Effects of swimming on metabolic recovery from anoxia in the painted turtle
Department of Molecular Pharmacology, Physiology and Biotechnology, Brown University, Box G, Providence, RI 02912, USA
* Author for correspondence (e-mail: Daniel_E_Warren{at}brown.edu)
Accepted 11 May 2004
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Summary |
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Key words: active recovery, anoxia, Chrysemys picta bellii, lactate, reptile, swimming, turtle
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Introduction |
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Vertebrate lactate metabolism is best understood under conditions following
exhaustive exercise. Within vertebrates, the fate of lactate varies across
class. The traditional view is that lactate is primarily oxidized in mammals
(Brooks and Gaesser, 1980),
although recent evidence indicates this might not be clearcut
(Fournier et al., 2002
).
Fishes and reptiles (Gleeson,
1996
), including turtles following anoxic submergence
(Jackson et al., 1996
),
convert most of the lactate load back to glycogen in muscle and liver. It has
been suggested that any difference in lactate clearance strategy is due to the
marked differences in metabolism between ectotherms and endotherms, and,
specifically, that the lower metabolic rate of ectotherms limits the
proportion of the lactate load that can be oxidized
(Gleeson and Dalessio,
1989
).
Within mammals, moderate aerobic exercise after a bout of exhaustive
exercise, termed active recovery, results in an enhanced rate of lactate
disappearance from blood (Ahmaidi et al.,
1996; Bangsbo et al.,
1994
). The mechanism for enhanced lactate clearance during active
recovery is thought to be increased lactate oxidation, which generates ATP to
help sustain the exercise. Active recovery following lactic acid accumulation
by strenuous exercise has also been shown to enhance metabolic recovery in
trout (Milligan et al., 2000
),
although the suggested mechanism is thought to be related to the inhibitory
effects of cortisol on glycogen repletion in muscle
(Milligan, 2003
). The effect
of active recovery has yet to investigated in reptiles recovering from lactic
acidosis or any animal recovering from hypoxia or anoxia.
In this experiment, we tested the hypothesis that elevated recovery
metabolism, through 12 h of continuous aerobic exercise at
23x resting oxygen consumption rate
(O2), would
increase the rate of lactate disappearance from plasma following 2 h of anoxic
submergence in the Western painted turtle Chrysemys picta. Oxygen
consumption and carbon dioxide production rates as well as blood
acidbase status were monitored at rest and throughout the recovery
period. The results of these experiments reveal the relative importance of
active recovery in modulating metabolic processes in turtles following anoxic
submergence and demonstrate how recovery from exhaustive exercise and anoxic
submergence are affected by a similar alteration in metabolic state.
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Materials and methods |
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Training protocol
Prior to experiments (Days 114), turtles were divided into two
groups: trained and untrained. Trained animals were swum in a flume similar in
design to that used by Prange
(1976) (see
Fig. 1) for 40 min each day for
2 weeks at speeds ranging from 10.613.7 cm s1. During
this time, they learned to swim in the flume and to breathe from a chamber
built at the front of a lid covering the surface of the swimming area (see
Fig. 1). This range of speeds
was chosen to ensure that the animal would swim throughout the entire training
session. The lid prevented the animal from breathing anywhere except in the
chamber, where expired gases could be collected for determination of oxygen
consumption and carbon dioxide rates during recovery from anoxia as described
below. The untrained animals were placed in the flume for the same amount of
time and learned to find the breathing chamber, but were not made to swim
against a current.
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Catheterization
On day 15, all turtles were anesthetized with isoflurane and catheterized
(PE50, Intramedic) occlusively in the right carotid artery through a 2.5 cm
hole cut through the right pectoral scute of the plastron using a trephine.
The catheter was led out the side of the neck through a small hole and filled
with 20 IU ml1 heparinized 0.8% NaCl solution. An acrylic
plug was placed in the plastron hole and sealed with dental acrylic (Bosworth
Original Truliner, Stokie, IL, USA). The animals were fully recovered
13 h after plug sealing, placed in 20 liter buckets with approximately
25 cm of water and allowed to recover overnight. The following day (Day
16), the turtle was fixed with adhesive tape to a brick and placed in a water
bath at 25°C filled just high enough to completely cover the carapace
without preventing access to air. The fixing of the animal served two
functions: first, to prevent the animal from swimming around the water bath.
Second, to allow for a chamber to be lowered over the area on the water's
surface above the turtle's head so that when it raised its head to breathe, it
exchanged gases with a bias flow that passed through the chamber. The bias
flow was analyzed for O2 and CO2 (see further details
below). The animal was allowed to acclimate to the temperature and chamber
overnight.
Experimental protocol
The experimental protocol was approved by the Brown University
Institutional Animal Care and Use Committee (IACUC). Resting oxygen
consumption (O2)
and carbon dioxide production
(
CO2) rates were
measured for at least 1 h, after which a 0.6 ml blood sample was obtained for
analysis of arterial blood PO2,
PCO2, pH and plasma glucose and lactate. The
brick and turtle were then tipped onto their sides, the weight of the brick
anchoring the turtle to the bottom of the chamber and preventing it from
reaching the surface to breathe. Previous work in red-eared sliders
Trachemys scripta (Belkin,
1968
) has established that cutaneous oxygen consumption at
22°C is a negligible fraction of the total oxygen demand, making it
unnecessary to bubble the surrounding water with nitrogen to induce anoxia.
After 2 h, the turtle and brick were righted so that the animals could resume
breathing from the chamber to begin the recovery period. At this point,
O2 and
CO2 measurements
were also resumed. The arterial blood sample was taken after the first breath
to obtain the most accurate measurement of plasma lactate at the start of
recovery. As a consequence, an end anoxia arterial
PO2 measurement was not obtained. After the 1 h
recovery blood sample, the turtle was transferred to the flume and either swum
for 1 or 2 h (1 h active and 2 h active, respectively) at 12.112.9 cm
s1 or did not (passive/trained and passive/untrained
groups). The passive/trained group was used to determine if the 14 days of
training affected any of the recovery parameters. The 12 h swimming
period was chosen because we determined from a preliminary experiment, in
which a turtle was swum for 6 h after 2 h of anoxia and 1 h of recovery, that
12 h would be adequate time to see a potential difference while cutting
down on the already heavy logistical demands associated with the continuous
attending to the turtle during the swimming period.
O2 and
CO2 measurements
were recorded throughout the remainder of the recovery period (10 h total, 9 h
in the flume). Blood samples were withdrawn and analyzed 1, 3, 6 and 9 h after
transfer to the flume. An additional blood sample was taken at 2 h after
transfer to the flume in the 2 h active group, but was only analyzed for
plasma lactate. The flume temperature remained at 25.0±0.3 °C
throughout recovery.
Blood analysis
All blood samples were drawn into glass syringes and placed on ice for no
more than 1 h prior to analysis. Approximately 0.2 ml of the blood was used to
measure PO2,
PCO2 and pH (Radiometer PHM 73 pH/Blood Gas
Monitor and BMS3 Mk2 Blood Microsystem thermostatted to 25°C; Copenhagen,
Denmark). The remaining blood was placed in a 1.5 mlmicrocentrifuge tube,
centrifuged at 9300 g for 3 min and lactate and glucose levels
measured on the plasma (YSI 2300 Statplus, Yellow Springs, OH, USA). Blood
HCO3 concentrations were calculated using the
HendersonHasselbach equation using pK'=6.153 as interpolated from
Reeves (1976) and
CO2=0.0404 from Severinghaus
(1965
).
Metabolic rate measurements
O2 and
CO2 were
measured using standard flow-through respirometry techniques
(Withers, 1977
). As indicated
above, for the resting and first recovery hour measurements, the turtles
breathed from a chamber that had been lowered over the surface of the water
directly above the turtle's head, through which a bias flow passed. Once the
turtles were transferred to the flume, the bias flow was diverted through the
chamber, from which the turtles had learned to breathe during the training
sessions. Chamber bias outflows passed through Drierite and a portion was
pumped (AEI model R-2; Pittsburgh, PA, USA) through a carbon dioxide analyzer
(AEI model CD-3A) and an oxygen analyzer (AEI model S-3A). Gas meter outputs
were recorded and analyzed using the BIOPAC MP100 and Acknowledge data
acquisition software (Goleta, CA, USA). Bias flows were measured at the end of
each experiment (Vol-u-meter, Brooks Instruments, Hatfield, PA, USA) and
ranged from 210350 ml min1. The average gas fractions
were determined from the integral divided by the time integrated for each gas
at each time point and a minimum of three breathing episodes was used for each
of the calculations. The whole of each of the first 3 h recovery time was
integrated while the integrated signals for the resting, 4, 7 and 10 h
recovery times ranged from 4.589.3 min. The following equations from
(Otis, 1964
) were used to
calculate
CO2,
respiratory exchange ratio (RE) and
O2:
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Statistical analysis
Data were analyzed by two-way repeated measures multivariate analysis of
variance (RM-MANOVA) to determine if swimming or training affected each
parameter over time. Student's t-tests were used to elucidate any
time effects or treatment x time interactions. A difference was
considered significant if P<0.05. All statistical computations
were carried out using JMP 4.0.4 (SAS Institute).
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Results |
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Carbon dioxide production rate
(CO2) was
elevated 56x than the resting value during the first hour of
recovery in all animals (Fig.
2B) and returned to the resting value in passive animals by the
end of the second hour.
CO2 remained
elevated during the swimming periods in both the 1 and 2 h active groups,
although it was only 23x the resting value.
CO2 returned to
resting levels soon after the end of the swimming periods in both active
groups.
Respiratory exchange ratio (RE) (Fig. 2C) was significantly elevated after the first swimming hour in all groups. The trained/passive recovery group had a significantly higher RE than both the 2 h active and passive/untrained groups during the first recovery hour and was significantly lower than resting values during the second recovery hour. RE returned to resting levels in all other groups during the second recovery hour and was unaffected by swimming or training.
Blood
Swimming and training did not affect the recovery of arterial
PCO2, pH or plasma
[HCO3] (Fig.
3). They also had no effect on plasma lactate and glucose or
arterial PO2
(Table 1).
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Arterial PCO2 (Fig. 3A) was significantly higher than resting values at the start of the recovery period and then fell significantly below them after 1 h. It gradually increased during the remainder of the recovery period and was higher than resting values by 7 h.
Arterial pH (Fig. 3B) was significantly lower than resting at the start of recovery, was restored to resting values after 1 h, and fell slightly but significantly in all groups below resting until 10 h.
Plasma [HCO3] (Fig. 3C) was significantly lower at the start of recovery than at rest and was fully restored by 4 h. By 10 h, blood [HCO3] was slightly but significantly greater than resting values. Apparent differences between the 2 h active group and the other treatments at various time points results from this group having a generally higher plasma [HCO3] (a treatment effect) and is not due to an effect of the swimming (treatment x time interaction).
Arterial PO2 (Table 1A) was variable, tended to increase until 1 h, and then steadily decreased until it became significantly lower than resting values at 7 and 10 h.
Plasma lactate and glucose (Table 1B,C, respectively) peaked at the start of recovery and steadily declined until returning to resting values at 10 h. Because of the variability in the lactate accumulation after submergence (mean=21.0 mmol l1; S.D.=4.5 range=13.730.1) and because the rate of lactate disappearance for a given time period is dependent on the lactate concentration at the start of the period in question, we also expressed the recovery plasma lactate concentrations as a % change per hour from the previous time point (Fig. 4). This rate was highest during the first 2 h recovery than during the subsequent 6 h in all treatments except the passive recovery/trained group, indicating a biphasic pattern to the recovery process with respect to plasma lactate. The 2 hactive group had the fastest rate of decrease during the second hour, and was significantly higher than the other treatments at this time point and remained at these levels until the animals stopped swimming.
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Oxygen consumption versus lactate disappearance
To determine if there was any relationship between metabolic rate and the
rate of lactate disappearance, we plotted the percentage change in plasma
lactate concentration against
O2 for the
second recovery hour (first hour of swimming or not swimming) and for the
third and fourth recovery hours (second hour of swimming or not swimming + one
hour of not swimming) (Fig. 5).
The third and fourth recovery hours were pooled in this way because plasma
lactate data were not collected at the end of the third recovery hour in the 1
h active group or either of the passive groups. There was a significant
correlation between these two rates (P<0.001, r=0.52),
indicating that the rate of lactate disappearance is positively correlated
with metabolic rate.
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Discussion |
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Two hours of anoxic submergence at 25°C in painted turtles leads to a
significant acidemia, similar to that seen in the closely related red-eared
slider turtle in an anoxia experiment under similar conditions
(Jackson and Silverblatt,
1974). This acidemia is caused by a combined respiratory acidosis,
with mean arterial PCO2=47 torr (1 torr=133.3
Pa), and a metabolic acidosis, with mean plasma lactate elevated to 21 mmol
l1 and plasma [HCO3] depleted
to 18 mmol l1 from 31 mmol l1. These
lactate and HCO3 changes are equivalent to those
in iguanas and varanid lizards after exhaustive exercise at 35°C
(Gleeson and Bennett, 1982
).
Although the duration of anoxia in these experiments was long (2 h) compared
to the anoxia tolerance other vertebrates, turtles are known to recover from
up to 4 and even 7 h of anoxia at similar temperatures
(Jackson, 1968
).
Upon re-emergence, painted turtles hyperventilated for the first hour,
eliminating the respiratory acidosis and compensating for the lactic acidosis,
thereby restoring blood pH. These responses mirrored those of other reptiles
after exhaustive exercise (Gleeson,
1982,
1996
;
Gleeson and Dalessio, 1989
),
in which the RE values reach similar values for a similar duration. Both
varanids and iguanas recover much faster with respect to plasma lactate and
blood HCO3, requiring less than 1 h to return to
resting values, a difference we attribute partly to the higher recovery
temperatures in the lizard experiments. In addition, because anoxia is a
condition that affects all tissues whereas exercise involves primarily the
locomotory muscles, the anoxic turtles experienced a greater overall lactate
load that may also explain the prolonged elevations in plasma lactate
concentration. This lactate would continue to distribute to the extracellular
fluid from these tissues until, after conversion to pyruvate, it is either
converted back to glycogen or oxidized in the TCA cycle.
At the end of the first recovery hour, elevated plasma lactate levels did
not compromise the animal's ability to sustain moderate exercise, which
elevated O2
23x over the resting value during the swimming period. We cannot
state in absolute terms whether the anoxia diminished swimming capacity
because the variables in question were not measured during swimming in animals
that were not made anoxic. However, the purpose of the study was to determine
the effects of swimming on recovery processes, not the effects of anoxia on
swimming capacity.
This is the first study in reptiles where animals were exercised during recovery from metabolic acidosis of any kind and the first in any animal following hypoxia or anoxia. Swimming during recovery from anoxia-induced metabolic acidosis did not consistently affect the rate of plasma lactate disappearance (Fig. 4). Although the 2 h active group appeared to recover faster than both passive groups by the second and fourth hours of recovery, the 1 h active group was unaffected at the second hour. If swimming were a major modulator of the lactate recovery kinetics in painted turtles, we would have seen similar responses after the first hour of swimming between both active groups.
Because the metabolic recovery from exercise-induced lactic acidosis in
rainbow trout (Milligan et al.,
2000) and mammals (Bangsbo et
al., 1994
; Choi et al.,
1994
; Peters Futre et al.,
1987
) is enhanced by light to moderate exercise, we predicted a
more pronounced effect on plasma lactate disappearance in our turtles than the
one we observed. Despite a similar effect of exercise on the recovery
processes of fish and mammals after exercise, the mechanisms for the enhanced
recovery are very different between the two classes. In trout, swimming during
recovery decreases circulating cortisol, a hormone that inhibits glycogen
repletion from lactate in muscle, thereby hastening overall lactate clearance
(Milligan, 2003
). It is
unlikely, however, that corticosteroids play a major role in lactate
metabolism during recovery from anoxic submergence in turtles. Corticosterone
decreases during anoxia at 5°C in painted turtles and does not exceed
normoxic levels during recovery (Keiver et
al., 1992
) and lactate metabolism by lizard muscle is unaffected
by corticosterone (Gleeson et al.,
1993
).
The faster recovery in mammals is due to a combination of greater lactate
oxidation by moderately exercising muscle and enhanced clearance of lactate
from the sites of production by increased blood flow
(Gladden, 2000). The
correlation between the rates of lactate disappearance and oxygen consumption
(Fig. 5) suggests that this
mechanism might be working similarly in turtles. However, the weak correlation
between the two parameters and relatively high variability in the rate of
lactate disappearance from plasma potentially reflect the overlap of the two
complex processes, exercise and recovery from anoxia.
A number of factors could account for this variable recovery response of
the turtles to swimming. First, and simplest, is that lactate could have been
generated during the swimming period in some of the animals. We consider this
unlikely because all RE values were below 0.8, the
O2 values
reached during exercise were only 2030% of aerobic scope
(Gatten, 1974
), and the
exercise was sustainable for several hours.
A second explanation is that
O2 was not
significantly elevated long enough or high enough to have had a large effect
on lactate metabolism. We do not think that swimming the animals faster,
thereby elevating
O2, would have
had much of an effect because the 1 h active group, which had a slightly but
significantly higher
O2 than the 2 h
active group during the first hour of exercise, seemed to be affected less
(Fig. 4).Swimming the turtles
for a longer period, thereby maintaining elevated
O2 for a longer
duration, might have affected recovery more. The pattern of lactate decrease
in Fig. 4 supports this
hypothesis, although it appeared that the effectiveness of swimming at
maintaining a high rate of plasma lactate disappearance was beginning to
decrease, casting some doubt on how much a longer swimming period would have
enhanced recovery.
Third, it is possible that, in some animals, increased lactate oxidation
was offset by decreased lactate used for glycogen repletion in liver and other
tissues. This explanation is plausible because exercise decreases gut blood
flow in some fishes (Axelsson and Fritsche,
1991; Farrell et al.,
2001
), and if it occurred in our experiments, it could have
reduced hepatic gluconeogenesis from lactate, an important source of lactate
removal in turtles recovering from anoxia
(Jackson et al., 1996
).
A fourth explanation is that in some of the animals, the exercise altered
the proportions of the lactate load that were oxidized or used as a
gluconeogenic substrate, which would occur if the turtles were also using
fuels other than lactate to support aerobic ATP production during the
swimming, specifically fatty acids. Mammals use primarily fats during
continuous, low intensity exercise and carbohydrates during high intensity
exercise (Christmass et al.,
1999). In rainbow trout, fuel use is speed- and
temperature-dependent, with fats being the favored substrate at warmer
temperatures and at lower speeds (Kieffer
et al., 1998
). Ecological evidence supports this scenario as
painted turtles emerging from winter hibernation have been found to have 70%
of their glycogen stores depleted while only depleting 40% of their fat
(Crawford, 1994
). From this, it
is logical to think that turtles might be adapted to use fat to sustain
activity during recovery from anoxia without compromising replenishment of
precious glycogen stores. The low RE values observed in these experiments
support this hypothesis, although these are difficult to interpret because of
the high probability that the animals were retaining CO2 during
recovery. This is supported by the observation that the passive/trained group
had a RE significantly lower than resting values during the second recovery
hour (Fig. 3C).
These experiments also found that training had no effect on recovery. This
is not surprising as reptiles do not increase their aerobic capacity in
response to 8 weeks of endurance training
(Garland et al., 1987) and,
because our turtles were trained for only 2 weeks, there was probably not
sufficient time for any physiological changes to occur even if the potential
existed. In contrast, endurance-trained mammals recover more quickly than
untrained mammals from exercise-induced lactic acidosis
(Gladden, 2000
).
In conclusion, recovery metabolism in painted turtles after 2 h of anoxic submergence at 25°C is not affected by 1 or 2 h of moderate exercise. The rate of lactate disappearance is correlated with the metabolic state of the animal, but this correlation does not translate into a consistently faster recovery when metabolic rate is increased through swimming in these experiments. Future studies should investigate fuel utilization during recovery from anoxia in resting and elevated metabolic states and whether swimming can limit the liver's capacity for gluconeogenesis in turtles.
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Acknowledgments |
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