.M., Dodson, P., 1977. Mouth gaping as
an effective thermoregulatory device in alligators. Nature 265,
235–236.
Stinner, J.N., 1982. Ventilation, gas-exchange and blood gases in
the snake, Pituophis melanoleucus. Resp. Physiol. 47, 279–
298.
Sturbaum, B.A., Riedesel, M.L., 1974. Temperature regulation
responses of ornate box turtles, Terrapene ornata, to heat. Comp.
Biochem. Physiol. A 48, 527–538.
Tattersall, G.J., Gerlach, R.M., 2005. Hypoxia progressively lowers
thermal gaping thresholds in bearded dragons, Pogona vitticeps.
J. Exp. Biol. 208, 3321–3330.
Tattersall, G.J., Milsom, W.K., Abe, A.S., Brito, S.P., Andrade, D.V.,
2004. The thermogenesis of digestion in rattlesnakes. J. Exp.
Biol. 207, 579–585.
318
G.J. Tattersall et al. / Respiratory Physiology & Neurobiology 154 (2006) 302–318
Taylor, C.R., Lyman, C.P., 1972. Heat storage in running antelopes:
independence of brain and body temperatures. Am. J. Physiol.
222, 114–117.
Templeton, J.R., 1971. Periferal and central control of panting in
the desert iguana, Dipsosaurus dorsalis. J. Physiol. (Paris) 63,
439–442.
Thompson, G.G., Withers, P.C., 1997. Patterns of gas exchange
and extended non-ventilatory periods in small goannas (Squamata: Varanidae). Comp. Biochem. Physiol. A 118, 1411–
1417.
Veron, J., Heatwole, H., 1970. Temperature relations of the water
skink, Sphenomorphys quoyi. J. Herpetol. 4, 141–153.
Webb, G., Heatwole, H., 1971. Patterns of heat distribution within
bodies of some Australian pythons. Copeia, 209–220.
Webb, G.J.W., Firth, B.T., Johnson, C.R., 1972. Head–body temperature differences in lizards. Physiol. Zool. 45, 130–142.
Webb, G.J.W., Johnson, C.R., 1972. Head–body temperature differences in turtles. Comp. Biochem. Physiol. A 43, 593–611.
Wood, S.C., Gonzales, R., 1996. Hypothermia in hypoxic animals:
Mechanisms, mediators, and functional significance. Comp.
Biochem. Physiol. B 113, 37–43.
Zurovsky, Y., Laburn, H.P., 1987. The effects of ligation of the
oesophagus on body and brain temperature in pigeons. Comp.
Biochem. Physiol. A 87, 959–962.