Hypoxia progressively lowers thermal gaping thresholds in bearded dragons, Pogona vitticeps
Department of Biological Sciences, Brock University, St Catharines, Ontario, L2S 3A1, Canada
* Author for correspondence (e-mail: gtatters{at}brocku.ca)
Accepted 30 June 2005
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Summary |
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Key words: body temperature, evaporative heat loss, hypoxia, panting, reptile, set-point, sex differences, thermoregulation
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Introduction |
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Numerous physical factors have been shown to alter the temperature at which
lizards gape or pant. Panting thresholds have been shown to be altered by
dehydration (Parmenter and Heatwole,
1975), circadian rhythms (Chong
et al., 1973
) and the rate or source of heating
(Heatwole et al., 1973
). The
direction of these changes reflects the constraints of other physiological
processes on thermoregulation; to conserve water, lizards do not gape until
higher temperatures, and, since daily metabolic demand decreases at night in
many reptiles (Rismiller and Heldmaier,
1987
), a concomitant decline in the threshold for gaping occurs as
the thermoregulatory set-point (Tset) is reduced along
with the reduced metabolic requirements
(Rismiller and Heldmaier,
1982
).
It is well established that low oxygen causes many animals, including
reptiles, to lower Tb
(Wood and Gonzales, 1996).
Changes in preferred temperatures are often taken as proof of a change in
temperature set-point in the brain, since preferred temperature selection is a
behavioural and thus, ultimately, a neurophysiological phenomenon. Numerous
lizards (e.g. genera Iguana, Dipsosaurus and Anolis) select
temperatures in hypoxia approximately 10°C lower than normoxic preferred
temperatures (Hicks and Wood,
1985
; Petersen et al.,
2003
). If the Tset is decreased in hypoxia,
then the thresholds for any autonomic or behavioural response that results in
a decline or an attempt to decrease Tb should be
decreased. Since many lizards exhibit panting or gaping responses as ambient
temperature rises (Crawford and Barber,
1974
; Crawford and Gatz,
1974
; Crawford et al.,
1977
; Heatwole et al.,
1973
; Pough and McFarland,
1976
), this is taken to imply that reptiles exhibit some degree of
control of Tb, albeit manifesting as a behavioural
response.
With respect to behavioural thresholds for thermoregulation, Dupré
et al. (1986) showed that the
evaporative cooling threshold is diminished in hypoxic lizards; however, no
attempt to assess the magnitude or persistence of the gaping response was
made. Lizards that gape or pant may do so intermittently. It would be fruitful
to assess the entire gaping response across a wide range of temperatures in
order to determine whether the response is sustained, is proportional to
temperature and the severity of hypoxia and is dramatic enough to have an
effect on Tb regulation.
Studying the control of Tb in lizards under hypoxic conditions allows for the exploration of the existence of thermal threshold responses and thus makes inferences regarding the presence of thermoregulatory set-points. The objectives of this study, however, were to examine whether the gaping behaviour was proportionately related to ambient temperature and whether the threshold temperature at which gaping occurred was proportionately lowered in hypoxia. Understanding these two questions will shed light on the mechanism of thermoregulation in reptiles and other vertebrates and will provide evidence for whether hypoxia elicits a reduction in a hitherto seldom-studied behavioural response in reptiles. For the purpose of this study, we examined the gaping response (i.e. simple mouth opening) rather than panting (i.e. an altered breathing pattern). It is plausible that bearded dragons actually adopt panting, where the breathing frequency rises and tidal volume declines; however, assessing tidal volume accurately is difficult to do in lizards that open their mouths. Since simply opening the mouth may achieve a similar result of eliciting evaporative water loss across the mucosa within the mouth and throat, it is not necessarily required that panting accompanies gaping behaviour.
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Materials and methods |
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Experimental set-up
Throughout experimentation, an individual lizard was housed in a
24x24x40 cm clear acrylic box, which was blacked out on three
sides to prevent distractions and to minimise reflections. Once inside the
box, the lizard sat elevated 3.5 cm from the bottom on a perforated, clear,
acrylic platform, which allowed gas to be pumped into the box from a tube
below the platform and helped to collect urine and faeces. The box was located
within an environmental chamber (Thermo Forma; Marietta, OH, USA) to enable
changing temperatures between 30 and 40°C. A non-radiant heat source was
chosen in order to simplify the exposure regime. Since lizards reacted to
human presence, a small surveillance camera was affixed to the environmental
chamber inside wall and aimed towards the acrylic box to allow for observation
of the undisturbed lizard's behaviour on a video monitor outside the chamber.
An infrared (IR) thermal imaging camera (Mikron 7515; Oakland, NJ, USA) was
positioned on top of the box, looking down onto the lizard, to obtain body
surface temperature data. The IR imager was hooked up to a computer outside
the chamber to obtain computerised images. In order to allow for varying
oxygen levels inside the box, the IR camera rested on a set of `bellows',
sealed to the box with weather stripping, making the box relatively air-tight.
A small tube was inserted beneath the bellows into the box to allow for gas
sampling during hypoxic conditions to verify oxygen levels of 21, 10 and
6%.
Data collection
The animals were placed in the chamber to start experimentation in the
morning, preferably before feeding. Since it has been shown that lizards have
different gaping thresholds between night and day
(Chong et al., 1973), we
elected to perform the gaping measurements during the same time of the day,
between 10.00 h and 16.00 h. Lizards were given time to acclimate to the new
temperature, as well as for the box to reach hypoxic levels if necessary. This
usually required 2030 min.
Assessing gaping behaviour
The lizard was observed for 15 min at each temperature of interest (30, 32,
34, 36, 38, 40°C), and the time spent gaping was recorded together with
the degree or type of opening of the lizard's mouth
(Fig. 1). Type I represented a
barely open mouth, Type II was a typical gape and Type III was a wide open
mouth, usually accompanied by a head-back posture, with the tongue partially
protruding and a puffing out of the throat. The observation periods were
started once the lizard's dorsal surface temperature was within 0.5°C of
the ambient temperature of interest. The only exceptions were the observation
periods at 40°C (in normoxia and 10% oxygen) and 38°C (at 6% oxygen),
when the animal was observed before it had reached ambient temperature. This
was due to the long time required for the animal to reach the highest
temperatures. The animals were observed sooner in order to prevent heat
damage, since at this temperature all animals were already gaping
maximally.
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Assessing animal surface temperatures
The camera software, MikroSpec RT Version 2.1394 (Oakland, NJ, USA), was
set to capture an image of the thermal data every minute, up to a maximum of
500 frames. Image capturing was started upon the beginning of heating to
32°C (or 30°C at 6% oxygen). Images from the time during the 15 min
observation period were analyzed, and the lizard surface temperatures recorded
every minute. The mean temperature of a circular region of interest was
recorded from the lizard's back, head (between the eyes), tip of the nose,
tongue tip (if visible when gaping) and eye.
Experimental design and test conditions
The animals were each tested under normoxic and two hypoxic conditions (10
and 6% O2), which was accomplished by mixing air with nitrogen to
achieve the desired oxygen level. In all cases, gases entered the box at 5 l
min1. Since no previous data were known on the effects of
hypoxia in P. vitticeps, initial observations were made of the
animals at oxygen levels between 5 and 10%. An oxygen level of 6% was chosen
as appropriate for this experiment, since this placed a significant enough
stress on the animal while not seriously risking damage to the animal after
the 6 h ofexposure required (i.e. lizards appeared distressed at levels below
6% O2 whereas at 6% O2 or above they remained calm
throughout the procedures). Throughout the trials, the oxygen level was kept
to within ±0.2% of the desired level. One animal was tested per day at
each oxygen level. Two to three weeks passed before the performance of another
experiment on the same individual at a new level of oxygen. At each level of
oxygen, lizards were tested at 45 different ambient temperatures
between 30 and 40°C (32, 34, 36, 38 and 40 for 21 and 10% O2
and 30, 32, 34, 36 and 38°C for 6% O2). Lizards were exposed to
these temperatures in a step-wise fashion, with the 2°C increments lasting
either 1 h each or as long as it took to achieve skin surface temperature
equilibration with ambient temperature. It usually took approximately 1 h for
the lizard's body surface temperature to come into equilibrium with the
environment. The highest temperature (40°C) was not used in the 6%
O2 group out of concern for the lizard's survival. Previous studies
have shown that lizards held at high temperatures under hypoxic conditions
will die (Hicks and Wood,
1985).
Data analysis
All values reported are means ±
S.E.M., unless otherwise stated. The
percentage time spent gaping at the different ambient temperatures was
initially analysed to determine a temperature at which 50% of the animal's
time was spent gaping. This was done by fitting individual Hill equations to
each animal using:
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Data (either time spent gaping or surface temperatures) were analysed using repeated-measures two-way ANOVA, with oxygen and ambient temperature as the two treatments. On occasions where normality was not met, log transformations were performed and the test repeated. In all cases, residuals from the individual ANOVAs were examined to verify a normal distribution. If residuals were non-normal, a non-parametric repeated-measures ANOVA of ranks was performed. We were able to examine the effects of gender once we had calculated the ET50s and N. On that occasion, we used two-way repeated-measures ANOVA to test for significant ET50 and N, with oxygen level and sex as treatments. In cases where ANOVAs yielded significant effects, post-hoc multiple comparisons were performed using the Holm-Sidak method. All statistics were considered significant at P<0.05.
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Results |
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Gaping times in normoxia and hypoxia
Overall gaping time was significantly affected by inspired oxygen level
(P<0.001) and by temperature (P<0.001;
Fig. 3). In all cases, the
total gaping time increased sigmoidally at the higher ambient temperatures;
however, there was no significant interaction between oxygen and temperature
(P=0.112). The mean ET50 values for 21%, 10% and
6% O2 were 36.9±0.2°C, 35.5±0.4°C, and
34.3±0.4°C, respectively (Table
1), and the effect of hypoxia (10 and 6% O2) was found
to be significantly lower than normoxia. There was also a significant trend
for the Hill constant, N, to be higher in hypoxia, although this
effect was only significant at 6% O2 (P=0.05). N
was 69.8±11.0 at 21% O2, 78.4±10.8 at 10%
O2 and 113.4±15.6 at 6% O2
(Table 1). The appropriateness
of ET50 as an overall estimate of the threshold
temperature is demonstrated by the good fit (r2=0.873,
P<0.001) of the regression of ET50
versus the total time spent gaping between 30 and 38°C (i.e. the
experimental duration).
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Effect of sex on thermal preferences and ET50
Using a two-way repeated-measures ANOVA to test ET50
with oxygen and sex as the treatments, there was no significant interaction
(P=0.49), although sex and oxygen level each had a significant effect
(P=0.046 and P<0.001, respectively). Male lizards
exhibited significantly higher ET50 values than females at
all levels of oxygen tested (Table
1). Interestingly, this sex difference was also borne out in the
mean preferred temperatures of lizards in their home cages during the 3-month
period of experimentation; just as in the ET50 estimates,
there was a significant effect of sex on home cage preferred temperature
(P=0.02). Males exhibited a slightly, though significantly, higher
Tb of 35.2±0.17 versus
34.2±0.34°C in females.
Gaping type in normoxia and hypoxia
There was a significant effect of temperature on the percentage time spent
in Type I gaping (P=0.03), but no significant effect of oxygen
(P=0.31) nor a significant interaction effect (P=0.18). At
all three levels of oxygen tested, the percentage time spent in Type I gaping
gradually increased with increasing temperature before falling back down to 0%
at the highest temperatures (Fig.
4).
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Type II gaping was significantly affected by inspired oxygen (P=0.02) and ambient temperature (P<0.001). Furthermore, there was a significant interaction between oxygen and temperature (P<0.001). Type II gaping predominated at lower temperatures at 6% O2. At all three levels of oxygen, Type II gaping initially increased with higher temperatures before decreasing at the highest temperatures (Fig. 4).
There was a significant effect of oxygen and temperature on the percentage time spent in Type III gaping (P<0.001 for oxygen and P<0.001 for temperature) and a significant interaction between oxygen and temperature (P<0.001). Qualitatively, Type III gaping was initiated earlier (i.e. at lower temperatures) in hypoxia than in normoxia (Fig. 4). Indeed, at temperatures above 36°C, significantly more time (>50%) was spent engaged in Type III gaping at 6% O2 than at 21% O2.
Effect of body mass on gaping times
There was no significant effect of body mass on the
ET50 estimates at 21, 10 or 6% O2, despite the
large range of body masses examined (P=0.18, 0.29 and 0.45 and
r2=0.14, 0.09 and 0.05, respectively, determined through
linear regressions). Furthermore, body mass had no significant effect on
N estimates for 21 and 10% O2 (P=0.26 and 0.76
and r2=0.10 and 0.008, respectively); however, N
estimates were significantly and negatively correlated with body mass in the
lizards at 6% O2 (P=0.0005 and
r2=0.66), demonstrating that small lizards exhibited a
more rapid transition to continuous gaping as temperature increased.
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The only meaningful significant effects were on the tongue temperature. To simplify comparisons and account for some inter-individual responses, we also examined the body surfacetongue surface temperature difference. Oxygen level and ambient temperature had significant effects (P=0.011 and P<0.001, respectively) on the body surfacetongue surface temperatures, although there was not a significant interaction between oxygen and ambient temperature (P=0.92; Fig. 6). Overall, the bodytongue difference was greater at 6% O2 than at 21% O2, an effect that was most apparent at the lower ambient temperatures.
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Discussion |
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During heating, the periphery would be the first to warm up and, considering the fact that ET50s are always higher than preferred Tb values in normoxia (Fig. 7C,D), this suggests that the majority of gaping occurs at or above the normal Tset, acting as an important contributor to Tb regulation when ambient temperatures exceed Tset. The fact that, in normoxia, a regression of normoxic ET10 versus mean Tb in home cage yielded a significant regression suggests that the gaping thresholds determined here are meaningful values with respect to the individual lizard's normal preferred temperatures and that gaping is not simply a randomly displayed behavioural response.
One final concern was that at the highest temperatures of 3840°C, lizard surfaces did not come fully into equilibrium with ambient temperature within the experimental time period. This suggests the efficacy with which bearded dragons can defend a lower Tb through increased evaporative cooling, since at 40°C lizards spent 100% of their time gaping. Thus, although the surface temperatures (and thus also Tb) were not in true equilibrium with ambient temperature, this would not have affected the ET50 estimates, since the maximum gaping efforts were already reached (i.e. values greater than 100% would not have been possible and thus the Hill equations would not have been affected).
Hypoxia reduces ET50 through a proportional regulator
The main hypothesis tested in this study, that hypoxia would lower the
gaping threshold in a proportional fashion, was supported by the data. The
central hypothalamic thermostat is thought to operate as a proportional
controller (Mrosovsky, 1990).
In other words, the further the regulated variable deviates from a set-point,
the larger will be the corrective response. In this case, as lizards are
warmed up, they gape for progressively longer periods of time. This regulator
responds, as well, to magnitude; lizards in hypoxia had a greater tendency to
exhibit the more pronounced Type II and Type III gaping at lower ambient
temperatures than in normoxia (Fig.
4).
One interesting result from this study is that the three levels of
O2 yielded a proportionate reduction in the gaping threshold.
Previous work examining the preferred Tb of hypoxic
lizards seemed to indicate that a critical level of hypoxia lower than 10%
O2 was required before a proportionate drop in
Tb would occur (Hicks
and Wood, 1985). There are no data on the preferred temperatures
of P. vitticeps in hypoxia; however, it is possible that the gaping
threshold responds slightly differently to low oxygen than set-point driven
behaviour that requires activity or movement (i.e. preferred temperature).
Strict or `precise' thermoregulatory behaviour has been thought only to occur
in reptiles when inhabiting `low-cost' environments with low risk of predation
(Huey and Slatkin, 1976). If the costs for thermoregulating (e.g. locomotory
costs or risk of predation) are too high, then precise thermoregulation will
not occur. In this context, gaping or panting can be viewed as a low-cost
strategy for thermoregulation, inasmuch as its instantaneous costs are low.
Thus, it might be expected that the threshold for gaping could more easily be
sensitive and responsive to factors that alter set-point than a locomotory
means of regulating Tb could.
Regional differences in surface temperatures
During the present experiments, lizards were gradually warmed up from a
temperature of 30°C (their surface temperature in the early morning at the
beginning of experiments) to a final temperature of 38 or 40°C (depending
on O2 level; see Materials and methods). The overall heating times
between temperatures of 3038°C were progressively longer in the
hypoxic trials. This was probably due to their propensity to gape and exhibit
cloacal discharge at lower thresholds, and hence the augmented evaporative
cooling allowed for greater attempts to defend a lower core
Tb at the higher ambient temperatures. Whether other
thermoeffectors operate in a similar fashion remains to be shown. Despite the
slightly different heating times, most surface temperatures were not affected
by hypoxia, except for the tongue surface temperatures, where the changes that
occurred strongly suggest that some internal temperatures (i.e. brain) may be
differentially controlled in hypoxia.
Previously, Pough and McFarland
(1976) showed that brain
temperatures of lizards housed at temperatures greater than 40°C exhibit a
substantial difference from the body, a response that was not observed in dead
lizards held at similar temperatures. In extreme cases, lizard brain
temperature can be up to 6°C lower than Tb
(Crawford and Barber, 1974
;
Warburg, 1965
). It is tempting
to ascribe a physiological role (i.e. preferential blood flow that favours
brain cooling at high ambient temperature) for this response, although one has
yet to be shown. Since we were only examining surface temperatures, we cannot
comment on brain temperature or its regulation. Previous work by Webb et al.
(1972
) showed significant
bodyhead temperature differences in a wide variety of lizards. We did
not see very large differences in the present study, although this could be
because surface temperatures are not as informative as internal temperatures.
Interestingly, a dragon lizard in the Webb et al.
(1972
) study exhibited panting
at high temperatures (usually greater than 40°C), compared with P.
vitticeps in the present study. This could have been related to the
rapidly induced thermal changes, which is quite opposite to the present study.
Our study was looking at steady-state changes, where lizards had time to
equilibrate with their environmental temperatures, and, as such, we notice
lizards gaping at much lower temperatures.
We used bodytongue temperature differences to estimate the degree of
evaporative cooling. The difference between body surface temperature and
tongue temperature increases at higher ambient temperatures, suggesting a
greater degree of evaporative cooling at higher temperatures. It is also
apparent that the continuous gaping that occurred in hypoxia, combined with a
presumably higher ventilatory rate (i.e. an hypoxic ventilatory response), led
to a higher degree of evaporative cooling in the hypoxic lizards across all
the test temperatures. This is not surprising given that preservation of brain
function would be more critically challenged under hypoxic conditions. Small
changes in brain temperatures have been shown to produce large changes in
brain damage in either hypothermic or febrile animals
(Herrmann et al., 2003;
Kataoka and Yanase, 1998
;
Katz et al., 2004
;
Trescher et al., 1997
); higher
temperatures exacerbate excitotoxic damage, and lower temperatures lead to
less damage.
Qualitative aspects of the gaping response
It is possible that using a non-radiant means for changing
Tb is not the most appropriate for lizards that tend to
bask in the sun. Indeed, Heatwole (1973) showed that thresholds for gaping
were less variable in radiantly heated individuals than in non-radiantly
heated individuals, even though gaping thresholds were not affected by the
source of heat. Variability, however, did not appear to be a problem in our
study due to the paired, repeated nature of the experimental design and the
fact that we assessed percentage time spent gaping to estimate the
ET50 threshold (Fig.
2). Previous studies have used the first attempt at gaping as the
gaping threshold (Chong et al.,
1973; Dupré et al.,
1986
; Heatwole et al.,
1973
; Parmenter and Heatwole,
1975
). It is possible that assessing a simple value such as the
initial gape has much more variability inherent in the estimate, particularly
if the response is truly sigmoidal, as we have demonstrated. At the lower
temperatures, lizards spend so little time gaping that there is little effect
of increasing temperature on the time spent gaping. Furthermore, the magnitude
of gaping is much less at lower temperatures
(Fig. 4), begging the question
of how much evaporative cooling occurs when lizards are using Type I gaping.
Using an estimate such as the ET50 incorporates the entire
response over a range of temperatures and allows for an objective estimate of
the animal's overall gaping response to increasing temperature.
There was, however, a significant negative correlation between N and body size at 6% O2, suggesting that the smaller lizards exhibited a more typically onoff approach (i.e. a steep sigmoidal relationship between gaping time and ambient temperature) to gaping in severe hypoxia rather than a graded transition into increasingly more time spent gaping. This might reflect the fact that, as the smaller-sized lizards were undergoing more rapid changes in Tb, they responded with a more dramatic increase in time spent gaping as their Tb was raised above Tset and evaporative cooling mechanisms were required.
Effect of sex on gaping threshold
Few attempts have been made to examine the role of sex on normal
thermoregulatory behaviours in reptiles outside of the breeding season (see
Lailvaux et al., 2003). Even
with pregnancy, there are inconsistent results regarding whether males and
females exhibit consistently different preferred Tb. In
one previous study, females had higher mean 24 h Tb than
did males (Sievert and Hutchison,
1989
), although the reverse or lack of difference occurs just as
often, with field data often contradicting laboratory thermal gradient
experiments (Lailvaux et al.,
2003
). Interestingly, we have shown that sex had a significant
effect on the gaping threshold (Table
1).Females consistently initiated gaping at a lower temperature
than males, even during hypoxia. Previously, Heatwole et al.
(1973
) had shown that female
Jacky dragons had a tendency toward lower (although not significant) gaping
thresholds, a result consistent with the present study.
To the best of our knowledge, this is the first example of a sex difference
related to a physiological response to hypoxia in a reptile. If a lowered
set-point in hypoxia is truly adaptive, then it could be argued that all
lizards, regardless of sex, should lower Tb and gaping
threshold to an equal extent or as far as possible. The fact that the
difference between males and females is retained in hypoxia suggests that sex
differences in Tb regulation are of overriding importance.
A corollary of the above is that females will presumably have greater
tolerance to hypoxia if their lower gaping thresholds also translate into a
lower overall Tb regulation. Wood and Stabenau
(1998) showed that female rats
exhibit a lower Tb in hypoxia, which helped translate into
a greater tolerance to hypoxia. Survival times in hypoxic female rats were
also significantly longer than in male rats. Whether the same sensitivities
occur in reptiles is unknown.
Concluding remarks
It is apparent from the present study that bearded dragons make use of a
subtle behavioural response to effect changes in Tb. As an
ectotherm, they may not be able to artificially augment (for exceptions, see
Tattersall et al., 2004) or
decrease their overall Tb that far from ambient
temperature; however, they can use behavioural responses to serve as brakes on
thermal changes. The fact that gaping is proportionately controlled in both
duration and magnitude with respect to both ambient temperature and oxygen
strongly supports the importance of precise thermoregulatory control in as
much as other physiological and behavioural constraints will allow. It remains
to be shown exactly how effective gaping is at controlling
Tb for prolonged periods, how often this behaviour occurs
in the wild and whether it is routinely used in response to other stressors in
addition to hypoxia. Further information on the altered gaping or panting
thresholds in those species of lizards that do not routinely use panting as a
`low-cost' component to thermoregulation could be a fruitful avenue of future
research.
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Acknowledgments |
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