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First published online March 2, 2006
Journal of Experimental Biology 209, 1052-1057 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02121
Metabolic and blood gas dependence on digestive state in the Savannah monitor lizard Varanus exanthematicus: an assessment of the alkaline tide
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697-2525, USA
* Author for correspondence at present address: Wright State University, Neuroscience, Cell Biology, and Physiology, 3640 Colonel Glenn Highway, Dayton, OH 45435, USA (e-mail: lynn.hartzler{at}wright.edu)
Accepted 24 January 2006
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Summary |
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O2 and
CO2 were measured
continuously and arterial pH, blood gases and strong ions were measured every
8 h for 5 days. During peak digestion (24 h post feeding),
O2 and
CO2 increased to
approximately threefold fasting values
(O2, 0.95–2.57 ml
min–1 kg–1;
CO2 0.53–1.63 ml
min–1 kg–1) while respiratory exchange ratio
(R) remained constant (0.62–0.73). During digestion, arterial
PCO2 increased (from 4.6 kPa to 5.8 kPa), and
[HCO3–] also increased (from 24.1 mmol
l–1 to 40.3 mmol l–1). In contrast to early
studies on crocodilians, arterial pH in V. exanthematicus remained
relatively stable during digestion (7.43–7.56). Strong ions contributed
little to the acid–base compensation during the alkalosis. Collectively
the data indicate that the metabolic alkalosis associated with H+
secretion (as indicated by increased plasma bicarbonate) is partially
compensated by a respiratory acidosis.
Key words: Varanus exanthematicus, feeding, specific dynamic action, arterial blood gases, alkaline tide, acid–base balance, metabolic rate, pH
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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O2) during digestion that
is as large as that achieved during activity
(Andrade et al., 1997
;
Hicks et al., 2000;
Secor and Diamond, 1995;
Secor et al., 2000). While the
metabolic level reached during these two physiological challenges is similar,
there are considerable temporal differences in their development. During
exercise, reptiles immediately respond with an increase in metabolic rate,
which then returns to resting levels shortly after cessation of exercise
(Garland et al., 1987;
Wagner and Gleeson, 1997;
Wang et al., 1997). This
pattern differs from digestive metabolic responses which take hours to develop
and have an extended duration lasting days
(Coulson et al., 1950a;
Coulson et al., 1950b;
Hicks et al., 2000;
Jorgensen, 1992;
Secor et al., 2000). The
increased O2 associated
with digestion has been attributed primarily to the preparation of the gut for
digestion via protein synthesis and secretion of digestive compounds
(Andrade et al., 1997;
Secor and Diamond, 1995),
including acid secretion by the stomach
(Secor, 2003).
Cardiopulmonary studies during digestion in two species of reptiles
(Glass et al., 1979;
Hicks et al., 2000;
Secor et al., 2000) found a
relative hypoventilation during digestion in comparison to either rest or
activity.
The postprandial response is also associated with alkalization of the
blood, known as the alkaline tide. Recent studies in alligators, pythons and
boas reexamined the postprandial changes in pH
(Andrade et al., 2004;
Busk et al., 2000b;
Overgaard et al., 1999) and
found a significant increase in plasma [HCO3–], an
increase in O2 but no
significant change in arterial pH. However, these reptiles rely on anaerobic
metabolism to a large extent, so to test the generality of the postprandial
metabolic and acid–base response in reptiles it is necessary to examine
a reptile species that has a relatively high aerobic capacity. The present
study investigated the acid–base response during specific dynamic action
(SDA) in another large carnivorous reptile, the Savannah monitor lizard,
Varanus exanthematicus. Savannah monitor lizards belong to a group of
reptiles with activity levels higher than most other reptilian groups, and
they have the capacity to maintain relatively high rates of aerobic metabolism
(Wood et al., 1978). We
measured the magnitude and time course of the metabolic response, blood gases,
strong ions and acid–base balance associated with the postprandial
metabolic response in Savannah monitor lizards.
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Materials and methods |
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Surgery
Animals were fasted for at least 3 weeks prior to surgery and
experimentation. Animals were anesthetized by exposure to isoflurane (Isoflo:
Abbott Laboratories, North Chicago, IL, USA). Lizards were then artificially
ventilated with 2% isoflurane via a vaporizer (Dräger, Lubeck, Germany).
A femoral artery was occlusively cannulated with heparin-soaked, saline filled
PE-50 or PE-60 tubing (Harvard Apparatus, Inc., Holliston, MA, USA). To reduce
the risk of infection and post-surgical pain, antibiotics and analgesics were
administered immediately after surgery and every second day post-surgery
(Enrofloxacin; Baytril, Bayer Corporation, Shawnee Mission, KS, USA and
Flunixin meglumine; Flunixamine, Fort Dodge, Madison, NJ, USA, respectively).
Following surgery all animals resumed voluntary breathing and were allowed to
recover for at least 18 h in an 8-l plastic box in a walk-in environmental
chamber set at 35°C.
Protocol
Fasting animals were placed in an 8-l metabolic chamber fashioned from a
Rubbermaid box, which was placed in a temperature-controlled room at 35°C
(preferred body temperature of this species)
(Hicks and Wood, 1985). Room
air was pulled serially through the metabolic chamber, a Drierite (anhydrous
calcium sulfate; Xenia, OH, USA) column to remove water vapor, a flow meter,
and oxygen and carbon dioxide gas analyzers (model S3A, Applied
Electrochemistry, Inc., Sunnyvale, CA, USA and model LB2, Beckman, Schiller
Park, IL, USA) at an average flow rate of 240±2 ml
min–1 with a vacuum pump. Oxygen consumption
(O2) and carbon dioxide
excretion (CO2) were
monitored using AcqKnowledge data acquisition software (Biopac Systems, Inc.
Goleta, CA, USA) and converted to STPD. A second group of lizards
was used to measure arterial pH (pHa), blood gases and strong ions.
Fasting values were measured before each meal. Blood samples were taken every
8 h post-feeding, and measurements were made using a Nova blood gas analysis
system (Waltham, MA, USA). Blood gases and pH values were corrected for
temperature using correction curves that were generated for V.
exanthematicus blood as follows. Blood from V. exanthematicus
was equilibrated over a range of oxygen and carbon dioxide tensions. Samples
of this blood were then measured both by the Nova blood gas analysis system
and by a Radiometer blood gas analysis system (Copenhagen, Denmark) that was
thermostatted to the animal's body temperature (35°C). The differences in
values between these two measurement systems were used to correct for the
temperature difference between the animal's body temperature and the
temperature at which the blood sample was measured in the Nova blood gas
analysis system. Plasma bicarbonate concentration
([HCO3–]) was calculated from the
Henderson–Hasselbalch equation
([HCO3–]=
PCO2x
10(pH–pK')) using simultaneously determined pH and
PCO2; and pK' were corrected for temperature
and pH (Boutilier et al.,
1984). Following the fasting period, the animals were removed from
the chamber and offered 10% of their body weight in rat pups; each animal ate
readily within 10 min. After feeding, the animal was returned to its chamber,
and metabolic rate was measured continuously and 0.2 ml blood samples were
taken every 8 h post-feeding for 5 days. After each measurement cannulae were
refilled with a 100 IU ml–1 heparin saline solution
(Elkins-Sinn, Inc., Cherry Hill, NJ, USA).
Statistical tests
Repeated measures analysis of variance (ANOVA; Dunnett Test for Multiple
Comparisons vs Control Group) was used to analyze time course data
(Graphpad Software, San Diego, CA, USA). Levels of significance were assumed
with P values less than 0.05. Values are reported as means ±
standard error of the mean (s.e.m.); N=6 unless otherwise noted.
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Results |
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O2 of V.
exanthematicus increased from a fasting level of 0.95±0.19 ml
min–1 kg–1 to 2.57±0.85 ml
min–1 kg–1 24 h post-feeding
(Fig. 1A). This increase in
O2 began within 4 h post
feeding, and reached a maximum at 24 h postprandial, remaining elevated above
fasting values until 114 h postprandial. Carbon dioxide excretion exhibited a
similar pattern to that of oxygen consumption with
CO2 increasing from a
fasting level of 0.53±0.31 to 1.63±0.58 ml
min–1 kg–1 24 h postprandial, and remaining
elevated until 114 h postprandial (Fig.
1B). Consequently, respiratory exchange ratio (R) did not change
during the course of digestion (Fig.
1C), with a mean value of 0.62±0.21 prior to feeding and
0.73±0.18 24 h postprandial.
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Blood gases, pH and strong ions
A significant increase in pHa was measured at 8 h after feeding
(7.43±0.03 to 7.51±0.03) with an apparent peak in the alkaline
tide at 40 h postprandial (7.56±0.04). pHa was no longer
significantly elevated by 56 h postprandial
(Fig. 2A). Bicarbonate levels
in the arterial blood increased from 24.1±2.6 mmol l–1
fasted to 34.6±2.4 mmol l–1 by 8 h postprandial with
an apparent peak at 40 h postprandial (40.34±5.3 mmol
l–1). Bicarbonate was no longer significantly elevated by 64
h postprandial (Fig. 2B). The
increase in pHa resulting from the increase in bicarbonate was
reduced by a significantly increased PaCO2
(5.7±0.2, 5.7±0.2, 5.8±0.4 kPa at 24, 32 and 48 h,
respectively) compared to the fasted state (4.6±0.2 kPa;
Fig. 2C). Throughout the
postprandial period, PaO2 did not significantly change
(Fig. 2D). Hematocrit was
significantly elevated at 24 and 32 h postprandial (0.23±0.01 and
0.23±0.01, respectively) compared to the fasted state
(0.2±0.01), data not shown. A significant increase in plasma lactate
concentration was measured at 24 and 32 h (1.2±0.2 and 1.3±0.3
mmol l–1, respectively) compared to fast levels
(0.3±0.1 mmol l–1;
Fig. 3A). Chloride
significantly decreased between 24 and 48 h postprandial (115.7±1.9
mmol l–1 at 24 h, 113.8±2 mmol l–1 at
32 h, 115.6±2.9 mmol l–1 at 40 h, 115.7±3.6
mmol l–1 at 48 h) compared to fast (122±1.9 mmol
l–1; Fig. 3B).
An increase in sodium was measured at 32, 40 and 48 h postprandial
(152.5±2, 150.6±1.5 and 150.7±2.4 mmol
l–1, respectively) compared to fast (144.7±1.7 mmol
l–1; Fig. 3C).
Potassium levels did not change during the postprandial period
(Fig. 3D).
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Discussion |
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O2
(Busk et al., 2000b;
Hicks et al., 2000;
Overgaard et al., 1999;
Secor and Diamond, 1995), and
the postprandial rise in O2
reported here is consistent with previous studies on V.
exanthematicus (Fig. 1)
(Hicks et al., 2000). While
there was a clear metabolic elevation and an alkaline tide following feeding
during this study, the alkalemia did not approach the magnitude previously
reported in Alligator mississippiensis
(Coulson et al., 1950b). The
smaller increase in pH is similar to those reported in recent studies of
Python molurus (Secor and
Diamond, 1995) and Boa constrictor
(Andrade et al., 2004), but
higher than that reported for A. mississippiensis or Python
molurus (Busk et al.,
2000b; Overgaard et al.,
1999), suggesting that the magnitude of the alkaline tide varies
amongst carnivorous reptiles.
Metabolic response: fasted vs fed
Elevation in metabolic state typically accompanies digestion in vertebrates
with both the increment and duration of the increase varying among species,
type of forager, and relative meal size
(Andrade et al., 1997;
Coulson et al., 1950b;
Hicks et al., 2000;
Preest, 1991;
Secor and Diamond, 1995;
Secor and Diamond, 1997;
Secor and Phillips, 1997;
Secor et al., 1994;
Wang et al., 1995). Reptiles
are extreme with regard to metabolic changes during digestion ranging from as
high as 44 times standard metabolic rate
(Secor and Diamond, 1997) to
this study where the increase in
O2 of V.
exanthematicus was much less (threefold increase) than that seen in
P. molurus. As indicated by the consistency of the respiratory
exchange ratio, increases in
CO2 paralleled those of
O2
(Fig. 1C). The time course for
the postprandial metabolic response is consistent among reptiles with a peak
in SDA at 24 h after feeding, lasting about 5 days
(Andersen and Wang, 2003;
Busk et al., 2000a;
Busk et al., 2000b).
Time course of the acid-base response: fasted vs fed
In addition to the metabolic response, pHa increased during
digestion in V. exanthematicus; the apparent highest mean value
occurred 40 h post-feeding (Fig.
2). Arterial pH peaks before metabolic rate (40 h vs 24
h). In A. mississippiensis the highest postprandial pHa
was measured at 9 h (Coulson and Hernandez,
1983). Overgaard et al.
(Overgaard et al., 1999) also
reported a peak in pHa before 12 h while maximal
O2 of P. molurus
did not occur until 48 h postprandial. In this study, pHa was
significantly increased from fasting values by 8 h postprandial and remained
elevated until 56 h postprandial.
Blood gas response: fasted vs fed
As illustrated in Figs 2 and
5, feeding elicits an increase in PaCO2 and
[HCO3–], and no change in
PaO2. An increase in PaCO2 has also
been reported for A. mississippiensis
(Busk et al., 2000b), P.
molorus (Overgaard et al.,
1999), B. constrictor
(Andrade et al., 2004), and
Bufo marinus (Andersen and Wang,
2003). In mammals, an increase in PaCO2 is
associated with a reduction in arterial PaO2. This inverse
relationship is due to the tight coupling of ventilation and metabolic rate as
expressed in the alveolar ventilation equation. However, reptiles do not
necessarily follow this pattern (Wang et
al., 1998). PaO2 could be increased or
unchanged by improving ventilation perfusion
(V/
) inhomogeneity or by
decreasing the intrapulmonary or intracardiac shunt. Increase in
PaCO2 could be achieved by a relative hypoventilation as
has been shown in a previous study of the cardiovascular and ventilatory
response to digestion in V. exanthematicus
(Hicks et al., 2000). This
hypoventilation is seen as a decrease in air convection requirement for
CO2 and probably represents changes in postprandial ventilatory
control.
Strong ions
Chloride and bicarbonate exhibited the most pronounced changes after
feeding, although sodium and lactate also both increased. A significant
increase in lactate concentration (Fig.
3A) during the postprandial period was also seen Scincella
lateralis (Preest, 1991),
and A. mississippiensis (Busk et
al., 2000b), but not in Rana catesbeiana
(Busk et al., 2000a), B.
marinus (Andersen and Wang,
2003) or P. molorus
(Overgaard et al., 1999).
Although this study measured a fourfold increase in lactate postprandially,
the actual contribution of lactate to the total anion concentration is very
small. The greatest changes in plasma electrolyte concentration were the
decrease in chloride (secreted into the lumen of the stomach to form HCl) and
the accompanying increase in bicarbonate, and, hence, the alkaline tide (Figs
2A,B,
3B). A similar decrease in
chloride during the postprandial period was reported for B. marinus
(Andersen and Wang, 2003),
R. catesbeiana (Busk et al.,
2000a) and A. mississippiensis
(Coulson et al., 1950b).
However, no change was reported in chloride concentration for A.
mississippiensis in another study
(Busk et al., 2000b), and an
increase in chloride was reported for P. molorus
(Overgaard et al., 1999).
An assessment of the alkaline tide and postprandial metabolic response
This study has delineated the changes in metabolic function as well as
blood gases and acid-base status that accompany feeding in V.
exanthematicus. There is some variation in the acid-base response to
feeding in reptiles and amphibians. Some studies have reported a large
increase in pH (Coulson et al.,
1950b; Secor and Diamond,
1995), some a moderate increase in pH
(Andrade et al., 2004;
Busk et al., 2000a), and some
no change in pH (Andersen et al.,
2003; Andersen and Wang,
2003; Busk et al.,
2000b; Overgaard et al.,
1999) during the postprandial period. While it appears that there
is a different response to feeding, it is rather the fasted pH values that
differ most strikingly between studies. For example, fasted pH was found to be
7.36 in an early study on alligators
(Coulson et al., 1950b), and
7.51 in a more recent study (Busk et al.,
2000b) whereas postprandial pH in both studies was approximately
7.57; similarly, fasted pH was 7.39 in an early study on the python
(Secor and Diamond, 1995), and
7.52 in a more recent study (Overgaard et
al., 2002) whereas postprandial pH was 7.49 and 7.53,
respectively. Each of the studies discussed above showed a significant
increase in bicarbonate during the postprandial period, but the impact of the
alkaline tide on the acid–base status of the animal is varied by that
animal's ventilatory response (Wang et
al., 2001). The response to an increase in bicarbonate
post-feeding in V. exanthematicus is an initial metabolic alkalosis
followed by a relative hypoventilation, a return to fasting pH levels, and a
return to fasting PaCO2
(Fig. 4). The same response has
been reported for B. constrictor
(Andrade et al., 2004), and
B. marinus (Andersen and Wang,
2003); however, A. mississippiensis showed a relative
hypoventilation prior to a small metabolic alkalosis
(Busk et al., 2000b).
|
)
proposed that 55% of the metabolic cost of digestion can be attributed to the
production of HCl and other gastric functions related to breakdown of the food
bolus. This study measured an increase in oxygen consumption up to 5 days
after feeding (Fig. 1A). Part
of this cost includes the secretion of hydrogen ions into the lumen of the
stomach via the H+,K+-ATPase, however, in the
present study it appears that H+ secretion does not continue past 3
days (Fig. 2). Blocking this
H+,K+-ATPase
(DiPalma, 2001) should give an
estimate of the relative cost of H+ transport. However, while
omeprazole successfully blocked the alkaline tide in B. constrictor,
the postprandial increase in metabolic rate was indistinguishable from
untreated animals (Andrade et al.,
2004). This result suggests that the cost of H+
transport is negligible in terms of the overall cost of digestion in B.
constrictor. Other processes contributing to the cost of digestion
include protein synthesis (Coulson and
Hernandez, 1971; McCue et al.,
2004), biosynthesis (mass) and nutrient transport
(Secor and Diamond, 1995);
however, the cost of increasing intestinal mass has been called into question
by more recent studies (Overgaard et al.,
2002; Starck and Beese,
2001; Starck and Beese,
2002) leaving the attribution of costs associated with digestion
an open and interesting question.
Conclusion
It is concluded that carnivorous reptiles develop a metabolic alkalosis
during digestion. Recent studies of alligators, pythons, toads and boas, as
well as this study on monitor lizards, support the hypothesis that this
metabolic alkalosis is partially or completely compensated by a respiratory
acidosis (Andersen and Wang,
2003; Busk et al.,
2000b; Coulson et al.,
1950b; Hicks et al.,
2000; Overgaard et al.,
1999; Wang et al.,
2001). The degree of compensation may explain the variability of
the pH change during digestion in different species; however, why there are
different degrees of compensation remains unclear.
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Acknowledgments |
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Footnotes |
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Present address: Discipline of Physiology and Pharmacology, School of
Veterinary and Biomedical Sciences, James Cook University, Townsville, QLD
4811, Australia 
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References |
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