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First published online December 16, 2008
Journal of Experimental Biology 212, 137-144 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.023531
Decreased precision contributes to the hypoxic thermoregulatory response in lizards
Department of Biological Sciences, Brock University, St Catharines, ON, Canada, L2S 3A1
* Author for correspondence (e-mail: viviana.cadena{at}brocku.ca)
Accepted 2 November 2008
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Summary |
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2–4°C in
Tb, the drop being greatest in situations where
Tb must be actively defended. Situations that force the
lizards to continually choose temperatures, rather than passively remain at a
given temperature, lead to an increase in the variability in the manifested
Tb, which is further exaggerated in hypoxia. This study
reveals that a decrease in thermoregulatory precision caused by a diminished
propensity to move or effect appropriate thermoregulatory responses may be a
contributing component in the lowering of selected body temperatures observed
in many hypoxic ectotherms.
Key words: hypoxia, behavioural thermoregulation, thermosensitivity, thermoregulatory effort, variability, anapyrexia
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) as well
as in the field (Rollinson et al.,
2008). Indeed, it is common for most animals studied to reduce
Tb in hypoxia (Wood,
1995; Wood and Gonzales,
1996), an inherent regulatory response that protects tissues
against oxygen depletion, particularly in life-sustaining organs such as the
heart and the brain. This fall in Tb can reduce oxygen
demands by up to 50% (Hicks and Wood,
1985) through a combination of lowered metabolic rate via
Q10 effects [as well as metabolic depression
(Bickler and Buck, 2007;
Hicks and Wang, 2004)], an
accompanying reduction in ventilatory costs, and an increase in the
oxygen-loading capacity of the lungs (Wood
and Gonzales, 1996).
It is not uncommon for reptiles in nature to encounter situations which can
cause hypoxaemia. Infections from blood-borne parasites are known to reduce
the oxygen-carrying capacity of the blood
(Saint-Girons, 1970;
Schall et al., 1982); anaemia
and exhaustive exercise can also cause temporary hypoxaemia. These conditions
are known to induce decreases in Tb similar to those
induced by external hypoxia (Hicks and
Wood, 1985; Petersen et al.,
2003). A fall in Tb also commonly occurs in
response to numerous stressors in addition to hypoxia [e.g. dehydration,
hypoglycaemia, toxins (Kozak,
1997)], suggesting a common regulatory process that responds to
alterations in the neurochemistry of the brain
(Bicego et al., 2007). Thus,
the relevance of examining hypoxia-induced alterations in
Tb also lies in its potential for shedding light on the
thermoregulatory defence mechanisms common to a number of stressors.
The natural and laboratory Tb values of reptiles have a
skewed distribution (Dewitt and Friedman,
1979), dropping off sharply at higher temperatures with a wider
distribution at lower temperatures. One explanation for this may be the
decrease in locomotor performance observed in reptiles when exposed to low
temperatures, prolonging the time animals spend at low Tb
values. Higher temperatures, on the other hand, are thought to be typically
avoided due to lethal effects and potential cardio-respiratory limitations
(Wood, 1984). Any factor that
decreases the responsiveness to cold could increase the overall variability in
Tb, because animals will not respond as readily to lower
temperatures. The net result of encountering a wider distribution of low
temperatures is an overall fall in selected Tb. Although
hypoxia has been shown to lower the preferred Tb along
with other thermoeffectors [e.g. panting, skin reflectivity
(de Velasco and Tattersall,
2008; Hicks and Wood,
1985; Petersen et al.,
2003; Tattersall and Gerlach,
2005)], the precision of thermoregulation has been largely
overlooked. If the decrease in Tb observed in conditions
like hypoxia is associated with a decrease in thermoregulatory precision, it
is possible that changes to the underlying thermosensation may be significant
contributors to the change in Tb
(McKemy, 2007;
Sayeed and Benzer, 1996).
On the other hand, severe hypoxia can limit the capacity for aerobic
metabolism (Hicks and Wang,
2004; Wood and Glass,
1991) and therefore the potential for aerobic activity. Given that
ectotherms commonly reduce metabolic expenditure in response to hypoxia
(Bickler and Buck, 2007), it is
expected that lizards exposed to low oxygen concentrations will be less apt to
exhibit movement than those in normoxia. If extensive movement is required for
thermoregulation, it is plausible that hypoxia will induce a decrease in
thermoregulatory precision. To test this prediction we took advantage of the
different metabolic efforts associated with three different techniques
(Withers and Campbell, 1985)
commonly used to assess thermal preference.
This study aimed to answer whether the hypoxia-induced lowering of Tb consists solely of a regulated decrease in Tb (i.e. decrease in set-point), as has been extensively suggested, or whether the decrease in Tb is accompanied by a decrease in thermoregulatory precision (i.e. an increase in load error). In addition, this study examined the importance of `effort' (i.e. amount of locomotion required to maintain a constant Tb) on the variability and magnitude of the hypoxic thermoregulatory response. The recognition of a decrease in thermoregulatory precision during hypoxia would shed light on the potential for a reduction in thermosensitivity and/or a diminished propensity to move as contributing factors to the hypoxic decline in Tb.
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MATERIALS AND METHODS |
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).
All procedures involving the use of these animals were approved by the Brock
University Animal Care and Use Committee (protocol no. 041001).
Experimental set-up
To examine the effect of thermoregulatory effort on the variability and
magnitude of the hypoxic thermoregulatory response, we used two configurations
of an electronic temperature shuttle box (see below for details), as well as a
thermal gradient [all methods are similar to those described in another
publication (Cadena and Tattersall,
2009)]. The temperature on each side of the shuttle box and the
thermal gradient were measured using platinum thermistor wires and
thermocouples calibrated against a known temperature standard. Body
temperatures of lizards were monitored using implanted telemeters (model
TA11CTA-F40 or TA10CTA-F40, Data Sciences International PhysioTel® and
MultiplusTM implant; St Paul, MN, USA), calibrated to the same source.
Both air temperature (Ta) and Tb were
thus recorded to an accuracy of ±0.1°C. The shuttle box was
essentially a two-choice chamber, where the two chambers were held at
different temperatures. We used the shuttle box in two configurations: (1)
ramping temperatures and (2) extreme temperatures. The ramping temperature
protocol was designed such that a 10°C differential was always maintained
between the two chambers, using electronically controlled radiator fans and
heater coils. Temperatures inside the box changed dynamically according to the
location of the lizard (either the heating or the cooling compartment), so
that Ta rose at a fixed rate of 0.7°C
min–1 whenever the lizard moved to the heating compartment
and cooled at this same rate when the lizard moved to the cooling compartment.
A detailed description of the shuttle box specifications is provided in
another study (Cadena and Tattersall,
2009). Previous experiments showed that this rate of heating and
cooling provides estimates of preferred Tb and
Tb precision equivalent to those obtained in a thermal
gradient (Cadena and Tattersall,
2009). The extreme temperatures protocol used the same shuttle box
with one compartment held at a constant 15°C while the other was held at
50°C. In this kind of shuttle box the temperatures inside the chambers are
maintained well above and below the animals' preferred temperatures
(Berk and Heath, 1975a;
Berk and Heath, 1975b;
Blumberg et al., 2002;
Hicks and Wood, 1985;
Myhre and Hammel, 1969),
relying on the animal shuttling at higher rates than in either the thermal
gradient or the ramping shuttle box to achieve a desired
Tb. In the extreme temperatures shuttle box, extra
energetic costs are added to the thermoregulatory behaviour of lizards, which
will potentially influence variability
(Cadena and Tattersall, 2009);
this was consistent with the objectives of the study. Finally, a thermal
gradient was utilised to test thermoregulatory preference in a low effort
environment. The gradient [described elsewhere
(Cadena and Tattersall, 2009)]
consisted of a flat, copper sheet with one end maintained at 15°C and the
other at 50°C. Fans at either end of the gradient helped to ensure a
linear gradient in air temperatures similar to floor temperature, as well as
circulating the gases during hypoxic exposure.
Experimental design
Lizards were fasted for a period of 12 h prior to the experiments.
Experiments were run from 08:00 to 20:00 h, with the first 4 h consisting of a
habituation period (in normoxia). Previous experiments indicated a
considerable decline of putative non-thermoregulatory activity (`exploratory
shuttling') after an initial 4 h period inside the shuttle box
(Cadena and Tattersall, 2009).
At the beginning of the day the animals were cold (Tb at
08:00 h, 28.5±0.4°C) and had just emerged from their nocturnal
shelter. To avoid further cooling-induced lethargy, individual lizards were
placed on the warm side of the experimental apparatus at the start of each
experiment. Upon completion of the experiment, lizards were returned to their
housing facilities.
Series I: influence of hypoxia on thermoregulatory behaviour in a ramping shuttle box
Each individual lizard was exposed to five different oxygen concentrations
(4, 5, 7, 10 and 21% O2) in a random order, one oxygen level per
day. After the initial habituation period, the oxygen concentration was
manipulated using an oxygen controller (Pro-Ox, model 110, BioSpherix,
Redfield, NY, USA). This was done by delivering nitrogen into the shuttle box
and flushing out the air, until the desired level of oxygen (±0.2%
O2) was reached, usually within 30 min. This half hour following
the initiation of hypoxia was not included in the data analysis, leaving a
total of 7.5 h of analysable data. Normoxic levels (21% O2) were
produced by leaving the shuttle box open to room atmosphere.
Ta and Tb were recorded at 30 s
intervals throughout the experiments. The time and temperature at the moment
the lizard exited either compartment of the box were also recorded. The number
of times each lizard shuttled was also calculated over the 7.5 h period as an
indication of thermoregulatory effort and activity.
Series II: influence of methodology on the assessment of thermoregulatory behaviour in hypoxia
We used nine lizards in these experiments and exposed them to 21% and 4%
O2 [normoxic data are derived from our previous study
(Cadena and Tattersall, 2009)].
As in series I, individual lizards were placed in the experimental apparatus
for an initial 4 h habituation period and 30 min were required for oxygen to
reach the desired level of 4% O2. Lizards were then allowed to
thermoregulate inside the experimental apparatus for an additional 7.5 h.
Data recording and analysis
Assessment of the thermoregulatory variables, data acquisition, recording
and processing followed the methodology described elsewhere
(Cadena and Tattersall, 2009).
Significant differences between groups detected by a repeated measures
analysis of variance (RM ANOVA) (see below for details) were further explored
using the Holm–Sidak procedure as a post-hoc method.
Differences were considered significant at P
0.05. Whenever data
were not normally distributed, log transformations were applied to comply with
the homoscedasticity requirements of the statistical tests. An analysis of the
residuals on the log-transformed data indicated these were normally
distributed. On occasions where normality could not be achieved, an RM ANOVA
on ranks was used instead. All statistical analyses were performed using
SigmaStat statistical software (version 3.0.1, Systat Software Inc., San Jose,
CA, USA).
Series I: influence of hypoxia on thermoregulatory behaviour in a ramping shuttle box
Medians for upper escape ambient temperature (ambient temperature at which
a lizard exited the hot side of the shuttle box; UETa), lower
escape ambient temperature (ambient temperature at which a lizard exited the
cold side of the shuttle box; LETa), Tb and
Ta and means for the Tb range (central
68% range of the Tb distribution; RTb), as well
as coefficients of variation (c.v.) of UETa, LETa, upper
escape Tb (body temperature at which a lizard exited the
hot side of the shuttle box; UETb) and lower escape
Tb (body temperature at which a lizard exited the cold
side of the shuttle box; LETb) across the 7.5 h of experimental
conditions were compared between treatments using RM ANOVA. The c.v. was used
as an indicator of intra-individual variability since it standardises
differences in variability that may result from the level of the values.
RTb was described using the central 68% of the data range, as it is
analogous to the standard deviation around the median (see
Dewitt, 1967). Due to the
intrinsic dependence between RTb and the corresponding high and low
limits of this range (HTbL and LTbL), statistical
analysis was only performed on RTb.
A one-way RM ANOVA was also used to test differences in the number of
shuttles between oxygen levels. To account for possible confounds between the
multiple test procedures performed on the Ta and
Tb variables (i.e. Tb,
Ta, UETa, LETa and RTb
and also between c.v. of escape temperatures) Bonferroni–Holm procedures
(Holm, 1979) were performed on
the P-values.
Series II: influence of methodology on the assessment of thermoregulatory behaviour in hypoxia
The median values for Tb from each individual
(N=9) were calculated. Tb and RTb were
compared between the three different methodologies (i.e. ramping shuttle box,
extreme temperatures shuttle box and thermal gradient) and oxygen levels using
a two-way RM ANOVA, with methodology and oxygen level as factors.
The number of shuttles that occurred in the extreme trials was compared between 21% and 4% O2 using Student's paired t-test. Additionally, in the extreme temperatures shuttle box, animals were noted to spend time straddling the cold and warm compartments. The proportion of time spent in the cold, hot and `middle' (straddling the two compartments) was calculated for both oxygen concentrations, but to avoid type I error only the proportion of time spent in the middle was compared between 21% and 4% O2 using an RM ANOVA. For the thermal gradient experiments, `movement' was approximated by summing up the number of times that animals moved greater than 20 cm in a 1 min period. This value was subsequently compared between the 21% and 4% O2 treatments. P values for movement estimates in the extreme temperatures shuttle box and the thermal gradient and for time spent in the middle between compartments of the shuttle box were Bonferroni–Holm corrected.
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RESULTS |
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There were no significant differences in the c.v. of UETa and UETb (F4,40=1.45, P=0.235 and F4,40=2.22, P=0.167, respectively) between oxygen treatments. The c.v. of LETa and LETb increased significantly at the lowest oxygen concentrations. When compared with normoxia, the c.v. of LETa was significantly higher at 4%, 5% and 7% oxygen (F4,40=8.71, P<0.001) and the c.v. of LETb rose to reach significance at 4% oxygen (F4,40=5.65, P=0.003; Fig. 3).
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The pronounced decrease in LETa was reflected in the resulting preferred RTb; both the high (HTbL) and low (LTbL) limits of RTb decreased with lower oxygen concentrations (Fig. 2; Table 1). Because LTbL exhibited a more pronounced decrease than HTbL, RTb increased significantly at 4% oxygen (F4,40=5.92, P<0.001; Table 1).
Exposure to 5% and 4% oxygen led to significantly lower Ta values (F4,40=9.91, P<0.001) than exposure to 21% oxygen (Table 1). Preferred Tb followed a similar pattern, presenting slightly higher values than Ta at all levels of oxygen (Fig. 2; Table 1). Tb was 34.7±0.7°C under normoxic conditions. Tb decreased significantly at 4% and 5% O2 (F4,40=15.99, P<0.001) compared with normoxia (Fig. 1; Table 1).
Hypoxia elicited a progressive decrease in the number of shuttles between compartments (Fig. 4). This decrease was significant at 5% and 4% O2 (F4,40=5.69, P=0.001) where lizards shuttled 27.4±7.4 and 20.7±6.7 times, respectively, during a 7.5 h period compared with 59.5±61.2 times in normoxia.
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Series II: influence of methodology on the assessment of thermoregulatory behaviour in hypoxia
Methodology had a significant effect on Tb; lizards
exhibited significantly lower Tb values at both 21% and 4%
O2 (two-way RM ANOVA, F2,16=24.20,
P<0.001) when evaluated in the extreme temperatures shuttle box
compared with both the thermal gradient and the ramping shuttle box.
Regardless of the methodology used, however, hypoxia (4% O2)
induced a significant decrease in Tb (two-way RM ANOVA,
F1,8=57.75, P<0.001;
Table 2;
Fig. 5). LTbL and
HTbL were affected by hypoxia (4% O2) in all
methodologies used (Table 2);
however, a significant effect of hypoxia on RTb was only seen in
the ramping shuttle box, but not in either of the other two treatments
(two-way RM ANOVA, F1,8=16.09, P=0.003).
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Movement between the cold and hot side of the extreme temperature shuttle box was significantly affected by hypoxia (t11=2.47, P=0.031). The shuttling frequency over the 7.5 h recording period fell from 77.7±68.9 shuttles in normoxia to 23.7±25.1 shuttles at 4% O2 (Fig. 4). Similarly, in the thermal gradient trials, movement (assessed as the number of times in 7.5 h that the animals moved more than 20 cm min–1) fell significantly from 76.8±66.5 in normoxia to 25.2±25.6 at 4% O2 (t10=3.24, P=0.027). Interestingly, in the extreme trials, lizards spent a considerable amount of time straddling the transition zone between the cold and warm chambers, something not observed in the ramping shuttle box trials. Moreover, at 4% oxygen, lizards spent significantly more time (F1,9=13.10, P=0.018) inactive in the middle section between the two choice chambers (49.4±36.9% of the time compared with 17.2±23.6% in normoxia; Table 3).
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Time course and Tb distributions: comparison of methodology
Low oxygen induced changes in selected Ta, and
therefore Tb, within the first hour of exposure in all
methodologies (Fig. 6). The
decline in Tb in the ramping shuttle box protocol and
thermal gradient was gradual, taking 2–3 h, after which it became more
variable, whereas the extreme shuttle box induced a rapid (within 30 min)
decline in Tb that was nearly sustained throughout the 7.5
h of measurement. The resulting Tb distribution patterns
(Fig. 6) reveal the widening of
the Tb distribution that occurred in both shuttle box
experiments compared with the thermal gradient trials.
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DISCUSSION |
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) predicts that lizards will actively thermoregulate if the
associated costs are low. Although the model was intended to account for costs
of an ecological nature (i.e. food availability, homogeneity of the thermal
environment, accessibility of basking sites, etc.), it should also be relevant
to situations where metabolic or physiological costs are associated with
thermoregulation. In severe hypoxia, oxygen becomes a limited resource and
locomotion becomes impossible to conduct aerobically. In addition, if frequent
movements are necessary to maintain a narrow Tb range,
lizards are expected to minimise locomotion at the expense of precise
behavioural thermoregulation.
In the present study, bearded dragons did not abandon temperature
regulation at low oxygen conditions, as might be expected if the response was
an unregulated (i.e. hypothermic) decrease in Tb. Instead,
they reduced locomotory oxygen expenditure by reducing the frequency of
shuttles between compartments in the shuttle box
(Fig. 4) and overall movement
in the thermal gradient. In the case of the ramping shuttle box experiments,
this led to a decrease in the precision of thermoregulation, manifested in the
widening of the Tb range. The fact that the frequency of
shuttles at the most extreme level of hypoxia (21 shuttles) is still well
above the predicted number of shuttles (8) if the behaviour was purely
exploratory (Cadena and Tattersall,
2009) provides further evidence that hypoxic lizards are indeed
still actively thermoregulating. Surprisingly, we did not observe a decrease
in thermoregulatory precision in the extreme temperatures shuttle box, where
locomotory requirements are expected to be largest. However, animals in this
protocol were able to compensate by remaining for longer periods of time
straddling the cold and the warm compartments, thus decreasing the amount of
locomotion required to maintain a constant Tb (albeit
lower, compared with the other methodologies;
Fig. 5;
Table 2), and avoiding the
`extreme temperatures' that would have otherwise resulted in a decrease in
thermoregulatory precision.
The effect of hypoxia on lizard thermoregulation was previously described
by Hicks and Wood who showed significant decreases in the preferred
Tb of four different species of lizard exposed to 7%
oxygen (Hicks and Wood, 1985).
Similar decreases in Tb have been observed in situations
such as anaemia and exhaustive exercise, both conditions in which the oxygen
content of the blood is low (Hicks and
Wood, 1985; Petersen et al.,
2003), suggesting similar underlying mechanisms to the
thermoregulatory response. The response observed by Hicks and Wood, however,
was much more pronounced (Hicks and Wood,
1985) than the one observed here (a decrease of 5–7°C
vs the 2–4°C decrease observed by us with exposure to
4% O2). Although this difference may be attributed to differences
between species, it might also be due to methodological differences between
the studies. Hicks and Wood used a thermal gradient and an extreme
temperatures shuttle box to estimate the preferred Tb of
lizards (Hicks and Wood,
1985). Even though thermal gradients require less locomotory
`effort' from the animal, it is hard to discriminate between thermoregulating
lizards and lizards that are not actively thermoregulating but remaining
stationary, due to lack of knowledge of an animal's motivational state. As we
and others (Schurmann and Steffensen,
1994) have observed, ectotherms may not be motivated to actively
thermoregulate in every experiment, and the inclusion of these data may lead
to a lower (usually) estimation of the preferred Tb
(Cadena and Tattersall, 2009).
An extreme temperatures shuttle box, on the other hand, is an energetically
costly condition since it requires frequent and constant shuttling between
compartments to maintain relatively high and constant Tb
levels and can therefore cause decreases in normal Tb
itself (Fig. 5)
(Cadena and Tattersall, 2009).
Our results indicate that the use of a dual-choice shuttle box can inflate the
effect of hypoxia on Tb by twofold compared with other
techniques.
The decrease in Tb of hypoxic lizards observed by Hicks
and Wood was accompanied by a decrease in both UETb and
LETb [when thermoregulating inside an extreme temperatures shuttle
box (Hicks and Wood, 1985)],
suggesting a decline in the upper and lower temperature set-points
(Barber and Crawford, 1977).
Escape Tb and Tb set-points, however,
are not necessarily analogous, since the thermal inertia of even small animals
is usually large enough to cause changes in Tb to lag
behind those of Ta, which is why we report different
variables in our study (see Table
1). Interestingly, however, the upper escape
Ta of bearded dragons in our study rose slightly (but not
significantly), while the lower escape Ta decreased at
lower oxygen concentrations. In other words, it was the drastic decline of the
lower escape Ta and not a decrease in both the upper and
lower temperature set-points that caused the general decrease in
Tb. These findings suggest that in conditions in which
continuous locomotion is required, hypoxia induces changes in behavioural
thermoregulatory precision, a fact hitherto unappreciated.
Implications for the neurophysiological control of Tb
Similar thermoregulatory responses to those reported here have been
observed in experiments in which the medial preoptic area of the brain of the
lizard Dipsosaurus dorsalis was lesioned
(Berk and Heath, 1975b). When
allowed to thermoregulate inside a thermal shuttle box, lesioned lizards
decreased their lower escape temperature and increased their upper escape
temperature while significantly reducing their shuttling frequency compared
with unoperated control groups. Thus, interference with the thermoregulatory
integrative centres of the brain will decrease the precision of
thermoregulation at both upper and lower ranges. Interestingly, hypoxia has
also been shown to significantly decrease the cutaneous sensitivity of humans
to cold but not to warm temperatures
(Golja et al., 2004). This is
consistent with the observation that rhesus monkeys exposed briefly to anoxia
drastically diminished the firing rate of cutaneous cold-sensitive units
(Iggo and Paintal, 1977). The
firing rate of thermosensitive neurons in the preoptic area of rats has also
been shown to change in hypoxia (Tamaki
and Nakayama, 1987), although, generally, the main effect is to
demonstrate an increase in firing rate at low oxygen levels. It is possible,
therefore, that hypoxia causes a decrease in the sensitivity of skin
temperature receptors, thereby diminishing peripheral feedback, as well as
altering the preoptic thermosensitive neurons responsible for thermoregulatory
control in lizards. The tendency for bearded dragons to select lower
Ta and the greater variability in their lower escape
temperatures in low oxygen is consistent with a greater influence of hypoxia
on the cold-sensitive side of thermoregulation. These changes in sensitivity
would be manifested in a decrease in locomotory behaviour, as lizards would
tolerate higher than and lower than normal temperatures and remain stationary
for longer periods of time at Ta values outside their
normally preferred range. This is consistent with the observations in this
study. Although we do not exclude the possibility that the decrease in
Tb observed in hypoxia is a regulated response (i.e.
decrease in set-point), the present study reveals another component and
potential mechanism of the thermoregulatory response to hypoxia; a decrease in
thermoregulatory precision, possibly due to a hypoxia-induced decrease in
thermosensitivity.
Conclusions
The evidence presented here provides further information that, in addition
to the effect on the level of thermoregulation, the temporal patterns and
variance in selected Tb are influenced by the methodology
of assessing thermal preference (Fig.
6). These differences are further increased by hypoxia. The
integrated behavioural thermoregulatory response to hypoxia could be viewed as
resulting from a number of factors. Firstly, severe hypoxia has an impact on
the capacity for aerobic activity. This decreases movement and thereby causes
decreased precision in behavioural thermoregulation requiring locomotory
efforts. Indeed, we observed a decline in the locomotory behaviour of lizards
in hypoxia under all experimental conditions, suggesting a reduction in
activity. Secondly, this behavioural response could be manifested through
differential effects on the cold- and warm-sensing pathways that influence
thermal sensation and effect the changes that accompany behavioural
thermoregulation. This is consistent with data from studies of
thermoregulation in mammals which also show that the precision of
Tb control in hypoxia may be lower than that observed in
normoxia (Barros et al., 2001;
Dupré et al., 1988;
Gordon and Fogelson, 1991;
Tattersall and Milsom,
2002).
Other stress stimuli (that in one way or another increase the costs of
thermoregulation), such as low environmental thermal quality, risk of
predation, territorial defence, or water or food availability have been shown
to evoke similar decreases in Tb and/or thermoregulatory
precision (Cabanac, 1985;
Dewitt, 1967;
Huey and Slatkin, 1976;
Ladyman and Bradshaw, 2003;
Lorenzon et al., 1999;
Mathies and Andrews, 1997),
suggesting conserved thermoregulatory mechanisms in response to costly
conditions. Discovering how these stressors alter the sensation of temperature
and the underlying neurophysiological control of Tb
remains a challenge for future studies.
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Barber, B. J. and Crawford, E. C. (1977). A stochastic dual-limit hypothesis for behavioral thermoregulation in lizards. Physiol. Zool. 50,53 -60.
Barros, R. C., Zimmer, M. E., Branco, L. G. and Milsom, W.
K. (2001). Hypoxic metabolic response of the golden-mantled
ground squirrel. J. Appl. Physiol.
91,603
-612.
Berk, M. L. and Heath, J. E. (1975a). An analysis of behavioral thermoregulation in the lizard, Dipsosaurus dorsalis. J. Therm. Biol. 1,15 -22.[CrossRef]
Berk, M. L. and Heath, J. E. (1975b). Effects of preoptic, hypothalamic, and telencephalic lesions on thermoregulation in lizard, Dipsosaurus dorsalis. J. Therm. Biol. 1, 65-78.[CrossRef]
Bicego, K. C., Barros, R. C. H. and Branco, L. G. S. (2007). Physiology of temperature regulation: comparative aspects. Comp. Biochem. Physiol. A, Mol. Integr. Physiol. 147,616 -639.[CrossRef][Medline]
Bickler, P. E. and Buck, L. T. (2007). Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu. Rev. Physiol. 69,145 -170.[CrossRef][Medline]
Blumberg, M. S., Lewis, S. J. and Sokoloff, G.
(2002). Incubation temperature modulates post-hatching
thermoregulatory behavior in the Madagascar ground gecko, Paroedura
pictus. J. Exp. Biol. 205,2777
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Cabanac, M. (1985). Strategies adopted by juvenile lizards foraging in a cold environment. Physiol. Zool. 58,262 -271.
Cadena, V. and Tattersall, G. J. (2009). The effect of thermal quality on the thermoregulatory behaviour of the bearded dragon, Pogona vitticeps: influences of methodological assessment. Physiol. Biochem. Zool. 82 (in press).
de Velasco, J. B. and Tattersall, G. J. (2008). The influence of hypoxia on the thermal sensitivity of skin colouration in the bearded dragon, Pogona vitticeps. J. Comp. Physiol. B, Biochem. Syst. Environ. Physiol. 178,867[CrossRef][Medline]
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Significant effect of 4% O2 on
Tb within a trial.