Digestive state influences the heart rate hysteresis and rates of heat exchange in the varanid lizard Varanus rosenbergi
1 Adaptational and Evolutionary Respiratory Physiology Laboratory,
Department of Zoology, La Trobe University, Melbourne, Victoria 3086,
Australia
2 School of Biosciences, University of Birmingham, Birmingham B15 2TT,
UK
* Author for correspondence (e-mail: timothy.clark{at}latrobe.edu.au)
Accepted 18 April 2005
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Summary |
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Key words: metabolic rate, metabolism, digestion, rate of oxygen consumption, body temperature, reptile, goanna, fasting, postprandial
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Introduction |
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A study on the savannah monitor (Varanus exanthematicus) reported
that the rate of cooling from 35°C to 27°C was not affected by SDA
(Bennett et al., 2000), leading
the authors to dismiss the thermoregulatory hypothesis proposed for the
evolution of endothermy, which postulates that increments in metabolic rate of
ancestral ectotherms elevated Tb and helped to retard
changes in Tb in different thermal environments
(Ruben, 1995
). Nevertheless,
in the study by Bennett et al.
(2000
), the heat increment of
feeding of V. exanthematicus at 32°C (increase of 0.65°C) was
greater than that at 35°C (increase of 0.40°C). Furthermore, the
Q10 of the metabolic increment associated with digestion in the
Burmese python (Python molurus) from 25°C to 35°C was less
than that of resting metabolic rate (reworked data from
Wang et al., 2003
), indicating
that the relative increase in metabolism associated with digestion is greater
at cooler temperatures than at warmer temperatures.
It may be hypothesized, therefore, that the rate of cooling during
digestion would be more greatly influenced at lower temperatures when the heat
increment of feeding is proportionately greater. Additionally, like other
vertebrates, reptiles cannot maximally perfuse all of the circulatory beds at
the same time, thus the increased perfusion of the gastrointestinal organs
that occurs during digestion may compromise cutaneous perfusion during warming
if fH cannot increase sufficiently to perfuse enough blood
to satisfy both processes (see Zaar et
al., 2004). Consequently, the rate of heating may be reduced in
postprandial animals, although this was reported not to be the case for V.
exanthematicus over a relatively narrow temperature range (28-38°C;
Zaar et al., 2004
). Finally,
if the changes in fH are solely for the purpose of
modifying peripheral perfusion, there should be no associated changes in
energy demand and, consequently, no hysteresis in the rate of oxygen
consumption
(
O2). To test
these hypotheses, we measured the rates of heating and cooling, and the
associated changes in fH and
O2, in fasting
and postprandial Varanus rosenbergi Mertens 1957 when given the
opportunity to thermoregulate behaviourally over a broad
Tb range of 19-35°C, which is within the
Tb range (10-38°C) previously reported for this
species in the natural environment
(Christian and Weavers, 1994
;
Rismiller and McKelvey,
2000
).
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Materials and methods |
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Instrumentation
The lizards were instrumented using similar methods to those described in
Clark et al. (2005a). Briefly,
O2 was obtained
by lightly taping a lightweight (approximately 10 g), transparent,
loose-fitting mask over the head of the animal. Air was drawn through the mask
by a pump (1-4 l min-1), and a subsample of the air leaving the
pump was passed through columns containing a drying agent (Drierite; Hammond,
Xenia, OH, USA) and a carbon dioxide absorbent (Dragersorb; Lubeck, Germany)
and subsequently analysed for the fractional content of oxygen by a calibrated
gas analyser (Powerlab ML205; ADInstruments, Sydney, Australia). The rate of
oxygen consumption was calculated from airflow through the mask and the
difference between incurrent and excurrent fractional concentrations of dry,
CO2-free air (see appendix in
Frappell et al., 1992
). Values
of
O2 are
expressed at STPD.
Heart rate was determined from an electrocardiogram (ECG). Three leads were attached to the dorsal surface of the animal, in an arrangement that triangulated the heart, by using self-adhesive Ag/AgCl ECG electrode pads (Unilect, Wiltshire, UK). The ECG signal was appropriately amplified (BIO amp; ADInstruments). Body temperature was measured by inserting a calibrated thermocouple (T-type Pod; ADInstruments) 5-6 cm into the cloaca, which remained in position for the duration of the experiment. The outputs from this, the gas analyser and the ECG amplifier were simultaneously collected at 100 Hz (Powerlab 8sp; ADInstruments) and displayed on a computer using Chart software (ADInstruments). Animals were monitored throughout all experiments using a digital computer-linked camera.
Protocol
Heating and cooling in fasting lizards
Animals were fasted for at least 8 days prior to the first series of
experiments. Animals were removed from the holding facility (28-31°C),
instrumented and placed in a constant temperature room (floor area 1.5
mx2.0 m) at 14°C. When Tb dropped below
19°C, a heat lamp positioned above the floor was switched on. The maximum
skin temperature that a lizard could possibly attain under the heat lamp was
43°C [determined during a control experiment when three dead lizards (mean
Mb=1.59±0.11 kg) were left under the heat lamp
until skin temperature reached a plateau]. Hence, the temperature differential
between Tb and Ta (T)
was similar when Tb was 29°C during heating
(
T=43-29=14°C) and 28°C during cooling
(
T=28-14=14°C) or when Tb was 30°C
during heating (
T=43-30=13°C) and 27°C during cooling
(
T=27-14=13°C), and so on. Most lizards voluntarily moved
underneath the lamp to bask, although on very few occasions the lizard was
initially gently moved by the experimenter. All lizards voluntarily moved from
underneath the lamp when they reached a Tb of 33-36°C,
and either rested and cooled, or shuttled in and out from underneath the heat
lamp. After a few hours, the heat lamp was switched off and the lizards that
had shuttled were allowed to cool again to obtain a Tb
below 19°C (two fasting individuals were cooled only to 20°C; see
Table 1). The lizard was then
removed from the room and returned to the holding facility.
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Heating and cooling in postprandial lizards
Five to 10 days after the initial series of experiments, animals in the
holding facility were individually fed mice and/or chicken necks to satiation
(7-18% of fasted body mass, mean 10±1%; all animals fed voluntarily).
Animals were then placed in the constant temperature room at 30±1°C
and observed (maximum 5 h) for any food regurgitation, after which time they
were instrumented as outlined above. One animal regurgitated part of its meal
3.5 h after feeding, so the mass of the food consumed by that individual was
recalculated accordingly. All animals remained relatively quiescent for at
least 23 h after consumption of a meal, and any brief periods of activity were
excluded from the analysis (see below). After approximately 23 h (in V.
exanthematicus, postprandial fH and
O2 reach a
maximum at
24 h; Hicks et al.,
2000
), the room temperature was dropped to 14°C (taking
approximately 30 min) and, when Tb dropped below 19°C,
the heat lamp was switched on and the heating and cooling protocol followed as
outlined above. This protocol made it possible to perform fasting and
postprandial heating and cooling experiments on each individual with only
small differences in Mb (mean fasting
Mb, 1.35±0.09 kg; mean postprandial
Mb, 1.34±0.09 kg), given that the increase in
Mb that was associated with consumption of a meal was
typically countered by the decrease in Mb that had
occurred for each individual between the fasting and postprandial experiments
(i.e. 5-10 days).
Data analysis and statistics
Body mass was measured immediately prior to each particular experiment, and
O2 was
normalised using fasting Mb (to account only for
metabolizing tissue), while time taken to heat/cool was normalised using total
Mb, which included any food that had been consumed (see
Discussion). Data for all variables were averaged into 30 s blocks before
further analysis. Only data for resting animals were used in the analysis; any
periods of activity during the postprandial, heating or cooling periods
(determined using the camera and/or interference signals on the ECG trace)
were excluded. The dead lizards that were used as a control (see above) were
heated and cooled, following the same protocol as outlined above, for
comparison with live animals (see Table
1). It should be noted that this study was not undertaken for a
comprehensive comparison of heating versus cooling rates, but rather
to compare fasting and postprandial lizards under an identical experimental
setup. Differences in heat exchange,
O2 and
fH during heating and cooling for fasting and postprandial
animals at each Tb were analysed using two-way analysis of
variance (ANOVA) for repeated measures. A Bonferroni t-test was
applied where appropriate to distinguish mean values that differed
significantly. N=7 unless otherwise indicated. All data are presented
as means ± S.E.M.
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Results |
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Both fasting and postprandial lizards displayed a hysteresis in fH, with values during cooling being lower than those during heating at a given Tb. Heart rate during heating was the same for each digestive state at any given Tb between 19°C and 35°C (Fig. 3B), although the magnitude of the hysteresis for postprandial lizards was reduced (P<0.05 above 23°C only) in comparison with that of fasting lizards (P<0.05 at all Tbs) as a result of a higher fH during cooling for a given Tb (Fig. 3B). The mean maximum difference in fH between cooling and heating for fasting lizards was 19.7 beats min-1, which occurred at 31°C, while the mean maximum difference in fH for postprandial lizards was only 10.4 beats min-1, which occurred at 33°C (Fig. 3C).
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Inverse rates of heating (the time taken per kg for a 1°C change in Tb) for fasting and postprandial animals were temperature independent over the entire range (P>0.05; Table 1), and both fasting and postprandial lizards heated more rapidly than the dead control animals (Table 1; P>0.05). Postprandial lizards tended to heat more slowly than fasting lizards at all Tbs and, consequently, took 1.7x longer than fasting animals to heat from 19°C to 35°C (P=0.043; Table 1). The control animals cooled quicker than live fasting animals under the same experimental conditions, suggesting that the resting heat production of live fasting animals, albeit minor, is sufficient to reduce the rate of cooling. Additionally, the time taken per degree Tb change during cooling below 23°C was greater in postprandial animals than both in fasting animals and in the control animals (P<0.05).
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Discussion |
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It is generally accepted that the sympathetic (adrenergic) and
parasympathetic (cholinergic) nervous systems are principally responsible for
short-term cardiovascular control in vertebrates
(Akselrod et al., 1981);
however, evidence exists for alternative [i.e. non-adrenergic and
non-cholinergic (NANC)] cardiovascular control systems. For example, in the
snake Boa constrictor, double autonomic block of ß-adrenergic
and cholinergic systems prevented an increase in fH during
exercise, but not during digestion, so it was subsequently postulated that a
circulatory regulatory peptide may exert a positive chronotropic effect on the
heart during the postprandial period (Wang
et al., 2001a
). Furthermore, prostaglandins have been suggested to
be primarily responsible for the fH hysteresis in
Pogona vitticeps during heating and cooling
(Seebacher and Franklin,
2003
), given that the fH hysteresis in the
closely related Pogona barbata was maintained following double block
of the ß-adrenergic and cholinergic control systems
(Seebacher and Franklin,
2001
).
In the present study for V. rosenbergi, the inability of
postprandial animals to increase fH above that of fasting
animals during heating at a given Tb suggests that the
regulatory system(s) responsible for fH during digestion
and heating in inactive animals may have reached a maximum and may only be
increased further by modifying the influence of ß-adrenergic and
cholinergic control systems, as occurs during exercise, for example (see
Wang et al., 2001b and
references within). Indeed, Clark et al.
(2005a
) reported for maximally
exercising V. rosenbergi at 25°C a fH of
51.0±0.9 beats min-1, which is greater than that obtained at
the same Tb during heating in the present study (see
Fig. 3). In this context,
postprandial Python molurus can achieve a higher
fH during exercise than a similarly exercising individual
in a fasting state, although this increase is not enough to demonstrate a
complete additive response in fH for simultaneous
digestion and exercise (Secor et al.,
2000
).
If, indeed, a limit has occurred in fH during heating
in postprandial V. rosenbergi, then it is likely that prioritization
of blood flow to the periphery or to the gastrointestinal organs would be
necessary with a subsequent impairment of the other process
(Zaar et al., 2004). It seems
as though digestion may have taken at least partial priority over
thermoregulation, as indicated by the increased time taken for postprandial
animals to heat from 19°C to 35°C (see below;
Table 1). Similarly, Axelsson
et al. (2002
) concluded for sea
bass that once food has been eaten, it is digested and absorbed, even at the
expense of a reduced oxygen supply to other organs. By contrast, it has
recently been reported for V. exanthematicus that simultaneous
digestion and heating resulted in an additive response in
fH such that fH during heating was
higher in postprandial animals in comparison with that in fasting animals
(Zaar et al., 2004
) and,
consequently, the rate of heating of postprandial animals was not compromised.
Further studies on cardiovascular control of reptiles are required to clarify
the interaction that exists between exercise, digestion and
thermoregulation.
As far as we are aware, there is no study of reptiles that has
simultaneously measured
O2 with
fH during heating and cooling, and it is evident in the
present study that the fH hysteresis, and the resultant
enhancement of thermoregulation, does not have an associated hysteresis in
energy demand; that is, fH and
O2 are uncoupled
during thermoregulation. Such a dissociation between fH
and
O2 would
also be expected for a thermally stressed bird or mammal in which peripheral
blood flow would increase to enhance heat loss. As a consequence of this
uncoupling, a hysteresis must exist in the reverse direction (i.e. higher
during cooling) for at least one of the other circulatory variables (i.e.
cardiac stroke volume and/or tissue oxygen extraction) in accordance with the
Fick equation for the cardiovascular system (see
Clark et al., 2005b
). Of these
other circulatory variables, it may be suggested that the hysteresis exists
for tissue oxygen extraction, as a result of there being little or no oxygen
extracted from the blood perfusing the periphery during heating (see
Baker and White, 1970
). Cardiac
stroke volume is a structural component that is thought not to change
substantially without morphogenetic processes
(Hoppeler and Weibel, 2000
),
and it has been reported for the turtle, Trachemys scripta, that
cardiac stroke volume remained the same for a given Tb
during heating and cooling (Galli et al.,
2004
). Having said this, quite substantial changes in cardiac
stroke volume were reported for V. rosenbergi during exercise in an
earlier study (see Clark et al.,
2005a
), implying that further measurements are required to clarify
the component(s) of the circulatory system for which a hysteresis exists in
the reverse direction to that of fH.
Heating
It has been suggested that thermoregulation in reptiles is facilitated by
the light-sensitive pineal gland situated at the top of the head
(Tosini and Menaker, 1996;
Tosini, 1997
), although there
is also evidence that reptiles respond to heat rather than light per
se (see Seebacher and Franklin,
2001
). Nevertheless, the fact that lizards in the present study
wore masks that encompassed the head created some concern that the function of
the pineal gland may be compromised. In an attempt to counter this, care was
taken to ensure that masks were as transparent as possible, and observations
of most lizards repositioning themselves under the heat lamp shortly after it
was switched on suggested that the mask did not considerably obstruct the
ability of the lizards to detect light and/or heat.
Both for fasting and postprandial animals, the time taken to heat between
19°C and 35°C was less than that taken to cool, which is consistent
with several previous studies of reptiles (e.g.
Bartholomew and Tucker, 1963;
Grigg and Seebacher, 1999
).
Given that
T was similar when Tb was
34°C during heating (
T=43-34=9°C) and 23°C during
cooling (
T=23-14=9°C) (see Materials and methods), the
variation in the time taken to change Tb by 1°C during
heating and cooling at these Tbs (see
Table 1) cannot be explained by
T alone, thus implying a regulation of thermal conductance by
live animals. The fact that the control animals did not heat as rapidly as the
live animals suggests that increased blood flow to the periphery (see above)
is critical to increase thermal conductance and obtain the fast rate of
heating. The speed at which fasting V. rosenbergi heated from
19°C to 35°C (1.7 min deg.-1 kg-1) is faster
than has been reported for several other varanids including V.
exanthematicus (7.1 min deg.-1 kg-1 between
28°C and 38°C; calculated from
Zaar et al., 2004
), V.
gouldii (2.3 min deg.-1 kg-1 at 30°C) and
V. varius (3.0 min deg.-1 kg-1 at 30°C;
calculated from Bartholomew and Tucker,
1964
). Differences in operative temperatures and/or digestive
state between studies may account for some of the disparity, although the
rapid heating of V. rosenbergi in the present study is probably
assisted by the dark colouration of its skin, which is an adaptation to a
high-latitude habitat and has been reported to display a greater absorptance
than the skin of any other varanid
(Christian et al., 1996
).
Interestingly, the period of time taken for postprandial lizards to heat from 19°C to 35°C was compromised when compared with that for fasting animals. Generally speaking, as a consequence of consuming a meal, postprandial lizards would have a reduced surface area to mass ratio (the magnitude of which is dependent on the size of the meal) and a higher heat capacity and would therefore take longer to warm the entire body. The protocol followed in the present study, however, ensured that each lizard was of similar Mb when in the fasting state and in the postprandial state (see Materials and methods). It is possible that postprandial lizards had a reduced rate of heating due to a decrease in peripheral blood flow during digestion, resulting from a limitation in the fH response and therefore a prioritization of digestion over thermoregulation (see above). Measurements of blood flow to the gastrointestinal organs and/or the periphery of simultaneously heating and digesting animals are required to investigate this suggestion.
Cooling
This study is the first to report the heat increment of feeding acting to
slow the rate of cooling of a reptile. Postprandial lizards with a
Tb less than 23°C cooled more slowly than fasting
lizards and the control animals, exemplified at 19°C when the mean times
taken to cool were 47.4 min deg.-1 kg-1, 13.9 min
deg.-1 kg-1 and 9.8 min deg.-1
kg-1, respectively (Table
1). It appears as though the rate of decline in
Tb is reduced at low temperatures due to the heat
increment of feeding being proportionately greater at such low temperatures
(see Introduction). Alternatively, it may be suggested that the development of
a net right-to-left intracardiac shunt during digestion would produce a
similar result by decreasing pulmonary circulation and reducing the heat lost
across the surface of the lungs during cooling, although the development of
such a shunting pattern during digestion seems unlikely (see
Wang et al., 2001b for a
review) and shunt patterns are thought to contribute little to heat exchange
(Weathers and White, 1971
;
Galli et al., 2004
).
Nevertheless, given that the difference in cooling rates of fasting and
postprandial lizards was apparent only below 23°C, it is clear why
previous studies, which were performed over narrower and higher
Tb ranges, have not reported such findings (e.g.
Bennett et al., 2000
;
Zaar et al., 2004
).
It appears that the heat increment of feeding temporarily enhances
thermoregulatory ability in V. rosenbergi at low temperatures, and
this would presumably prolong the period for which Tb
exceeds ambient temperature throughout cooler periods in the natural
environment (e.g. at night), possibly augmenting the rate of digestion and/or
digestive efficiency (Harlow et al.,
1976; Stevenson et al.,
1985
; Toledo et al.,
2003
; see Wang et al.,
2003
for a review) and reducing the time required to reheat upon
the onset of warmer conditions (e.g. the following morning). Consequently, in
addition to considering the effects of Mb and the rate at
which an animal moves through a thermal environment (see
Seebacher and Shine, 2004
),
the postprandial influence on rates of cooling must be considered in studies
that predict the minimum operative temperature available to an animal in a
particular environment.
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Acknowledgments |
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References |
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