Postprandial exercise: prioritization or additivity of the metabolic responses?
Department of Ecology and Evolutionary Biology, University of California at Irvine, Irvine, CA 92697, USA
*e-mail: abennett{at}ci.edu
Accepted March 28, 2001
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: activity, digestion, exercise, lizard, maximal aerobic speed, maximal rate of oxygen consumption, oxygen consumption, postprandial, prioritization, reptile, specific dynamic action, symmorphosis, Varanus exanthematicus, ventilation.
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Both exercise and digestion independently increase rates of oxygen consumption (.O2). In many organisms, the magnitude of
.O2 during strenuous exercise greatly exceeds the specific dynamic action observed during digestion (Kleiber, 1975). However, in others, particularly in infrequently feeding reptiles, the metabolic scopes of exercise and digestion can be similar (Benedict, 1932; Secor and Diamond, 1995; Secor and Diamond, 1997). In Python molurus, for example, postprandial
.O2 values are equal to those of snakes engaging in maximal sustainable exercise (Secor et al., 2000). Reptiles therefore provide an ideal organismal system in which to study physiological prioritization because of the major energetic commitments, and potential conflicts, caused by exercise and digestion. What happens to oxygen consumption and transport when postprandial animals exercise? Is priority of oxygen transport accorded to exercise or to digestion, is it shared or is the capacity for
.O2 somehow increased to accommodate both (additivity)? Here, we study the pattern of oxygen transport during fasting exercise and postprandial exercise in the monitor lizard Varanus exanthematicus. This study is an extension of earlier observations (Hicks et al., 2000) on the cardiopulmonary physiology of this species during fasting exercise and during digestion at rest.
Graphical models of prioritization and additivity
We present graphical hypotheses concerning potential patterns of oxygen transport during postprandial exercise (Fig.1). These will be tested directly in the ensuing experiments. These hypotheses are each compared with known patterns (see Hicks et al., 2000) of .O2 during fasting rest, fasting exercise and postprandial rest (Fig.1A). As in most other animals during fasting exercise,
.O2 increases approximately linearly with exertion (in this case, speed of walking on a treadmill) to the maximal aerobic speed (MAS), the speed at which the maximal rate of oxygen consumption (
.O2max) is attained. Walking at speeds faster than MAS does not increase
.O2max and entails rapid exhaustion associated with extensive supplemental anaerobic metabolism. At rest, postprandial animals have a
.O2 elevated above fasting levels. The following are some potential outcomes for
.O2 during postprandial exercise which are compared with the pattern described above.
|
Priority to digestion (Fig.1C). During postprandial exercise, digestive metabolism continues unabated, leaving less aerobic metabolic scope for exercise. .O2max is the same as in fasting animals, but it is attained at a lower MAS with an attendant decrease in endurance.
Additivity (Fig.1D). The resting postprandial metabolic increment is maintained during exercise, increasing O2 by a similar amount at all levels of exertion.
.O2max is also increased by this increment, resulting in the same MAS and endurance as in fasting animals.
There are obviously also possible intermediate conditions among these three hypotheses, such as a shared prioritization between exercise and digestion. However, we believe that these hypotheses, with their clear and contrasting predictions concerning metabolic rates of exercising animals, MAS, .O2max and endurance, form a useful framework for data analysis, and one turns out to describe the experimental results precisely.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Measurement of ventilation and gas exchange
In the first set of experiments (N=8, mass 145170g), .O2 was determined using an open mask system (Gleeson et al., 1980; Mitchell et al., 1981a; Mitchell et al., 1981b; Thompson and Withers, 1997). Room air was drawn (at 300400mlmin-1) through a loose-fitting, lightweight acetate mask placed over the head of each animal. The expired air was dried (Drierite) and continuously monitored with an oxygen analyzer (Applied Electrochemistry; model S-3A). In the second set of experiments (N=5, mass 480900g), ventilation and gas exchange were directly measured using an experimental arrangement modified from Wang and Warburton (Wang and Warburton, 1995) and previously described in detail (Hicks et al., 2000). Briefly, short pieces of flexible gas-tight tubing were glued to both nostrils, fused on top of the head of the lizard and connected to a T-piece. This T-piece was, in turn, attached to gas-tight Tygon tubing at both ends. One end led to the oxygen analyzer, connected in series, while the other served as a reservoir. A flow pump (Applied Electrochemistry), connected in series with the gas analyzers, maintained a constant gas flow between the T-piece and the gas analyzer and, thus, provided continuous delivery of room air to the lizard. A pneumotachograph (8421 Series, 0-5 LPM, H. Rudolph, Inc.) was connected upstream relative to the T-piece. At this position, airflow decreased during exhalations, while inhalations caused increases in airflow. A Valendyne (MP-45-1-871) differential pressure transducer continuously monitored the resulting changes in pressure gradients across the pneumotachograph. At any given breath, the signal from the differential pressure transducer preceded that from the gas analyzer by approximately 2s.
The .O2 of single breaths was determined as the area below the baseline signal for room oxygen. The relationship between this area and gas exchange was determined by simulating exhalations with known gas compositions through the T-piece (which during experiments was connected to the nostrils of the lizard). Similarly, the expired tidal volume of single breaths was determined from the integrated flow signal from the differential pressure transducer. Again, the relationship between this integral and tidal volume (in ml) was quantified by injection of a range of gas volumes through the T-piece. All calibration procedures produced very tight correlations between injected gas volumes and integrated flow signal (r2>0.98) and were reproducible within a few per cent before, during and after experiments. In both sets of experiments, experimental variables were recorded on a computer using the Acknowledge (version 3.2.4) data-acquisition system (Biopac Inc., Goleta, CA, USA).
Experimental protocol
At least 18h prior to experimentation, animals were placed within a large climatic chamber maintained at 35°C, the preferred body temperature of this species (Hicks and Wood, 1985). A few hours before treadmill exercise, the lizard was placed on the treadmill, covered with a cloth and left undisturbed with the mask or tubing connected to the experimental apparatus. Immediately before running, pre-exercise ventilation and/or gas exchange rates were measured over a 60min period. Although the lizards quickly relaxed and remained quiescent when placed on the treadmill, these pre-exercise values do not represent true standard values. The exercise regime commenced with a walking speed of 0.25kmh-1, followed by 0.5, 0.75, 1.0, 1.25 and 1.5kmh-1 (in that order). Each tread speed was maintained for approximately 5min. The maximum speed is the highest at which the lizards were able to match the belt speed for at least 2min.
In the first experiment (N=8), only .O2 was measured, because the animals were too small for simultaneous measurements of ventilation with this apparatus. The second experiment (N=5) was identical in protocol except that ventilation was also monitored in these larger animals. In all animals, gas exchange and minute ventilation were measured and averaged during the last 23min of each level of exercise. Following exercise, gas-exchange rates and minute ventilation were measured for an additional 34min. On the following day, lizards were fed a mixture of Tegu and Monitor Food (Zoomenu, San Luis Obispo, CA, USA) and raw eggs equal to 20% of their body mass. The size of the postprandial metabolic increment is a direct function of meal size in this species (Hicks et al., 2000). This ration was previously shown to generate a maximal postprandial metabolic increment of approximately 2.5mlO2kg-1min-1 (Bennett et al., 2000). The animals were left undisturbed for 24h, and the exercise protocol was then repeated; the maximal postprandial metabolic increment occurs at 24h post feeding in this species (Hicks et al., 2000).
Data analysis
Oxygen consumption measurements are corrected to STPD conditions; ventilation volumes are corrected to BTPS conditions. Except as noted, data are analyzed using paired (by individual, fasting versus postprandial) t-tests. Data are reported as means ± 1 S.E.M.. Significance is judged as P<0.05.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The key to sustaining both exercise capacity and the postprandial metabolic increment is the increase in .O2max. The 18% increment was attained not by an increase in
.E but rather by an increase in O2 extracted from ventilated air; a similar pattern was previously found in exercising postprandial pythons (Secor et al., 2000). This greater extraction efficiency is reflected in hypoventilation during both rest and exercise. How might this increased oxygen extraction efficiency be attained? A variety of factors, singly or in combination, might at least theoretically be responsible for increased extraction. We regard the most likely factors to be decrements in shunts and/or lower mixed venous oxygen content. Shunts, both cardiac and pulmonary, occur extensively in reptiles under a variety of circumstances (for a review, see Hicks, 1998). A right-to-left ventricular shunt diverts an average of 30% of mixed venous blood directly to the systemic arterial circulation in resting Varanus exanthematicus (Heisler et al., 1983). Decrement or abolition of this shunt could direct substantially more venous blood into the pulmonary circulation and increase oxygen uptake. Also, a reduction in right-to-left shunt leads to an increased arterial PO2 and a higher overall PO2 gradient for diffusion from the blood to the mitochondria. In addition, pronounced ventilationperfusion (V/
) heterogeneity and intrapulmonary shunt exist within the lungs of these animals. These factors contribute to a large gradient between faveolar PO2 and left atrial PO2 (a 4kPa PO2 gradient at rest and during exercise in Varanus exanthematicus) (Hopkins et al., 1995). During exercise, a reduction in areas of low V/
and in the intrapulmonary shunt would further increase oxygen extraction from ventilated air. Simultaneous measurements of PO2 of blood within the left and right atria and systemic arterial and venous circulation in fasting and postprandial animals, exercising and at rest, would clearly indicate whether shunts were decreasing in active or digesting animals. Additional pulmonary oxygen extraction could occur if mixed venous O2 content were lowered during postprandial exercise. Such a decrement might occur, depending on the relative flow and oxygen content of blood returning in the splanchnic and skeletal muscle circulation, if both systems were maintaining high metabolic rates. Measurement of mixed venous O2 content in fasting and postprandial animals, exercising and at rest, would indicate whether this is an additional source of increased pulmonary oxygen extraction. The increase in
.O2max may also be partially attributable to additional cardiovascular factors not measured in these experiments. For instance, maximal heart rate in exercising postprandial pythons exceeds that of either resting postprandial or exercising fasting animals (Secor et al., 2000). Only more detailed physiological studies can fully partition the mechanistic basis of the greater
.O2max.
The increment in .O2max in postprandial exercising animals (Fig.2) suggests that exercise alone does not elicit
.O2max. This conclusion follows similar observations on exercising postprandial pythons (Secor et al., 2000). These studies suggest that excess oxygen transport capacity in the cardiopulmonary system exists that is not accessed by maximal muscle activity. This result is a significant caveat to the use of exercise alone to define maximum oxygen transport capacities. It is also a significant challenge to the hypothesis of symmorphosis (Taylor and Weibel, 1981; Weibel et al., 1991), which proposes that organisms are efficiently designed without excess capacity. It should be recognized, however, that considerable structural and physiological plasticity exists during the postprandial state in reptiles, including upregulation of transport capacities within the intestine and, in some instances, an increase in organ size (Secor and Diamond, 1995; Secor and Diamond, 1997). It may be possible that, during the 24h postprandial period, the cardiopulmonary system has been sufficiently remodeled such that its transport capacity has been significantly increased. Only more detailed studies of the kinetics of the postprandial cardiopulmonary response can permit a determination of whether such changes, if they do occur, are sufficient to permit an 18% increment in
.O2max.
From a design point of view, then, what accounts for the apparent excess capacity of the cardiopulmonary system to transport oxygen? This is only excess capacity from the point of view of fasting exercise. Animals in nature may well have to exercise while digesting, and cardiopulmonary design may thus naturally have to accommodate postprandial exercise. A closely related species, Varanus albigularis, has been observed to be very active during its feeding and growth season, walking an average of 1.52kmday-1 (Phillips, 1995). In Varanus exanthematicus, if .O2max had not increased during the postprandial period and metabolic priority was accorded to digestion (Fig.1C), then MAS and endurance would have decreased. In this instance, assuming the average postprandial metabolic increment of 3.3mlO2kg-1min-1, MAS would have been reduced to between 0.5 and 0.75kmh-1, a value typical for lizards dependent principally on anaerobic metabolism to fuel higher-intensity exercise (Bennett, 1991; Bennett, 1994). Thus, to sustain high levels of aerobic activity, oxygen delivery systems may necessarily have to be designed to accommodate simultaneous elevated metabolic rates in two or more functional systems.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Benedict, F. G. (1932). The Physiology of Large Reptiles. Washington: Carnegie Institute Washington Publication 425.
Bennett, A. F. (1991). The evolution of activity capacity. J. Exp. Biol. 160, 123.[Abstract]
Bennett, A. F. (1994). Exercise performance of reptiles. Adv. Vet. Sci. Comp. Med. 38B, 113138.
Bennett, A. F., Hicks, J. W. and Cullum, A. J. (2000). An experimental test of the thermoregulatory hypothesis for the evolution of endothermy. Evolution 54, 17681773.[Medline]
Gleeson, T. T., Mitchell, G. S. and Bennett, A. F. (1980). Cardiovascular responses to graded activity in the lizards Varanus and Iguana. Am. J. Physiol. 239, R174R179.[Medline]
Heisler, N., Neumann, P. and Maloiy, G. M. O. (1983). The mechanism of intracardiac shunting in the lizard Varanus exanthematicus. J. Exp. Biol. 105, 1531.[Abstract]
Hicks, J. W. (1998). Cardiac shunting in reptiles: Mechanisms, regulation and physiological functions. In The Biology of the Reptilia, Morphology, vol. G, The Visceral Organs (ed. C. Gans and A. S. Gaunt), pp. 425483. Ithaca, NY: Society for the Study of Amphibians and Reptiles.
Hicks, J. W., Wang, T. and Bennett, A. F. (2000). Patterns of cardiovascular and ventilatory response to elevated metabolic states in the lizard Varanus exanthematicus. J. Exp. Biol. 203, 24372445.
Hicks, J. W. and Wood, S. (1985). Temperature regulation in lizards: Effects of hypoxia. Am. J. Physiol. 248, R595R600.
Hopkins, S. R., Hicks, J. W., Cooper, T. K. and Powell, F. L. (1995). Ventilation and pulmonary gas exchange during exercise in the savannah monitor lizard (Varanus exanthematicus). J. Exp. Biol. 198, 17831789.
Jackson, D. C. (1987). Assigning priorities among interacting physiological systems. In New Directions in Ecological Physiology (ed. M. E. Feder, A. F. Bennett, W. W. Burggren and R. B. Huey), pp. 310326. New York: Cambridge University Press.
Kleiber, M. (1975). The Fire of Life, revised edition. Huntington, NY: Krieger Publ. Co.
Mitchell, G. S., Gleeson, T. T. and Bennett, A. F. (1981a). Ventilation and acidbase balance during graded activity in lizards. Am. J. Physiol. 240, R29R37.[Medline]
Mitchell, G. S., Gleeson, T. T. and Bennett, A. F. (1981b). Pulmonary oxygen transport during activity in lizards. Respir. Physiol. 43, 365375.[Medline]
Phillips, J. A. (1995). Movement patterns and density of Varanus albigularis. J. Herpetol. 29, 407416.
Schultz, T. J., Christian, K. A. and Frappell, P. B. (1999). Do lizards breathe through their mouths while running? Exp. Biol. Online 4, 4.
Secor, S. M. and Diamond, J. (1995). Adaptive responses to feeding in Burmese pythons: pay before pumping. J. Exp. Biol. 198, 13131325.
Secor, S. M. and Diamond, J. (1997). Determinants of the postfeeding metabolic response of Burmese pythons, Python molurus. Physiol. Zool. 70, 202212.[Medline]
Secor, S. M., Hicks, J. W. and Bennett, A. F. (2000). Ventilatory and cardiovascular responses of pythons (Python molurus) to exercise and digestion. J. Exp. Biol. 203, 24472454.
Taylor, C. R. and Weibel, E. R. (1981). Design of the mammalian respiratory system. I. Problem and strategy. Respir. Physiol. 44, 110.[Medline]
Thompson, G. G. and Withers, P. C. (1997). Standard and maximal metabolic rates of goannas (Squamata: Varanidae). Physiol. Zool. 70, 307323.[Medline]
Wang, T. and Warburton, S. J. (1995). Breathing pattern and cost of ventilation in the American alligator. Respir. Physiol. 102, 2937.[Medline]
Weibel, E. R., Taylor, C. R. and Hoppeler, H. (1991). The concept of symmorphosis: A testable hypothesis of structurefunction relationship. Proc. Natl. Acad. Sci. USA 88, 1035710361.[Abstract]