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Am J Physiol Regul Integr Comp Physiol 288: R992-R997, 2005. First published December 2, 2004; doi:10.1152/ajpregu.00593.2004
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SLEEP AND TEMPERATURE REGULATION

Factorial scopes of cardio-metabolic variables remain constant with changes in body temperature in the varanid lizard, Varanus rosenbergi

T. D. Clark,1 T. Wang,2 P. J. Butler,3 and P. B. Frappell1

1Adaptational and Evolutionary Respiratory Physiology Laboratory, Department of Zoology, La Trobe University, Melbourne, Victoria, Australia; 2Department of Zoophysiology, University of Aarhus, Aarhus, Denmark; and 3School of Biosciences, University of Birmingham, Birmingham, United Kingdom

Submitted 30 August 2004 ; accepted in final form 25 November 2004


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The majority of information concerning the cardio-metabolic performance of varanids during exercise is limited to a few species at their preferred body temperature (Tb) even though, being ectotherms, varanids naturally experience rather large changes in Tb. Although it is well established that absolute aerobic scope declines with decreasing Tb, it is not known whether changes in cardiac output (b) and/or tissue oxygen extraction, (CaO2 – C), are in proportion to the rate of oxygen consumption (O2). To test this, we studied six Rosenberg's goannas (Varanus rosenbergi) while at rest and while maximally exercising on a treadmill both at 25 and 36°C. During maximum exercise both at 25 and 36°C, mass-specific rate of oxygen consumption (O2kg) increased with an absolute scope of 8.5 ml min–1 kg–1 and 15.7 ml min–1 kg–1, respectively. Interestingly, the factorial aerobic scope was temperature-independent and remained at 7.0 which, at each Tb, was primarily the result of an increase in bkg, governed by approximate twofold increases both in heart rate (fH) and cardiac stroke volume (VSkg). Both at 25°C and 36°C, the increase in bkg alone was not sufficient to provide all of the additional oxygen required to attain maximal O2kg, as indicated by a decrease in the blood convection requirement bkg/O2kg; hence, there was a compensatory twofold increase in (CaO2 – ). Although associated with an increase in hemoglobin-oxygen affinity, a decrease in Tb did not impair unloading of oxygen at the tissues and act to reduce (CaO2 – C); both CaO2 and C were maintained across Tb. The change in O2kg with Tb, therefore, is solely reliant on the thermal dependence of bkg. Maintaining a high factorial aerobic scope across a range of Tb confers an advantage in that cooler animals can achieve higher absolute aerobic scopes and presumably improved aerobic performance than would otherwise be achievable.

metabolic rate; Fick equation; exercise; cardiac output; oxygen consumption; heart rate; stroke volume; reptile; goanna; oxygen extraction.

THE FACTORS THAT DETERMINE the rate of transfer of oxygen (O2) through the various steps of the circulatory system in vertebrates can be summarized by the equation describing the Fick principle:

(1)

where O2 is the rate of oxygen consumption, b is cardiac output [the product of heart rate (fH) and cardiac stroke volume (VS)], CaO2 and C are the O2 contents of arterial and mixed venous blood, respectively. The arterio-venous oxygen content difference, (CaO2 – C), depends both on the capacity of the blood to deliver and on the tissues to extract oxygen. Thus, for the vertebrate circulatory system, delivery of oxygen depends both on the properties of the heart as a pump and on the amount of oxygen carried to and from the tissues (2, 9, 10, 30). The pertinent structural parameters for the circulation are the amount of blood delivered by the pump per beat, or VS, and the oxygen-carrying capacity of the blood, that is, the amount of hemoglobin. It is well accepted that such structural parameters typically cannot be regulated or changed without morphogenetic processes, and this occurs only in response to chronically altered demand (21). In contrast, functional parameters such as fH and (CaO2 – C) can be regulated immediately in response to increased requirements for O2, within the limits established by parameters of diffusion and affinity of hemoglobin for O2.

Correspondingly, it has been shown that varanid lizards, including Varanus exanthematicus (7, 18, 41), V. mertensi (16), and V. gouldii (17) primarily utilize increases in fH and (CaO2 – C) to attain maximum O2 during exercise, though one species, V. spenceri, displayed similar proportional increases in b and O2 such that (CaO2 – C) remained constant (17). The majority of this literature is concerned with animals at their preferred body temperature (Tb; ~35°C) even though, as ectotherms, varanids naturally experience relatively large changes in Tb.

It is well documented for reptiles that a decrease in Tb is typically accompanied by a decrease both in fH and in the absolute aerobic scope (1, 5, 6, 8, 22, 40), although it is not known whether changes in b and/or (CaO2 – C) are in proportion to O2. It may be hypothesized that the increased hemoglobin-oxygen affinity with reduced Tb will impair unloading of O2 at the tissues and act to reduce (CaO2 – C). Certainly, in mildly hypothermic mammals (Tb ~ 30°C), there is evidence for a reduction in (CaO2 – C), but only under situations where O2 has become supply dependent (Ref. 32, and references within). Whether or not the leftward shift of the hemoglobin oxygen equilibrium curve associated with the decline in Tb is causal to the reduction in (CaO2 – C) remains contentious, though, as yet, this has only been studied by artificial manipulation of hemoglobin-oxygen affinity (19, 38).

The present study's objective was to characterize in a varanid lizard the effects of temperature on the cardio-metabolic responses to exercise, with the aim of deducing which circulatory parameter(s) might account for the reduced absolute aerobic scope at Tbs below preferred. Rosenberg's goanna (V. rosenbergi) was selected, as it lives in a cool temperate climate in South Australia and experiences marked daily and seasonal changes in the thermal environment. Although the Tb of active free-ranging animals is often maintained at 34–36.5°C [determined as the preferred Tb in the laboratory; (26)], marked changes in Tb in active animals have been documented on a daily and seasonal basis (seasonal Tb range 10–38°C) with a substantial portion of the year spent at temperatures that are well below preferred (12, 13, 35).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Data on the rate of O2 consumption, CO2 production (CO2), fH, and blood variables were obtained from six lizards with a mean body mass (Mb) ± SE of 1.31 ± 0.21 kg. The animals were obtained from Kangaroo Island, South Australia, kept in a temperature-controlled holding facility at La Trobe University for up to 20 days before use, exposed to a 12:12 photoperiod, fed twice a week and had unrestricted access to water. Experiments were conducted under the La Trobe University Animal Ethics Approval Number 99/42L. Food was withheld for 3 days before experiments to reduce influences on metabolism and acid-base balance associated with digestion (20). All animals were acclimated to an experimental temperature (25°C or 36°C) for at least 6 h and usually overnight before experimentation. This period of acclimation is sufficient as it is known that Tb, fH, and O2 of V. rosenbergi reach steady state after 2–3 h following approximately a 10°C change in ambient temperature (T. D. Clark, P. J. Butler, and P. B. Frappell, unpublished observation).

Rates of oxygen consumption and carbon dioxide production. Rates of O2 consumption and CO2 were determined by placing a lightweight (10 g), transparent and loose-fitting plastic mask over the head of the animal, thus enclosing the nose and mouth. The mask was fitted with an outlet tube through which air was drawn at a rate of 3–8 L/min by a pump, which was monitored by a mass flowmeter. A subsample of the air leaving the pump was passed through a drying column (Drierite, Xenia, OH) and analyzed for the fractional content of O2 and CO2 by gas analyzers (models S-3A/1 and CD-3A, respectively, Applied Electrochemistry, Pittsburgh, PA). The rates of O2 consumption and CO2 were calculated from airflow through the mask, and the difference between incurrent and excurrent fractional concentrations of dry air (see Refs. 15 and 16). Gas volumes are given at STPD.

Heart rate. Heart rate was obtained by attaching self-adhesive Ag/AgCl ECG electrode pads to the dorsal surface of the animal. One electrode was placed one side of the midline a few centimeters in front of the heart, and the other electrode was positioned on the opposite side several centimeters behind the heart. An earth electrode was also attached near the pelvis. The ECG leads were connected to an amplifier (BIO amp, ADInstruments, Castle Hill, New South Wales, Australia), and the output from this and from the gas analyzers was collected at 1 kHz (Powerlab 800, ADInstruments).

Catheterization and blood variables. Each animal was implanted with a catheter both in the venous and arterial sides of the circulation. The animals were initially anesthetized by ventilating them with a mixture of 5% halothane in air, and then maintained at 3.5% halothane throughout surgery. The right carotid artery and the right anterior jugular vein were exposed low in the neck and a polyethylene catheter (ID 0.58 mm, OD 0.96 mm) was implanted into each vessel, with that in the jugular vein being advanced several centimeters toward the right atrium to obtain mixed venous blood. The catheters were sutured in place, looped loosely to avoid tension, led to the exterior through a small hole on the dorsal surface of the animal just above the shoulders, filled with heparinized saline and sealed. The wound was closed with sutures. The surgical procedure lasted no more than 40 min, and the animals were allowed to recover for at least 24 h postsurgery. Arterial and mixed venous blood samples (denoted by the modifiers a and , respectively) were collected during rest and maximum exercise, and the samples were stored anaerobically on ice for no more than 30 min.

At the time of analysis, the blood was remixed and analyzed for a number of variables. Partial pressures of oxygen and carbon dioxide (PO2 and PCO2, respectively) and pH were determined at the appropriate temperature by a blood gas analyzer system (models PHM 73 and BMS 3 Mk 2, Radiometer, Denmark); the electrodes were calibrated at each temperature with appropriate gas mixtures or buffers. Oxygen content was measured using a galvanic cell (Oxycon, University of Tasmania, Tasmania, Australia), lactic acid concentration using an Accusport analyzer (Boehringer Mannheim, Mannheim, Germany) and hemoglobin concentration [Hb] spectrophotometrically (Roche, kit number 124 729/MPR 3). A 70-µl blood sample was centrifuged for 4 min in a microcapillary to determine hematocrit (Hct).

On another occasion during the experimental period, a 2-µl blood sample was collected from each animal and oxygen equilibrium curves determined on a modified Hem-O-Scan (Aminco Instruments) at 25°C and 36°C, and at PCO2s of 3.20 and 5.60 kPa. These PCO2s were chosen because they are within the range of blood PCO2s typically reported for varanids (16). The P50 (partial pressure of oxygen at which hemoglobin is 50% saturated) and the Bohr effect were determined as previously described (see Ref. 16, and references within).

Protocol. Presurgery O2, CO2, and fH data were obtained for each animal at both temperatures to assess the effect of subsequent implantation of catheters. After the thermal acclimation period (see above), the animals were fitted with masks and ECG electrodes and left for at least 30 min on a variable-speed treadmill in a controlled-temperature room at the appropriate experimental temperature. After this period, they were run on the treadmill at the maximum speed they could maintain for 5–10 min. The treadmill was ramped to maximum speed typically within 1 min, and maximum speed varied between Tbs and between individuals (mean speed: 25°C, 0.82 ± 0.08 km/h, 36°C, 0.95 ± 0.07 km/h). When a lizard no longer wanted to run (i.e., could no longer be enticed to run with gentle tapping on the hind legs), the treadmill was stopped and the lizard returned to the holding facility. Data for all measured variables were obtained from each animal 3–4 min before running (rest) and during the final 2 min of exercise (one set of data points at each). After the placement of catheters, the animals were again instrumented and exercised on the treadmill as described above. This time, small blood samples (~300 µl) of arterial and mixed venous blood were collected, together with gas exchange and fH data.

Derived variables. Using a rearrangement of Eq. 1, stroke volume and total cardiac output were derived using measured values of O2, CaO2, C, and fH.

Data analysis and statistics. Mass-specific data are denoted by the subscript, kg. Factorial scope of a particular variable is defined as the proportional change in that variable from rest to maximum exercise. Differences between temperatures for all variables were determined using post-hoc Bonferroni t-tests, and significance was considered at P < 0.05. Mean data, including the proportional changes in each variable with temperature and exercise state, were calculated from individual values from each animal (n = number of animals).


   RESULTS
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Respiratory gases and cardiac output. There was no significant difference in O2kg, CO2kg, or fH between the presurgical and postsurgical treatments (P > 0.300) so, accordingly, we only present data obtained from catheterized animals.

At 36°C, resting O2kg was approximately twice that at 25°C (Q10 1.8) and was primarily accompanied by a doubling in bkg (P = 0.045) achieved through a doubling in fH (P = 0.001). Tissue oxygen extraction remained statistically unaltered (Table 1), and consequently, the blood convection requirement (bkg/O2kg) during rest did not differ between temperatures (P = 0.136).


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  		Table 1. Cardiorespiratory variables during rest and exercise for V. rosenbergi at 25°C and 36°C

 
During maximum exercise at 25 and 36°C, the absolute scopes in O2kg were 8.5 ml·min–1·kg–1 and 15.7 ml·min–1·kg–1, respectively, though the factorial scope remained constant at 7.0 (Fig. 1; Table 1) which, at each temperature, was the result of approximate 3.4-fold and 2.1-fold increases in bkg and (CaO2 – C), respectively (P < 0.020 for both variables). The cardio-metabolic parameters contributing to the Fick equation (Eq. 1) can be visualized for resting and exercising animals as illustrated in Fig. 2. At each Tb, the increase in bkg resulted from approximate twofold increases both in fH and VSkg, and the increase in (CaO2 – C) was the result of a decrease in C(P = 0.015), while CaO2 tended to increase slightly. During exercise, bkg/O2kg decreased to about half the resting value, indicating that bkg alone is unable to sufficiently supply O2 to the active tissues.



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  		Fig. 1. Factorial increase in the rate of oxygen consumption (O2), heart rate (fH), cardiac stroke volume (VS), and tissue oxygen extraction [(CaO2 – C)] during exercise for V. rosenbergi at 25 and 36°C; variables are arranged according to the Fick equation (see Eq. 1). Values are calculated as means of individual values ± SE.

 


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  		Fig. 2. Effect of exercise and temperature on arterial and mixed venous PO2 and O2 content (25°C, {square}; 36°C, {blacksquare}) in relation to hemoglobin oxygen dissociation for Varanus rosenbergi. Values are means ± SE. {circ}, actual measured values of PaO2 and CaO2 determined at the appropriate temperature (indicated) from blood taken from animals at rest. The dashed and dot-dashed regression lines have been adjusted according to the pH during exercise and Bohr effect for each temperature, 25 and 36°C, respectively. Right: graphical representation of the Fick principle (Eq. 1) showing the relative contributions of cardiac output (bkg) and arterial and mixed venous oxygen content difference [(CaO2 – C)] to O2kg (enclosed area) during rest and maximum exercise at each temperature.

 
Blood variables. Resting [Hb] remained at ~9 g/dl, irrespective of Tb. Likewise, resting Hcta remained constant at both Tbs (Table 1). Resting pHa decreased with increasing Tb with a {Delta}pH/{Delta}T°C of –0.008. Conversely, the resting level of blood lactate was temperature-independent, although during exercise, a higher lactate accumulation was evident at 36°C (up 6.1-fold, P < 0.001) when compared with that at 25°C (up 3.2-fold, P = 0.005), suggesting that anaerobic metabolism may supplement aerobic energy production during exercise to a greater extent at higher Tbs. Consequently, there was a decrease in pHa and pH during exercise at both Tbs (P < 0.020).

At both PCO2s of 3.20 kPa and 5.60 kPa, the affinity of the hemoglobin was greater at 25°C (P50 = 3.21 ± 0.11 kPa and 3.96 ± 0.12 kPa, respectively) than at 36°C (P50 = 5.60 ± 0.20 kPa and 6.44 ± 0.28 kPa, respectively). The Bohr effect ({Delta}logP50/{Delta}pH) was approximately –0.21 at both Tbs, which is lower than that generally reported for varanids [approximately –0.3; (16, 45)]. The heat of oxygenation ({{Delta}H = –2.303R·[{Delta}logP50/{Delta}(1/T)]}, where R = 8.314 J·mol–1·K–1 and T = temperature in °K) was ~37 kJ/mol and was not significantly affected by PCO2 (P > 0.05). This value is between the range calculated for other species of varanid [V. exanthematicus, {Delta}H = 36 kJ/mol (45); V. gouldii, {Delta}H = 44 kJ/mol (4)] between 25 and 35°C.


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Rest. Typically, for resting ectothermic vertebrates, the increase in O2 demand with increased Tb is met primarily by an increase in b rather than by an increase in (CaO2 – C) (27, 45). For resting V. rosenbergi, the increase in bkg with elevated Tb was achieved solely through a rise in fH. As both VSkg and (CaO2 – C) remained constant, the oxygen pulse [the product of VSkg and (CaO2 – C); corresponding to the volume of oxygen extracted per heart beat] was also independent of temperature. Consistent with this finding, temperature did not affect the oxygen pulse at rest in two species of scincids and an agamid lizard (43). Further, bkg/O2kg was not affected by temperature in resting V. rosenbergi, and the values were similar to those previously reported for other reptiles at similar temperatures (27, 45).

Resting pHa of V. rosenbergi decreased with increasing Tb to a greater extent than has been reported for other varanid lizards, including V. exanthematicus (44, 46) and V. gouldii (4). Nevertheless, the {Delta}pH/{Delta}T°C of –0.008 determined for V. rosenbergi in our study is less than that found for many other poikilotherms (see Ref. 44, and references within), and is much less than would be expected if V. rosenbergi were conforming to the relative alkalinity (or imidazole alphastat) concept [{Delta}pH/{Delta}T°C {approx} – 0.017, (33, 34, 36, 42)].

Maximum exercise. The factorial aerobic scope, with almost a sevenfold increase in O2kg at the preferred Tb of 36°C (Fig. 1, Table 1), is similar to that reported in a previous study on V. rosenbergi (11), but lower than that has been reported for most other species of varanid lizards at 35–36°C (37, 40). It is noteworthy that the factorial aerobic scope of varanids decreases as Mb increases and, in larger species such as V. rosenbergi, it has been shown to range between 8 and 13 (40). Some of the range in factorial aerobic scope may also be explained by ecological differences between the species (for discussion, see Ref. 40), or by the extent to which lizards are able to rest before obtaining a minimum O2 measurement.

At temperatures at or below the preferred Tb, but within the normal operant range, factorial aerobic scope would appear to be thermally independent in lizards such as Dipsosaurus dorsalis (iguanid) (22); Amblyrhynchus cristatus (iguanid) (from Fig. 1 in Ref. 6); V. gouldii (varanid) (from Fig. 2 in Ref. 5); Physignathus lesueuri (agamid), Egernia cunninghami (scincid), and Tiliqua rugosa (scincid) (from Figs. 2, 3, and 4, respectively, in Ref. 43), but not in Sauromalus hispidus (iguanid) (from Fig. 1 in Ref. 5). The majority of these studies induced muscle activity through electrical stimulation, so it is interesting to note from the present study that the factorial aerobic scope of V. rosenbergi determined through treadmill exercise is also maintained.



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  		Fig. 3. An interspecific comparison for varanids of factorial aerobic scope vs. the change in cardiac output per unit increase in the rate of oxygen consumption ({Delta}b/{Delta}O2) that occurs during activity. Values are from Table 2; letters correspond to species: m, V. mertensi; r, V. rosenbergi; s, V. spenceri; e, V. exanthematicus; g, V. gouldii. {bullet}, 35–36°C, {circ}, 25°C.

 
With respect to structural capacity, the cardio-metabolic responses contributing to greater O2 delivery during exercise appear to be similar for most vertebrates (see Ref. 23, and references within). In mammals, the circulatory convection is thought to operate at, or close to, the upper limit of structural capacity (24), and this also appears to be the case for varanids (e.g., Refs. 3, 18, and 31). Subsequently, maximum O2 for varanids where b has become limiting is achieved through increased (CaO2 – C) [Table 2; (16, 17)]. Data for V. rosenbergi from the present study have demonstrated that bkg and (CaO2 – C) make similar contributions to maximum O2kg at each Tb. The similar factorial increase in bkg during exercise at either temperature was achieved through similar increases in fH and VSkg. The notable increase in VSkg that occurred with exercise in V. rosenbergi is in contrast to that generally reported for birds (e.g., Ref. 9) and mammals (e.g., Refs. 10 and 25), while the contribution of VS to blood flow during exercise is far less generalized in reptiles (e.g., Refs. 16–18, 20, 29, 39) and fish (see Ref. 14, and references within). It is interesting to note that during rest and exercise at each Tb, (CaO2 – C) remained constant despite differences in P50; that is, the increase in hemoglobin-oxygen affinity associated with a decrease in Tb from 36 to 25°C did not compromise (CaO2 – C). Hence, differences in maximum O2kg that accompany changes in Tb are attributable to differences in bkg alone. Similarly, a study of dogs has shown that altering P50 does not affect the O2 achieved during maximal exercise (38).


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  		Table 2. Values for convective variables at rest and during maximum aerobic exercise in varanids

 
It has recently been argued that strong selective pressure to improve the speed of cardiovascular responses to activity occurred during vertebrate evolution (28). In recognizing that the relative change in O2 depends not only on the product of changes in b and (CaO2 – C) but also on the initial resting value of O2, these authors determine that higher resting metabolic rates are associated with a reduction in the demand for extra blood flow per unit increase in O2 (i.e., a reduction in the incremental change in the blood convection requirement, {Delta}b/{Delta}O2) during activity, thereby improving response times for convective O2 transport. Undertaking a cost-benefit analysis, Krosniunas and Gerstner (28) predict that the optimal level of resting O2 to achieve the greatest reduction in {Delta}b/{Delta}O2 with activity and the smallest loss of aerobic capacity is 11% of maximum O2; equating to a factorial scope of approximately ninefold. Although the factorial aerobic scope of V. rosenbergi, irrespective of Tb, is close to Krosniunas and Gerstner's predicted ninefold value, the increase in resting O2kg that occurs with temperature is not accompanied by a decrease in {Delta}bkg /{Delta}O2kg with activity; the value being about 13 and close to values determined for other varanids (Table 2). Thus, with increasing Tb and the associated increase in resting O2kg, the maintenance of factorial aerobic scope in V. rosenbergi will ensure a greater absolute aerobic scope but not, as predicted, much faster cardiovascular response rates during aerobic transitions from rest to exercise. Interestingly, {Delta}b/{Delta}O2 is strongly correlated with factorial aerobic scope in varanids (Fig. 3); those species with the highest factorial aerobic scope have the greatest ability to increase b per unit increase in O2 during activity.

In summary, at Tbs of 25°C and 36°C, V. rosenbergi is capable of maintaining the same factorial increase in aerobic metabolism. During maximum aerobic activity at both Tbs, an increase in bkg alone is not capable of meeting the increased demands for O2, as demonstrated by a decline in bkg/O2kg, hence the high O2kg associated with activity is achieved through a compensatory increase in (CaO2 – C). Although associated with an increase in hemoglobin-oxygen affinity, a decrease in Tb did not impair unloading of oxygen at the tissues and act to reduce (CaO2 – C); both CaO2 and C were maintained across Tb. The change in O2kg with temperature, therefore, is solely reliant on the thermal dependence of bkg. Maintaining a high factorial aerobic scope across a range of Tb confers an advantage in that cooler animals can achieve higher absolute aerobic scopes and presumably improved aerobic performance than would otherwise be achievable. The ability to achieve a high factorial aerobic scope over a broad temperature range appears to be associated in varanids with an ability to increase b with respect to incremental changes in O2 during exercise.


   ACKNOWLEDGMENTS
 
B. Green is thanked for capturing animals. E. Suric and T. Cousipetcos are commended for all aspects of animal husbandry. T. Clark (E-mail: timothy.clark@latrobe.edu.au) was the recipient of an Australian Postgraduate Association scholarship.


   FOOTNOTES
 

Address for reprint requests and other correspondence: Corresponding author: P. B. Frappell, Adaptational and Evolutionary Respiratory Physiology Laboratory, Dept. of Zoology, La Trobe Univ., Melbourne, Victoria 3086, Australia (E-mail: p.frappell{at}latrobe.edu.au)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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