The cardiovascular responses of the freshwater turtle Trachemys scripta to warming and cooling
1 Department of Zoophysiology, Aarhus University, 8000 Aarhus C,
Denmark
2 Department of Biosciences, The University of Birmingham, Edgbaston B15
2TT, England
* Author for correspondence (e-mail: ginaljgalli{at}hotmail.com)
Accepted 2 February 2004
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Summary |
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Key words: temperature, rate of heat exchange, turtle, Trachemys scripta, reptile, heart rate, blood flow, blood pressure, cardiac shunt, heart rate hysteresis
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Introduction |
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There is a close relationship between heart rate and peripheral blood flow,
and heart rate has, accordingly, been taken as a sufficient indicator of
changes in blood flow (e.g. Grigg and
Seebacher, 1999; Seebacher,
2000
). Studying the lizard Amphibolurus barbatus,
Bartholomew and Tucker (1963
)
were the first to establish that heart rate, at any given body temperature, is
higher during warming than cooling; this response is known as heart rate
hysteresis. This phenomenon has subsequently been documented in many other
lizards (e.g. Bartholomew and Lasiewski,
1965
) and reviewed by Grigg et al.
(1979
), Seebacher
(2000
) and Seebacher and Grigg
(2001
), crocodilians
(Smith, 1976
;
Franklin and Seebacher, 2003
)
and turtles (Weathers and White,
1971
; Voigt,
1975
). Heart rate hysteresis also occurs in free-ranging
Pogona barbata (previously known as A. barbatus), and the
corresponding changes in blood flow have been estimated to prolong
significantly the time that body temperature remains within the preferred
range (Grigg and Seebacher,
1999
; Seebacher,
2000
).
Heart rate hysteresis may be a simple consequence of a barostatic
regulation that acts to alter heart rate in response to changes in peripheral
resistance, but blood pressures have generally not been measured during
changes in body temperature. However, heart rate hysteresis persists following
total autonomic blockade in Pogona barbata
(Seebacher and Franklin,
2001), and autonomic blockade does not affect subcutaneous blood
flow in the iguana Ctenosaura hemilopha during heating
(Weathers and Morgareidge,
1971
).
Apart from regulated changes in the perfusion of the surface of the body,
it has also been proposed that cardiac shunt patterns should influence the
rate of temperature change in reptiles
(Tucker, 1966;
Baker and White, 1970
;
Hicks, 1998
) as bypass of the
pulmonary circulation could reduce heat loss at the lung surface and promote
heating. According to Tucker
(1966
), bypass of the
pulmonary circulation reduces heat loss at the lung surface and promotes
heating. In turtles, blood flow distribution among the systemic and pulmonary
circulations is determined by their relative vascular resistances
(Crossley et al., 1998
;
Hicks, 1998
). It is possible,
therefore, that changes in the net cardiac shunt patterns merely reflect a
passive consequence of an altered balance between the vascular resistance in
the systemic and pulmonary circulations
(Hicks, 1998
). Thus, when
resistance in the systemic circulation decreases during heating, a net
right-to-left (RL) cardiac shunt develops, while the increased systemic
resistance during cooling leads to a net LR shunt developing. However,
an increased RL shunt during warming will lower arterial oxygen levels
(Wang and Hicks, 1996
),
reducing oxygen supply even though demands for oxygen are rising.
Consequently, the benefits conferred by increasing rates of heat transfer
during warming may be countered by the need to maintain sufficient rate of
oxygen delivery.
So far, no previous studies have provided a complete set of measurements of systemic and pulmonary blood flows during heating and cooling in reptiles, and blood pressures are rarely reported. Here we wish to establish whether blood pressure remains constant during heating and cooling, which would be indicative of a functional barostatic regulation. Secondly, having established normal blood flows and net shunt pattern during heating and cooling, we wish to manipulate pulmonary blood flow using atropine infusion to investigate whether the rates of heating and cooling are affected.
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Materials and methods |
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Surgery and instrumentation
For surgery, turtles were placed ventral side up, intubated with soft
rubber tubing inserted through the glottis, and artificially ventilated using
an HI 665 Harvard Apparatus Respirator (Cambridge, MA, USA), at approximately
1525 breaths min1, and a tidal volume of 3050
ml kg1. The ventilator was connected to an isoflurane
vaporizer (Keighley, England) initially set at 4% isofluorane, which normally
led to disappearance of the pedal withdrawal reflex within 15 min. The
following surgery was performed at 11.5% isofluorane. A 4 cmx4 cm
piece of the ventral plastron was removed above the heart, using a bone saw.
The pectoral muscles were loosened from the excised piece of plastron and
connective tissue surrounding the left pulmonary artery (LPA) and left aortic
arch (LAo) was carefully separated, so that ultrasonic blood flow probes
(Transonic System Inc., NY, USA) could be positioned around the vessels.
Acoustical gel was placed around the flow probes to displace air bubbles that
could disturb the signal. The left carotid artery was occlusively cannulated
for blood pressure measurements with PE-50 catheter tubing, filled with
heparinised saline, and previously treated with the anti-coagulate
triodecylmethylammonium chloride (TD-Mac) heparin complex to reduce blood
clotting. Occasionally the catheter was flushed with heparinised saline.
Finally, a thermistor, enclosed in a soft rubber coating, was placed beside
the heart for measurements of core body temperature. A small notch was cut
into the excised piece of plastron, so the leads and cannula could exit the
animal, and it was then replaced in the animal and glued in place using
silicone adhesive and two-component epoxy glue. The animal recovered from
anaesthesia by continuing the artificial ventilation with air for
approximately 25 min. When it had regained reflexes and spontaneous
ventilation, it was transferred to a holding chamber (30 cmx30 cm)
overnight for recovery. When the experimental protocol was completed, turtles
were killed by an overdose of pentobarbitol (vascular infusion of 200 mg
kg1).
Experimental protocol
Turtles were allowed to recover for 1648 h after surgery. On the
first day each animal was heated and cooled, while heart rate
(fH), systemic blood pressure (Psys),
pulmonary blood flow (pul),
systemic blood flow (
sys),
and body temperatures (Tb) were recorded. In addition, a
temperature probe was placed on the top of the carapace for surface
temperature (Ts) measurements. In order to warm the
animal, turtles were held in air in a box 50 cmx40 cmx60 cm with
an infrared (E27) 150 W heating lamp placed 10 cm above the box. When
Tb had reached 34°C, the heat lamp was switched off
and the animal cooled to approximately 2324°C. During the heating
phase the animal exhibited variable periods of activity, causing variations in
heart rate. The animal was then left overnight at room temperature in the box
with access to water. On the second day the heating and cooling was repeated
using identical conditions following an intra-arterial injection of atropine
(5 mg kg1), delivered through the catheter. The animal was
left for a period of 1 h and then heated and allowed to cool, as previously
described. During heating, the surface temperature probe recorded an increase
in temperature from 23±0.4 to 31.4±0.6°C during the first
2.6±0.2 min. Following this, temperature rose to 38.9±0.6°C,
at which point the heat lamp was switched off. The temperature then dropped to
30.3±0.5°C within the first 4.3±0.4 min, and further
decreased to 24.0±0.2°C after a period of 309±18 min. All
animals were unrestrained throughout all of the experiments. The data for
relative rates of warming or cooling were mass specific.
Data recording
The arterial catheter was connected to a Baxter Edward disposable pressure
transducer (model PX600, Irvine, CA, USA), which was calibrated daily against
a static water column. The signals from the pressure transducer were amplified
using an in-house built preamplifier. The blood flow probes were connected to
a dual-channel blood flow meter (Transonic T206). All signals, including the
temperature measurements, were recorded using a Biopac MP100 at 100 Hz.
Data analysis and calculations
The data were analysed by taking an average of each physiological variable
at each desired temperature interval (2425, 2526,..........,
3334) during warming and cooling.
Heart rate was obtained from the pulsatile pressure of the carotid artery.
All blood flows were corrected for body mass, and following this
sys was calculated as
2.85x
LAo
(Wang and Hicks, 1996
), and
likewise
pul was recorded
as 2x
LPA under the
assumption that both pulmonary arteries receive equal flows. Systemic
resistance (Rsys) was calculated using the mean blood
pressure and mean blood flow
(Rsys=Psys/
sys).
This calculation assumes that central venous blood pressures are zero, which
may lead to an underestimation of Rsys. The net shunt flow
(
shunt) was calculated as
pul
sys.
A negative value would therefore indicate a net RL shunt, and a
positive value indicates a net LR shunt. The proportion of pulmonary
blood flow relative to systemic blood flow was expressed as
pul/
sys.
Total stroke volume (VStot) was calculated by
dividing total blood flow
(
sys+
pul)
by heart rate.
All haemodynamic variables were analysed using a general linear model 3-way analysis of variance (ANOVA) for repeated measures using a Minitab statistical package. Data were tested for differences among untreated and atropinised animals, and whether the animal was warming or cooling. The independent variables were body temperature (Tb), untreated or atropinised, and warming or cooling. Body temperature can be taken as an independent variable rather than time, because measurements of blood flow and other cardiovascular variables were taken continuously but sampled for analysis at a series of set temperatures. This rules out the need to compensate for different warming or cooling rates between animals and the need to make data mass specific, although blood flow data was of course corrected for body mass. Data from animals with a stable body temperature of 22°C, before heating commenced, on the first and second day were compared using a paired t-test. The effect of atropine on the second day was also assessed using a paired t-test. Rates of heating and cooling (min per degree temperature change) and the effect of atropine were analysed with a two-way analysis of variance for repeated measures (two-way RM ANOVA). Differences were considered significant at a 95% confidence levels, when P<0.05.
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Results |
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Heating and cooling rates
Untreated turtles placed under the heating lamp on average heated four
times faster than they cooled (Fig.
1A). This was also the case with atropinised turtles. However,
while all animals heated at similar rates, the time taken per degree
temperature change during cooling in atropinised animals was significantly
longer at all temperatures than in the untreated animals
(Fig. 1B), so that the time
taken for cooling in these animals was prolonged by approximately 1 h in
comparison to untreated individuals (Fig.
1A). This was more pronounced at temperatures below 27°C,
which accounted for the extended cooling period seen in atropinised
turtles.
|
Haemodynamic variables
Heart rate was significantly higher during warming than during cooling at
all temperatures, with all animals exhibiting a classic hysteresis of heart
rate (Fig. 2A). In untreated
animals, this was particularly evident at body temperatures above 30°C. In
atropinised turtles, heart rate was significantly higher, being almost double
the untreated rate at all temperatures
(Fig. 2A). There was no
significant change in VStot during heating and
cooling in untreated and atropinised animals
(Fig. 2B). However, atropine
significantly increased VStot.
|
In untreated animals, pulmonary blood flow increased twofold during
warming, and decreased correspondingly during cooling to previous resting
values (Fig. 3A). At body
temperatures above 30°C,
pul was significantly lower
during cooling than during warming. Overall,
pul was significantly
higher during warming than cooling. In atropinised animals,
pul was significantly
twofold higher than in untreated animals.
sys was considerably higher
during heating than during cooling in both untreated and atropinised turtles
(Fig. 3B). Atropinised animals
had higher
sys than
untreated animals during both heating and cooling, but this difference was not
significant. Systemic blood pressure (Psys) remained
constant during both warming and cooling, in both untreated and atropinised
animals (Fig. 4A). However,
Psys was significantly higher during warming than cooling.
The reduced
sys during
cooling was reflected by an increase in systemic vascular resistance
(Rsys) (Fig.
4B). In untreated turtles, Rsys was higher
during cooling at all temperatures, with the exception of 25°C, while in
atropinised animals, Rsys was higher during cooling at all
temperatures above 26°C (Fig.
4B). In addition, atropinised animals had significantly lower
Rsys values during both warming and cooling, compared to
those of the untreated turtles.
|
|
There was a net right-to-left shunt in untreated turtles at all
temperatures regardless of whether the turtles were heating or cooling
(Fig. 5A). However, the values
remained relatively constant, until temperatures above 31°C, when there
was a decrease in the right-to-left shunt during warming and an increase in
the right to left shunt during cooling. However, there was no significant
difference in
pul/
sys
between warming and cooling. In atropinised animals, a very large net
left-to-right shunt prevailed during both heating and cooling, which was
significantly different from untreated animals. However, as heating proceeded,
this net left to right shunt progressively decreased, and then increased
during cooling (Fig. 5A).
|
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Discussion |
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Hysteresis of heart rate and blood flows
Heart rate at any given body temperature was higher during heating than
cooling. This `heart rate hysteresis' has been described previously in turtles
(Lucey, 1974;
Voigt, 1975
;
Smith et al., 1981
) and
numerous other reptiles (Bartholomew and
Tucker, 1963
; Grigg et al.,
1979
; Grigg and Seebacher,
1999
; Seebacher,
2000
). The higher fH values during heating
were accompanied by an increased
sys, but because systemic
vascular resistance (Rsys) was reduced, blood pressure was
not affected by temperature. Conversely, systemic blood flow was reduced
during cooling and Rsys was increased so blood pressure
was once again maintained unchanged (Fig.
4A,B). Furthermore, blood pressure does not change appreciably
when reptiles are acclimated to different temperatures for several hours or
days (e.g. Stinner, 1987
;
Lillywhite and Seymour, 1978
;
T. Wang, A. Neto, E. W. Taylor, P. Koldkjær, D. Andrade and A. S. Abe,
manuscript submitted for publication). It is likely that hysteresis of heart
rate reflects a barostatic regulation of blood pressure, where heart rate is
increased in response to the lower Rsys during heating and
vice versa during cooling. The effects of temperature on the cardiac
limb of the barostatic response are not well characterised, but it remains
functional over a wide range of temperatures in snakes and seems to contribute
to maintenance of an almost temperature-independent blood pressure (T. Wang,
A. Neto, E. W. Taylor, P. Koldkjær, D. Andrade and A. S. Abe, manuscript
submitted for publication). In several species of reptiles, the heart rate
responses to altered blood pressure can be fully blocked by double autonomic
blockade (i.e. the combination of atropine with a beta blocker; e.g.
Altimiras et al., 1998
).
However, the hysteresis of heart rate was not abolished by autonomic blockade
in the lizard Pogona barbata
(Seebacher and Franklin,
2001
), and the hysteresis also persisted after atropinisation in
our study (Fig. 2). Obviously,
in order to fully investigate the suggestion that heart rate hysteresis is a
consequence of a barostatic response, further investigation of the regulation
of blood pressure during heating and cooling is required that should include
adrenergic blockade and vagotomy to remove both the afferent and efferent arms
of the barostatic response.
Our study provides the first complete set of measurements of systemic and
pulmonary blood flows during heating and cooling in a reptile, but our
measurements cannot reveal whether heating and cooling are associated with
preferential perfusions of the vascular beds in the skin and carapace, where
heat exchange is presumed to occur. Heart rate has previously been used as an
indicator of blood flow (Grigg and
Seebacher, 1999; Seebacher,
2000
). In several species of reptiles, the 133Xe
isotope clearance method shows that cutaneous blood flows increase during
warming, and decrease during cooling
(Morgareidge and White, 1969
;
Weathers and White, 1971
;
Baker et al., 1972
;
Smith et al., 1978
;
Weinheimer et al., 1982
).
Furthermore, in Iguana iguana, using laser doppler, Dzialowski and
O'Connor (2001
) observed
increased and decreased cutaneous blood flows with warming and cooling,
respectively. When blood flow was plotted against body temperature, a strong
hysteresis pattern was observed. This is consistent with our study, where
T. scripta exhibited a hysteresis in changes in blood flow in both
the systemic and the pulmonary circulation during warming and cooling.
Intracardiac shunt patterns
Although the physical conditions for heating and cooling were different, an
identical protocol was used before and after the atropinisation period; hence,
our experiment was designed to allow evaluation of the effects of net cardiac
shunt patterns on heat transfer. It has been suggested that an increased
RL shunt during warming contributes to an increased rate of heating
(Tucker, 1966), but a
comprehensive description of
pul and
sys during heating and
cooling has not previously been reported. Hicks
(1998
) argued that changes in
cardiac shunt patterns when body temperature changes merely reflect
differences in vascular resistances of the systemic and pulmonary
circulations, rather than representing an actual regulation of the shunt
patterns. In our study, the turtles exhibited a substantial RL shunt
that persisted during heating and subsequent cooling, although there was a
tendency for a higher
pul/
sys
at the highest temperatures during heating
(Fig. 5). This indicates that
pulmonary vascular resistance is decreased progressively as
Rsys was reduced during heating. After infusion of
atropine, a large LR shunt prevailed, but
pul/
sys
was progressively reduced with elevated temperature. Thus, when the turtles
were unable to reduce pulmonary vascular resistance through the vagal
innervation of smooth muscle surrounding the pulmonary artery, cardiac output
was directed towards the systemic circulation as Rsys
decreased in response to elevated temperature. During heating in untreated
animals, progressive changes in the relative resistances in the pulmonary and
systemic circuits may prevent the development of large RL shunts as
temperature rises. This response may reflect a need to maintain oxygen
delivery as metabolism rises with temperature (e.g.
Wang et al., 2001
). Indeed, in
rattlesnakes, varanid lizards and toads, the RL shunt is reduced when
acclimated to increased temperature
(Ishimatsu et al., 1988
;
Wang et al., 1998
;
Gamperl et al., 1999
).
The reversal of cardiac shunt patterns after atropine and the large
increase in heart rate did not affect the rate of heating, even though
sys was elevated. Weathers
and White (1971
) also observed
that atropine infusion failed to alter the rate of temperature change in a
previous study on turtles, leading to the conclusion that the rate of
temperature change is not obviously related to heart rate, systemic blood flow
or the net cardiac shunt. In the lizard Pogona barbata, the rate of
heating is, however, faster after atropine and slower after adrenergic
blockade with sotalol (Seebacher and
Franklin, 2001
). It is possible that the higher
pul after atropine leads to
an increased heat loss across the lungs, which could have offset an increased
rate of heat uptake over the skin and carapace. However, if heat is lost at
the lungs surface as a consequence of a large LR shunt, then it would
be expected that the rate of cooling in atropinised animals would be reduced.
Conversely, in this study the rate of cooling was significantly faster in
untreated turtles than in atropinised animals. It is therefore unlikely that
increased pulmonary blood flow would cause heat to be lost across the surface
of the lungs.
Concluding remarks
The maintenance of a constant blood pressure as body temperature changed
indicates that the hysteresis of heart rate during warming and cooling of
reptiles reflects barostatic regulation of blood pressure, but because this
response persists in atropinised turtles, the efferent arm of this control
remains to be understood. Future studies should include experimental
manipulation of blood pressure, so that its effects on rates of warming and
cooling can be ascertained. Major changes in the cardiac shunt pattern do not
seem to affect the rates of temperature change, so that we have to conclude
that changes in the net direction of blood flow, while critically involved in
determining respiratory gas exchange, seem ineffective in determining heat
exchange.
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Acknowledgments |
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