AMER. ZOOL., 27:41-47 (1987)
Thermal Dependence of Air Convection Requirement and
Blood Gases in the Snake Coluber constrictor1
JERRY N. STINNER
The University of Akron, Department of Biology,
Akron, Ohio 44325
SYNOPSIS. In this report I discuss ventilatory and circulatory adjustments that provide
for increased O2 transport associated with increased body temperature in the snake Coluber
constrictor. Also included is the effect of temperature upon acid-base status. Minute ventilation increases with rising body temperature but does not keep pace with the increment
in resting O 2 consumption. The decrease in air convection requirement (i.e., ventilation
-r oxygen consumption) causes lung pO2 and arterial oxygen content to fall and lung pCO2
to rise. With the rise in lung pCO2, systemic arterial pCO2 and H+ concentration increase
while plasma bicarbonate concentration does not change. The effect of temperature upon
air convection requirement, arterial pCG2, and pH are most pronounced at body temperatures above about 27°C where Coluber behaves approximately as an alphastat pH
regulator. Despite the inverse relationship between temperature and lung pO 2 , systemic
arterial pO2 is about 80 torr lower at 15°C than at 35°C. This decline in arterial pO2 as
temperature falls is explained by left shifting the oxygen dissociation curve in the presence
of a constant right-to-left intracardiac shunt.
INTRODUCTION
Changes in body temperature markedly
alter resting metabolic rate in reptiles.
Oxygen consumption typically exhibits a
thermal coefficient (Qi0) of two to three so
that, from 10 to 40°C, resting oxygen consumption increases about 15-fold. In view
of the large effect of temperature, it is
interesting to determine if ventilatory and
circulatory adjustments occur that provide
for increased oxygen and carbon dioxide
transport.
In this report I examine effects of body
temperature on oxygen and carbon dioxide transport in black racers, Coluber constrictor. Black racers were chosen because
they are active over a wide range of body
temperatures. Fitch (1956, 1963), studying
a population of C. constrictor in Kansas,
reported temperatures from 20.6 to 37.4°C
in active snakes while in their natural surroundings. Associated with their temperature tolerance, Fitch observed that, relative to other reptiles in the region, C.
constrictor emerges early in spring and
remains active late in the fall so that it has
a generally longer season of activity.
Topics discussed below are: 1) adjust-
ments in ventilation relative to increasing
resting metabolic rates and how this affects
lung pO 2 and pCO2; 2) the relationship of
lung pO 2 and pCO 2 to systemic arterial
blood gases (pO2, pCO2), pH, and HCO3~;
and 3) application of the imidazole-alphastat hypothesis to vertebrate ectotherms.
MATERIALS AND METHODS
Ventilation and oxygen consumption
Minute ventilation was measured plethysmographically in five snakes wearing
close-fitting latex masks (for details of the
procedure see Stinner [1982]). Each day
tidal volume, breathing frequency, and
oxygen consumption were monitored continuously for 10 to 12 hr. Tidal volume
was measured with a Validyne pressure
transducer (model DP45-16). For oxygen
consumption, a portion of the air exiting
from the snake's mask was passed through
an oxygen analyzer (Applied Electrochemistry, model S3A) after removal of carbon
dioxide and water. Oxygen consumption
in ml STPD was calculated with corrections for differences in incurrent and
excurrent airflowrates (Depocas and Hart,
1957). Air flow into the snake's mask was
measured with a Brooks flow meter cali1
From the Symposium on Cardiovascular Adaptation brated against a Collins respirometer.
in Reptiles presented at the Annual Meeting of the
Each snake remained in the plethysmoAmerican Society of Zoologists, 27—30 December
1984, at Denver, Colorado.
graph for 6 to 12 days while simultaneous
41
42
JERRY N. STINNER
measurements of oxygen consumption,
tidal volume, and ventilation frequency
were made at 2 or 3 temperatures. At least
12 hr were allowed for equilibration at each
temperature. Metabolic rates reported here
are the lowest values taken for 15 to 30
min at each temperature. During the same
periods ventilation volume in ml BTPS was
calculated by summing the inspired tidal
volumes.
Cannulation and blood gas analysis
Animals were chilled in crushed ice and
a PE 10 cannula was tied occlusively into
the dorsal aorta near the cloaca. Snakes
were then placed inside cabinets where
temperature could be maintained within
1°C. After 2-3 days recovery from surgery
blood was sampled at 3-5 temperatures.
At least 12 hr was allowed at each temperature before blood was sampled. After
thoroughly flushing a cannula, approximately 200 /xl of blood was drawn rapidly
into heparinized capillary tubes. Although
the snakes were handled during blood sampling, they generally remained calm. Arterial pO 2 , pCO 2 , and pH were determined
immediately using Radiometer BMS-3
electrodes thermostated to the snake's body
temperature. The pO 2 electrode was calibrated with Radiometer pO2-zero solution
and aerated water adjusted to electrode
temperature. The pCO 2 and pH electrodes
were calibrated with Radiometer gas mixtures and precision buffers respectively
adjusted to electrode temperature. Calibrations were verified immediately before
blood gas measurements.
RESULTS AND DISCUSSION
Air convection requirement, lung pCO2, and
blood acid-base status
A basic equation for convection of CO2
by the lung is:
Vco 2 = VA CA C O 2 - VA' CII co 2 (1)
where Vco 2 is CO2 production, VA is
expired alveolar ventilation, VA' is inspired
alveolar ventilation, and CA C O 2 and CiCO2
are CO 2 concentrations in the alveolar air
and inspired air. Assuming the inspired
concentration of CO 2 is zero and solving
for air convection requirement (VA/VCO 2 ):
V A / V C O 2 = 1/CA C O 2
(2)
Since the concentration of a gas equals the
ratio partial pressure/RT (cf. Dejours,
1981), substituting for CA CO2 yields:
VA/VCO2 = RT/PACO2
(3)
R is the universal gas constant, 2.768 torrid"1, T is degrees Kelvin, and PA CO2 is
alveolar pCO 2 . Equation 3 is generally
referred to as the alveolar, or effective,
ventilation equation. In reptiles and
amphibians the gas exchange regions of
the lung are partitioned into functional
units termed faveoli which are not homologous to the alveoli of mammalian lungs
(cf. Duncker, 1977). Consequently, it is
preferable in this report to refer to equation 3 as the effective ventilation equation.
This equation can be expressed in terms
of minute ventilation (Vmin) and O 2 consumption (Vo2) by assuming, as did Jackson
(1978), that: 1) effective ventilation equals
0.8 of minute ventilation, and 2) the respiratory exchange ratio (R) equals 0.8 and
hence Vco 2 = 0.8 Vo 2 . Making these
assumptions, equation 3 becomes:
V min /Vo 2 = R T / P A C O 2
(4)
Equation 4 can be used to calculate an average expired faveolar pCO 2 in Coluber from
measurements of minute ventilation and
oxygen consumption.
Air convection requirements at temperatures of 20 to 38°C are presented in Figure 1. At 20 and 27°C, V E / V O 2 is constant
at about 60 to 65 ml air/ml O2 but shows
a marked decline at higher temperatures.
At 36°C V E / V O 2 is roughly 55% of the
values measured below 30°C. Figure 2
shows calculated expired faveolar pCO 2 at
20, 27, and 35°C as well as in vivo arterial
pCO2 measured in seven C. constrictor. Calculated expired faveolar pCO2 is close to
in vivo arterial pCO 2 . Hence it appears that
arterial pCO 2 changes very little between
15 and 25°C owing to a relatively constant
air convection requirement. Above 25°C
arterial pCO 2 varies directly with body
temperature because of a declining air convection requirement.
Increasing pCO 2 can produce declining
PHYSIOLOGICAL RESPONSES TO TEMPERATURE IN A SNAKE
43
I
E
O
o
a.
Body Temperature (°C)
BODY TEMPERATURE(°C>
FIG. 1. Effect of temperature upon air convection FIG. 2. Effect of body temperature on arterial pCO2
requirement in five resting Coluber constrictor. Line in seven C. constrictor (filled circles). Unfilled circles
denote calculated expired faveolar pCO2- Line was
was fitted by eye.
fitted by eye.
plasma pH because CO2 reacts with water
to form carbonic acid. From the Hender- possible changes in bicarbonate ions due
son-Hasselbalch equation, pH = pK + log to temperature dependent changes in fixed
([HCO 3 ]/a pCO2), it is evident that pH is acid levels, e.g., lactic acid.) Various studies
a function of the equilibrium constant for have reported constant plasma bicarbonCO2 (pK) and the ratio [HCO ? -]/oc p CO 2 ate concentration over wide temperature
where <x. is the solubility coefficient for CO2. ranges in air breathing ectotherms (cf.
In Coluber, plasma pH changes very little Reeves, 1977). Thus acid-base changes in
between 15 and 25°C (Fig. 3) but from 25 the plasma of these animals appear to mimic
to 40°C pH declines about 0.014 units/°C. those in a sealed blood sample. When temAdjustments in pH result from changes in perature rises, pCO2 increases, pH declines
pCO2 since calculated plasma [HCOS~] is by about 0.017 unit/°C, and carbon dioxconstant at about 15.5 mM over the tem- ide content does not change. In air-breathperature range of 15 to 40°C (Fig. 4).
ing ectotherms, which of course are open
systems with respect to carbon dioxide, the
Imidazole-alphastat hypothesis
rise in blood pCO2 is accomplished by lowRobin (1962) first noted the similarity ering air convection requirement. Hence,
between the change in plasma pH with precise regulation of ventilation is necestemperature in a living ectotherm and the sary for achieving the acid-base status
change in pH of mammalian blood in vitro appropriate for each temperature.
cooled at constant carbon dioxide content
In the same paper Reeves (1972) also
(a Rosenthal system). Ten years later R. B. reported that total carbon dioxide content
Reeves accounted for the change in pCO2 of bullfrog heart muscle in vivo is indepenand pH in a Rosenthal system by using a dent of temperature and that intracellular
model consisting of two buffers, carbonic ApH/°C in bullfrog skeletal muscle in vivo
acid-bicarbonate and histidine. Applica- is about the same as in a Rosenthal system.
tion of Reeves' model to living air breath- He therefore suggested that his two buffer
ing ectotherms requires that total plasma model could be extended to the whole anicarbon dioxide concentration be indepen- mal. Later, measurements of in vivo ApH/A
dent of temperature as it is in a Rosenthal temperature in tissues of frogs and turtles
system. An equivalent requirement is that substantiated this conclusion (Malan et al.,
plasma bicarbonate concentration be inde- 1976). However, in some tissues such as
pendent of temperature because about 95% skeletal muscle, there is a significant quanof the carbon dioxide in blood is in the tity of a third buffer, phosphate. As temform of bicarbonate ions. (This ignores perature rises phosphate is titrated by car-
44
Artei ial Plasma
(mM
<»
JERRY N. STINNER
7.40
Body Temperature C O
FIG. 3. Body temperature and arterial plasma pH in
seven C. constrictor. Line was fitted by eye.
bonic acid yielding increased bicarbonate
levels. Hence, although pH changes by
0.017 unit/°C, the requirement for constant carbon dioxide content does not apply
to some tissues.
According to Reeves the ApH/A temperature observed in a Rosenthal system
and in tissues of living ectotherms parallels
the ApK/A temperature of imidazole
groups of histidine moieties in tissue proteins. Consequently, thermally induced
ionization of imidazole groups is prevented
by common ion effect. Reeves argues that
imidazole groups are particularly important in determining net protein charge over
the physiological pH range. Hence, acidbase regulation in ectotherms is directed
towards preserving protein charge. Functionally this stabilizes enzyme activity and
the Donnan equilibrium across cell membranes. The central importance of the
fractional ionization (termed alpha) of
imidazole groups in acid-base regulation
led Reeves to conclude that there is a regulatory area (termed alphastat) responding
to changes in alpha imidazole. The interesting concept that acid-base regulation in
animals can be viewed as preserving imidazole charge is referred to as the imidazolealphastat hypothesis.
Above about 25 to 30°C acid-base balance in C. constrictor appears to be similar
to an alphastat pH regulator. However, at
cooler temperatures plasma pH changes
very little, and thus pH regulation does not
t
14
-
.
:
•
: ;
:
10
20
>
I
i
i
30
40
Body Temperture (°C)
FIG. 4. Thermal dependence of arterial plasma
bicarbonate concentration in seven C. constrictor. Values were calculated from blood pCO2 and pH and the
Henderson-Hasselbalch equation. Temperature corrected pKs and CO2 solubility coefficients were
obtained from Reeves (1976).
preserve protein charge as required by the
imidazole-alphastat hypothesis. Departure
from alphastat control has been reported
to occur in other reptiles. In the marine
iguana (Ackerman and White, 1980), green
iguana (see figure 4 of Wood and Moberly
[1970]), green sea turtle (Kraus and Jackson, 1980) and red-eared turtle (Robin,
1962) arterial plasma pH is nearly independent of body temperatures below about
25°C. And in the savannah monitor plasma
pH changes only slightly (—0.005 pH unit/
°C) from body temperatures of 15 to 40°C
(Wood et ai, 1981). In addition, measurements of air convection requirement in
several turtle species suggest that they also
do not maintain constant net protein charge
over the entire temperature ranges studied
(for review see Glass and Wood [1983]).
Recently, Cameron (1984) and Heisler
(1984) seriously questioned the validity of
alphastat control in fish. They found that
tissue pH does not change by 0.017 unit/
°C in a number offish species. These examples, both in fish and reptiles, suggest that
the imidazole-alphastat hypothesis does not
adequately explain acid-base regulation in
animals.
Air convection requirement, lung pO2 and
arterial pO2
The relationship between alveolar ventilation and O 2 consumption is expressed
by the following equation:
Vo., = VA' CI O 2 - VACA O 2
(5)
PHYSIOLOGICAL RESPONSES TO TEMPERATURE IN A SNAKE
where VA' and VA are the inspired and
expired alveolar (or faveolar) ventilation
rates, and CiO2 and CA O2 are the concentrations of oxygen in inhaled air and
expired alveolar air. Assuming expired
alveolar ventilation volume equals inhaled
alveolar ventilation volume, and substituting Po 2 /RT for CO2 (see above):
Vo 2 = VA(PI O 2 - P A O 2 ) / R T
(6)
1
45
100
E
O
O.
Substituting equation 3 for VA and Vco 2 /R
for Vo2, and solving for PA O2 yields:
PAO 2 = Pio 2 -
(7)
Equation 7 is the alveolar oxygen equation (or alveolar gas equation) in which
inspired ventilation is assumed equal to
expired ventilation. This assumption results
in a 1 to 2 mm Hg underestimate of expired
faveolar pO 2 in Coluber (see below). Assuming R = 0.8, an approximate expired faveolar pO 2 can be calculated using either
expired faveolar pCO2 derived from equation 4 or, since calculated faveolar pCO 2 is
very close to arterial pCO2 (see Fig. 2), an
approximate faveolar pO 2 can be calculated using arterial pCO2.
In vivo arterial pO 2 and calculated
exhaled faveolar pO 2 in Coluber are presented in Figure 5. Unlike with lung and
arterial pCO 2 , arterial pO 2 does not follow
changes in lung air pO 2 . From 15 to 27°C
exhaled faveolar Po 2 declines by only 6 mm
Hg due to a nearly constant air convection
requirement. Above 36°C declining pO 2 is
more evident and results from a marked
decrease in air convection requirement
(Fig. 1). Despite reductions in V E / V O 2 and
lung pO 2 , arterial pO 2 increases linearly
from ca. 40 torr at 15°C to ca. 120 torr at
35°C. Consequently, expired faveolar-arterial pO 2 difference declines from about 100
mm Hg at 15°C to zero at 35°C. In other
words, as temperature increases to 35°C
arterial pO 2 approaches lung pO 2 .
The increase in arterial pO 2 evident in
Figure 5 results from right shifting of the
oxygen dissociation curve in the presence
of a right-to-left shunt (cf. Rossoff et ai,
1980; Wood, 1984). This can be understood from examination of curves "a" and
"b" in Figure 6. On both curves arterial
Body Temperature (°C)
Fie. 5. Effect of body temperature upon expired
faveolar and arterial pO2 in Coluber. Circles denote
arterial pO2 measured in six snakes. The line represents faveolar pO2 calculated from equation 7. Note
that as temperature increases faveolar-arterial pO2
difference decreases and, at 40°C, arterial pO2 exceeds
calculated faveolar pO2 by about 20 mm Hg.
O 2 content is lower than pulmonary endcapillary O 2 content. Pulmonary end-capillary-arterial O2 content differences could
result, for example, from systemic venous
blood mixing with oxygenated blood within
the heart {i.e., a right-to-left intracardiac
shunt). Note in Figure 6 that although the
pulmonary end-capillary-arterial O 2 content difference is the same for curves "a"
and "b," the pulmonary end-capillary-arterial pO 2 difference is considerably smaller
for curve "b." The reason is, owing to the
rightward position of curve "b," the slope
is greater between its pulmonary end-capillary and arterial points. Hence, arterial
pO 2 is higher in curve " b " than curve "a"
despite the same reduction in oxygen content caused by an equal shunt fraction.
Beginning with the pioneering efforts of
Dr. Fred White (see White, 1970) right-toleft intracardiac shunts have been demonstrated in a variety of reptilian species.
For example, Seymour (1978), using O2 as
a marker, found that an average of 28 to
76% of systemic cardiac output effectively
bypasses the lung in sea snakes. Heisler et
al. (1983), using radioactively labeled
microspheres, reports that the average
right-to-left shunt is about 30% in savan-
46
JERRY N. STINNER
i
.»;
*••«
C
o
O
g .6
O
d
Body Temperature (°C)
O2 Partial Pressure
FIG. 6. Effects of right shifting the O2 dissociation
curve and of lowering pulmonary end-capillary pO2
on systemic arterial pO 2 . Unfilled circles represent
pulmonary end-capillary blood and filled circles represent systemic arterial blood. Relative to curve "a"
the same reduction in O 2 content along curve "b"
produces less change in pO 2 because of its steeper
slope. The same is true for curve "c" relative to curve
"b." However, because of the lower pulmonary endcapillary pO 2 of curve "c," arterial pO2 is less affected
by shifting from "b" to "c" than from "a" to "b."
For "d" the pulmonary end-capillary point occupies
a very steep portion of the curve. Consequently the
reduction in pO 2 associated with a reduction in 0 2
content is not expected to be large. If, with the decrease
in O2 content, the O2 dissociation curve shifts to "e,"
arterial pO 2 will exceed pulmonary end-capillary pO2.
nah monitors. In addition, reptilian blood
generally exhibits a marked decrease in
oxygen affinity (i.e., increase in P50) when
body temperature increases (see review by
Pough [1980]). For example, P50 in the
green iguana is about 17 mm Hg at 20°C
and 54 mm Hg at 40°C (Wood and Moberly, 1970). The large increase in P50
results from elevating temperature (heat
of oxygenation) and, in alphastat pH regulators, increasing H + concentration (Bohr
effect).
Above about 36°C Coluber's arterial pO2
increases very little with temperature (Fig.
5). This probably happens because at high
temperatures there is decreasing pulmonary end-capillary oxygen content owing
to a rapidly declining air convection
requirement coupled with further right
shifting of the oxygen dissociation curve.
The reduction in oxygen content is evident
in systemic arterial blood (Fig. 7). The effect
of reducing pulmonary end-capillary O2
FIG. 7. Thermal dependence of arterial O2 content
in C. constrictor (n = 15). O2 contents were measured
with a Natelson Microgasometer and are expressed
as fractions of the highest O2 content measured in
each snake. Note that above about 30°C arterial O 2
content declines with increasing body temperature.
content on arterial pO 2 is illustrated in Figure 6 (curves "b" and "c").
Note also in Figure 5 that at 40°C arterial
pO 2 is very high (x = 128.5 mm Hg) and
exceeds calculated exhaled pO 2 by about
20 mm Hg. As predicted by Wood (1982),
this can occur because the oxygen dissociation curve of arterial blood is to the right
of the curve for pulmonary venous blood.
When CO2-rich systemic venous blood
mixes with pulmonary venous blood in the
heart, the oxygen dissociation curve shifts
to the right owing to the Bohr effect. Of
course this displacement of the oxygen dissociation curve within the heart also occurs
at lower temperatures but, owing to their
relatively shallow slopes, the resultant arterial pO 2 is lower than pulmonary end-capillary pO 2 . Oxygen dissociation curves "d"
and "e" in Figure 6 illustrate how a negative pulmonary end-capillary-arterial pO 2
difference can exist.
Rising systemic arterial pO 2 with increasing body temperature has been observed
in other reptilian species (Wood, 1982). (It
should be noted however that arterial pO 2
reported here for C. constrictor is about 20
to 30 mm Hg higher at any given temperature than in the savannah monitor [Wood
et al., 1981] and green sea turtle [Wood et
al., 1984]. Recent work in my laboratory
has shown that the higher pO 2 in C. constrictor occurs when the animals are disturbed. The probable cause for the rise in
arterial pO 2 is right-shifting of the oxygen
PHYSIOLOGICAL RESPONSES TO TEMPERATURE IN A SNAKE
dissociation curve due to metabolic acidosis.) Wood (1982) makes the intriguing
suggestion that elevating arterial pO 2 with
rising temperature is important in reptiles
since it may maintain tissue pO 2 above the
critical O2 tension which also increases with
temperature. Interestingly, the preferred
body temperature range of Coluber extends
up to 36°C (Fitch, 1963). Thus, Coluber
appears to avoid temperatures where arterial pO 2 might fall below the critical tension and tissue oxygenation would be insufficient to maintain metabolism.
47
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Kraus, D. R. and D. C.Jackson. 1980. Temperature
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Malan, A., T. L. Wilson, and R. B. Reeves. 1976.
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Pough, F. H. 1980. Blood oxygen transport and
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carbon dioxide content and body temperature in
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Reeves, R. B. 1976. Temperature-induced changes
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