Download Gas Exchange and Control of Breathing in Reptiles

PHYSIOL0GICU
REVIEWS
Vol. 63, No. 1, January
Printedin
USA.
1983
Gas Exchange and Control of
Breathing in Reptiles
MOGENS
L. GLASS
AND
STEPHEN
C. WOOD
I. Introduction
.........................................................
A. Patterns of breathing
.............................................
B. Gasexchange
.....................................................
C. Ventilation-perfusion
ratio ........................................
D. Pulmonary diffusing capacity ......................................
E. Control of breathing
..............................................
F. Respiratory symbols ..............................................
II. Ventilation
..........................................................
......................................................
A. Introduction
B. Breathing patterns ................................................
C. Scaling of ventilation and air convection requirements
..............
III. Gas Exchange ........................................................
A. Introduction
......................................................
B. Oxygen uptake during rest and activity
............................
C. Gas-exchange ratios ...............................................
D. Diffusing capacity of the lungs .....................................
E. Ventilation-perfusion
matching ....................................
F. Nonpulmonary gas exchange .......................................
G. Gas exchange in periodic breathing
................................
IV. Effects of Temperature on Control of Breathing ........................
A. Concepts of constant relative alkalinity and alphastat regulation
....
B. Consequences for ventilation and gas exchange .....................
C. Exceptions to alphastat regulation and constant relative alkalinity
..
V. Control of Breathing at Constant Body Temperature
...................
A. Ventilatory responses to carbon dioxide inhalation
..................
B. Anoxia and hypoxia: tolerance and regulatory responses ............
C. Receptor systems .................................................
VI. Conclusions ..........................................................
232
233
236
237
238
238
239
241
242
243
245
246
246
247
248
I. INTRODUCTION
This article reviews the respiratory
physiology of reptiles, specifically
ventilation,
gas exchange, and control of breathing. We do not attempt to
present a comprehensive or encyclopedic review but instead use data selected
from the literature to illustrate major points.
The diversity of modern reptiles and their many unique physiological
and biochemical traits make them attractive as experimental animals. These
232
0031-9333/83/000099-06$01.50
Copyright
0 1983 the American
Physiological
Society
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Abteilung Phgsiologie, Max-Planck-Institut fiir experiwmatelle Medixin,
G3tingen, West Gemnany; and Department of Phgsiologg, School of
Medicine, University of N&w Mexico, Albuquerque, New Mexico
January
1983
RESPIRATION
IN
233
REPTILES
features, however, also create problems in experimental
design and interpretation of data. In fact the problems associated with interpreting
reptilian
physiology emerge as the central theme in this review. To pique the reader’s
interest, perhaps it is worth summarizing
these problems at the outset.
A. Patterns
of Breathing
B. Gas Excharzge
Most equations
used by mammalian
physiologists
to analyze gas exchange are valid only under so-called steady-state conditions, i.e., when the
tissue respiratory
quotient (RQ) equals the respiratory exchange ratio (RE)
=
CO2
production
(ko2)/02
uptake (VO,)]. This creates a problem in
CRE
analyzing reptilian
data: steady state is difficult to determine and is an
infrequent
condition for reptiles. In reptiles, RE frequently deviates from
RQ owing to phenomena such as cutaneous CO2 elimination,
production of
ammonium bicarbonate in urine, and breath holding. A further complication
is the high anaerobic capacity of many reptiles. Alligators, for example, take
up to 12 h to repay an O2 debt. Turtles can tolerate complete anoxia for days
or months, accumulating
lactic acid levels up to 200 mmol liter-l, and can
survive a decrease in brain pH to 6.4.
l
C. Ventilation-Perfusion
Ratio
This concept presents a real problem when applied to reptiles because
both ventilation
(V) and pulmonary blood flow (QL) are often periodic. The
presence of large and variable central vascular shunts provides reptiles with
a flexible circulatory
system. Although
somewhat disadvantageous
to O2
transport, the central shunts permit the pulmonary circulation to be both
in series and in parallel with systemic circulation. For diving species this
provides a redistribution
of blood away from the lungs during submersion.
Obviously, the concept of %VQL matching as the important
determinant
of
gas exchange in mammalian lungs must be cautiously and carefully applied
to reptiles.
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Show the respiratory trace of a normal turtle to a group of physicians,
and they will probably identify it as a case of Biot’s breathing, a pathological
pattern of breathing in humans in which breathing episodes and breath
holds alternate. Such periodic breathing is found in most reptiles and creates
a problem in characterizing
minute ventilation as the product of tidal volume
(VT) and breathing frequency (f). For example, a reptile may increase minute
ventilation
simply by reducing or eliminating
the breath holds, without
changing VT or f during the ventilatory
periods (VPs).
M. L. GLASS
AND
Vdume
S. C. WOOD
68
E. Cimtrol of Breathing
This area of reptilian respiratory
physiology creates some interesting
problems of data interpretation.
For example, if CO2 is added to the inspired
gas of reptiles, some species respond with the increase in VT expected by
mammalian
physiologists but show a paradoxical decrease in f and a net
decrease in minute ventilation
leading to aggravated CO2 retention.
An interesting reptilian “trick” is the difference in control of breathing
between conditions of constant and increasing body temperature.
A given
species may show increased ventilation
when given exogenous CO2 at constant body temperature;
however, if CO2 increases because of increased metabolism as temperature
goes up, the same species shows no ventilatory
response.
F. Reqkatmq
Symbols
The use of equations is necessary to explain
Common symbols are listed below.
A
a
&I3
BTPS
C
DL
Dko
-2
Eoz
f
I
M
NVP
basic respiratory
concepts.
alveolar
arterial
solubility of a gas in blood or water
air convection requirement
body temperature
and pressure, saturated with water vapor
concentration
of a gas
diffusing capacity of the lung
carbon monoxide (CO) diffusing capacity of the lung
O2 diffusing capacity of the lung
pulmonary O2 extraction
breathing frequency
inspired
body mass
nonventilatory
period, i.e., breath-hold period
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The relatively low O2 consumption
of reptiles compared with that of
mammals of similar size (with both groups at 37°C) prompted some-authors
to look at pulmonary diffusing capacity (DL) as a probable limiting factor.
The presence of central vascular shunts creates considerable problems in
assessing the importance of DL in reptiles. Even if DL were infinite, the
admixture of venous blood would produce arterial desaturation.
Thus the
finding of PA% - Ph values [i.e., alveolar-arterial
differences in O2 partial
pressure (POT)]of 40-60 Torr in normal reptiles cannot be ascribed to inadequate lung architecture alone.
January
1983
P
Pa co2
PACO,
Pa 02
PA
02
02 - pa02
PC02
PA
PK'
QL
R
RE
RQ
STPD
T
V.
V
WQL
.
VA
vco
.
2
VD
.
VE
.
vo
2
VT
VP
II.
IN
REPTILES
235
gas pressure (total or partial)
partial pressure of CO2 in arterial blood
partial pressure of CO2 in alveoli
partial pressure of O2 in arterial blood
partial pressure of O2 in alveoli
alveolar-arterial
difference in partial pressure of O2
partial pressure of CO2
apparent first dissociation constant of the bicarbonate buffer
system
partial pressure of O2
pulmonary blood flow
gas constant
gas-exchange ratio for a gas exchanger, i.e., ratio of CO2
output to O2 uptake
respiratory
quotient
standard temperature
and pressure (OOC, 760 Torr) and dry
absolute temperature
gas volume
gas volume per unit time or ventilation
ventilation-perfusion
ratio
alveolar ventilation,
i.e., volume expired from the alveolar
compartment
per unit time
co2 output
dead-space ventilation
total ventilation,
i.e., total expired volume per unit time
O2 uptake
tidal volume, usually calculated as a mean value for expired
volume
ventilatory
period
VENTILATION
A. Introduction
Like birds and mammals, reptiles ventilate the lung by a suction-pump
mechanism. Thus inspiratory
flow is caused by the development
of subatmospheric pressures within the lung (cf. 84). Pressure gradients result from
rib cage movements alone because the diaphragm is absent in reptiles (121).
The basic respiratory
flow pattern in reptiles consists of an exhalation followed by inspiration.
If the glottis closes at end expiration,
a breath-hold
period follows (30,36,53). Some studies report a second expiration preceding
breath holds (91); however, these triphasic flow patterns apparently result
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PO
. 2
RESPIRATION
236
M. L. GLASS
AND
S. C. WOOD
ih?ume
63
from excitation of the animal or are artifacts of the methods used to measure
ventilation
(36).
Like mammals, reptiles have dead-space ventilation
(VD),
as well as
alveolar ventilation
(VA),
i.e., ventilation
of the gas-exchange surfaces (cf.
78). The value of VA determines intrapulmonary
gas partial pressures and
is consequently more important
than total ventilation
(VE)
in relation to
control of breathing and gas exchange. Unfortunately
most of the data available are for TE.
Patterns
Reptilian breathing patterns may surprise those who are familiar with
the continuous breathing activity typical of nondiving mammals and birds.
In reptiles, breathing invariably alternates with periods of breath holding.
Breath holds may be interrupted
by a series of breaths (2, 24, 64, 88, 109,
117). This pattern is typical of some aquatic reptiles and persists when the
animal is out of the water (cf. 60,84). An alternative breathing pattern that
consists of single breaths interrupted
by relatively short breath holds has
been reported in some chelonians (57,87), lizards (118,154), and snakes (67).
These two alternative
breathing patterns are shown in Figure 1.
Interruption
of breathing activity by breath holds appears to be a general characteristic
of pulmonary ventilation
in ectothermic
vertebrates. In
amphibians pulmonary ventilation may alternate with periods during which
only the buccal cavity is ventilated (96). Ventilation
is also intermittent
in
lungfish (105). Discontinuous breathing patterns may even occur in nondiving
mammals under some extreme conditions; for example, when undisturbed
hibernating
hedgehogs are in deep hypothermia,
series of breaths are interrupted by protracted periods of breath holding (100).
Reptilian breathing patterns are difficult to characterize in terms of f
and VT. In mammalian
studies, VE is conventionally
reported as minute
volume, i.e., the volume expired during a l-min period (VE = f VT). This
concept is not satisfactory for description off in reptiles because some species
may breath hold for hours (cf. 8). An alternative
approach in describing f
in reptiles is to quantitate
the breath-hold
period [nonventilatory
period
(NVP)], i.e., f,,,, = fvr [VP/(VP + NVP)], where fmean is mean breathing frequency, fvr is breathing
frequency during ventilation,
VP is duration of
ventilatory periods, and NVP is duration of nonventilatory
periods. Breathing activity may occupy a small fraction of total time. At 25°C the ratio VP/
(VP + NVP) is 0.38 in Caiman sclerops (ll?), 0.18 in Crocodylus niloticus (60),
and 0.10 in the snake Acrochordus javanicus (59). Breath-hold
duration decreases with increased body temperature
(1,59,107), but even at 20°C breath
holds may exceed 1 h. For example, dive duration in Pseudemys concinna
may reach 141 min (8). An accurate description of ventilation
in reptiles
may therefore require measurements
over hours or even days. Ventilation
l
l
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B. Breathing
Jammy
1983
RESPIRATION
IN
237
REPTILES
Crocodylus
Test udo
1 min
FIG. 1. Typical
breathing
patterns
of reptiles.
U’@pey trace, ventilation
crocodile
(Crocodylus
niloticus);
lower trace, breathing
pattern
of a 3-kg
d&s).
Both species
inspire
before
breath
holding.
Measurements
were
tachography
on resting
unrestrained
animals.
I
in a young, 5-kg Nile
tortoise
(Testudo
parobtained
by pneumo-
should be characterized by VP and NVP and not only by VT and an overall
f value. The need to measure over prolonged periods is emphasized by reports
of large diurnal variations in ventilation
(123, 154).
Problems is assessing resting values for f and VT in reptiles may be
caused by the methods used to measure ventilation.
Reptiles are often sensitive to disturbances, which may prevent measurement of true resting ventilation (1, 81, 117, 130). Even when noise and disturbances
are kept at a
minimum, resting values may not be achieved, because measurement of ventilation may involve restraints and unnatural conditions that may influence
the reptile’s behavior. A quiet animal is not necessarily resting if it is restrained. For example, Cragg (36) measured ventilation
in the small lizard
Lace&x viridis (-30 g). Minimum values for ventilation
of sleeping animals
were less than half as large as values measured during the daytime on
restrained but quiet lizards. Some studies report unpredictable
breathing
patterns (117, 122). Such patterns would conform to the idea that reptiles
are animals without precise control of breathing. Alternatively
we suggest
that some erratic breathing
patterns result from inadequate
methods of
measuring ventilation. The finding that breathing patterns may be very regular if measurements
are taken with the least possible disturbance of the
animal (59) supports our theory.
C. Scaling of Ventilation
and Air Convection Requirements
It may be difficult to establish true resting values for ventilation
in
reptiles, but all studies are consistent in reporting resting values for ventilation that are markedly lower than those reported, for similar-sized mam-
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I
238
M. L. GLASS
AND
S. C. WOOD
Votaww
63
l
l
l
III.
GAS
EXCHANGE
A. Introduction
The gas-exchange surfaces of reptilian
lungs are covered by faveoli,
which are honeycomblike
extensions of the pulmonary wall (46, 121). Rep-
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mals or birds. Most data are available for lizards, for which Bennett (14)
derived an interspecies relation (y) expressing the dependence of ventilation
on body mass. Such relations take the general form y = aMb, where M
= body mass (in kilograms) and a and b are empirically derived constants.
For ventilation
of lizards at a body temperature
of 3537”C, Bennett calculated the relation VE = 4,614 Mo*76 (where VE is measured in ml BTPWh).
In reptiles this relation predicts ventilation
volumes that are about 20% of
the values for mammals (143). Some later studies have confirmed predictions
for ventilation
(56, 154). In contrast, Bennett (14) also attempted to derive
interspecies relations for the subparameters
of ventilation,
i.e., VT and f.
These predictions contrast considerably with later studies (cf. X9), perhaps
because the relationships
between VT and f can be highly flexible in lizards
(63). It is presently impossible to derive reliable relations for scaling of
ventilation
in nonsaurian reptiles because data are incomplete.
The relationship
between v and 00~ of a gas exchanger is expressed as
.
=
v
CI~,
Eo,,
where
CI~, is the inspired O2 concentration
and Eo, is
vo
pulmonary
O2 extraction.
This equation may be rearranged
to (~/TO&
CI~, Eo, = 1 (cf. 43). The ratio of ventilation
to O2 uptake (~/VO,,
measured
in ml BTPS/ml STPD) is termed the air convection requirement
(ACR) because it represents the ventilation volume required to extract a unit amount
of 02. The equation shows that ACR and Eo, are inversely related. Obviously
the degree of ex .traction of O2 from the inspired gas is an important
variable
in determi ning PACT, and recent studies have emphasized the role of ACR
in respiratory control (cf. 83).
Bennett (14) compiled data for ACR in lizards and concluded that ACRs
did not vary significantly with M. Lizards resemble birds and mammals in
this regard (43,102,138,143).
Reptilian ventilation and the ACRs may change
with temperature
(see sect. IvB). Bennett (14) compared lizards at about
37OC to mammals and found almost identical values for ACR. Thus the
interspecies relation to lizards predicts that ACR = 37.7 ml BTPWml STPD
against 35.5 ml BTPWml STPD for mammals (43). The ACR of chelonians
is generally lower than that for lizards. At 35OC ACR is 10.8 ml BTPWml
STPD in Pseudemys scripta (81) and about 25 ml BTPWml STPD in Pseudemysjbridana
(98). This is consistent with predictions by Howell and Rahn
(78). They derived equations to show *that ACR is inversely related to the
blood bicarbonate ion concentration
([HCOJ). Since plasma [HCO,] is generally greater in chelonians than in lizards (44), a difference in ACR is
predicted. Data for v and TO, of snakes and crocodilians are too scarce to
allow general statements.
January
1983
RESPIRATION
IN
REPTILES
239
B. Oxygen Uptake During
Rest and Activity
Bennett and Dawson (16) reviewed data for vo2 in reptiles and calculated
interspecies relations for scaling of resting VO, at several body temperatures.
They recognized that the data were of limited usefulness because few studies
report vo2 on undisturbed
reptiles resting in the dark. Despite this finding,
some preliminary
conclusions can be derived from these data. Dependence
of resting-state
VO, on M is expressed by the relation vo2 = aM! The ex-
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tilian lungs range in complexity from simple saclike structures, as in the
tegu lizard Tupinambis teguixin (99), to multicameral
lungs, as in varanid
lizards (121) or in the turtle Pseudemys sctipta (120). Thus the gas-exchange
units in reptilian lungs are not alveoli as in mammals. We emphasize this point because discussions of gas exchange in reptiles may include topics such
as alveolar ventilation
or alveolar gas partial pressure. It might seem appropriate to substitute the termfaveoZar
for alveolar in discussing reptilian
ventilation. Introduction
of a new term is unnecessary, however, because the
alveolar and faveolar compartments
are functi .onally identical.
Some difficulties in describing venti lation in reptiles also apply to gas
exchange. A fundamental
problem is the acquisition of true resting values
for voz or CO2 elimination
(ho2). Note that resting values are not always
obtained even when a reptile has been quiet for hours. Food intake in reptiles
may cause pronounced metabolic changes that persist during the digestive
process, lasting days (12, 23, 34, 35, 63). For example, 60, in snakes may
increase several-fold during periods of digestion (12).
Other problems arise from discontinuous
breathing
patterns.
These
problems are aggravated at low temperatures,
because breathing
activity
may be absent for hours (1, 58). Clearly a l-h measurement
could lead to
highly unreliable conclusions, e.g., that the animal is not consuming OZ.
Diurnal changes in 60, may also occur (23, 68, 154, 158).
A useful variable in description of mammalian
gas exchange is the pulmonary ventilation-perfusion
ratio (~/QL),
which is the ratio of i7A (measured in ml BTPS/min) to pulmonary perfusion (measured in ml BTPS/min).
In healthy mammals this ratio is close to unity (128, 148). In reptiles the
concept of ~/QL
is problematic because the lungs are ventilated periodically,
and perfusion is also quite variable.
Another useful concept in mammalian
physiology is that of DL (cf. 51).
This variable was originally defined as a diffusive conductance for gas transfer through the pulmonary
membrane,
i.e., the tissue barrier separating
alveolar gas and pulmonary capillary blood (20).
All the above concepts have been applied in discussions of reptilian gas
exchange (83,120,154,159).
In this review we discuss the validity of applying
these traditional
concepts to reptiles. In addition, we discuss some aspects
of reptilian gas excha nge that seem exotic but that may be interesting
and
en lightening to those primaril .y fam iliar w ith mam malian physiology.
240
M. L. GLASS
AND
S. C. WOOD
Volume
63
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ponent b has attracted the most interest because it is close to 0.75 in overall
relations based on large groups of organisms (72). Bennett and Dawson calculated the following interspecies relation for scaling of resting state 90,
at 20°C as (TO2 = ml OZ/h) = 25.6 MO**‘. Hemmingsen
(72) had previously
derived a general relation for scaling of the TO, of ectothermic animals at
20°C. Comparing the two relations, Bennett and Dawson (16) concluded that
reptiles resemble other ectothermic vertebrates in general metabolic level.
This conclusion is not too surprising, because Hemmingsen included data for
reptiles in his calculations for the more general relation.
The value of 00, in reptiles increases predictably with body temperature.
The Qlo values for the increase of resting VO, are frequently 2-3, but exceptions occur. In the range of temperatures
at which a reptile is normally
active, Qlo may decrease and approach 1. Examples have been reported for
lizards (cf. 125), chelonians (54), a crocodilian (23), and snakes (42, 90). This
effect is species specific. For example, the To2 value of Pseudemys scripta is
a simple exponential function of temperature,
whereas the vo2 value of the
box turtle Terrapene ornata changes little between 20 and 30°C but changes
markedly with temperatures
outside that range (54).
At body temperatures
of 37-40°C the weight-specific VO, of a reptile is
much less than that of an endothermic vertebrate. Bennett and Dawson (16)
calculated that a l-kg lizard at 37OC consumes 122 ml OJh, which is 18%
of the vo2 for a l-kg mammal (143).
The difference in 60, values between reptiles and endotherms correlates
well with variations in values for fundamental
variables in pulmonary function. The ventilation
volume of a reptile is about 20% of the value for a
mammal of similar size. Similar differences exist for pulmonary
perfusion
and DL (see sect. III@.
The different demands for O2 of reptiles and mammals
are also reflected at the tissue level. Bennett (13) reported that the number
of mitochondria
per unit weight of tissue is greater in mammals than in
reptiles but did not provide quantitative
evidence. A recent study by Else
and Hulbert (48) compared mitochondrial
volume density in tissues of the
lizard Amphibolurus
nuchalis to values for a mammal of similar size (Mus);
they found the greatest mitochondrial
volume density in the mammal, which
also had the greatest mitochondrial
membrane surface area. Another important difference at the tissue level is the amount of capillary surface area
available per unit volume of tissue. Pough (124) estimates that the capillary
surface area per unit muscle weight of a reptile is about 20% of the value
for a mammal of similar size.
Some reptiles can expand voz values considerably relative to resting
values. The turtle Pseudemys scripta, for example, may increase vo2 ZO-fold
(54). Maximum 00, of reptiles increases with body temperature
(cf. 125),
which implies that the capacity for sustained exercise is greatest at high
temperatures.
Interestingly,
Moberly (116) found that the maximum
sustainable walking speed of Iguana iguana nearly tripled with an increase of
body temperature
from 20 to 40°C. The range at which the greatest increase
of aerobic metabolism is possible may correspond to the active temperature
January
RESPIRATION
1983
IN
REPTILES
241
C. Gas-Exchange
Ratios
Values for the pulmonary RE in mammals reflect (at steady state) the
stoichiometry
of reactions in food catabolism. Therefore values of RE outside
the range of 0.7-1.0 are not expected. In reptiles the RE value may be 0.71.0 (cf. 16), but values lower than 0.7 have been reported. The pulmonary RE
value of CrocodyZus ~orosus may be as low as 0.32 (69). In crocodilians a
decrease in pulmonary RE values relative to the tissue RQs can be due to
incorporation
of COZ into the urine to form ammonium bicarbonate (34, 69).
This mechanism has only been studied in crocodilians, but it probably is not
important in all reptiles because nitrogen excretion in the form of ammonia
is negligible in many terrestrial
species (cf. 39). In some reptiles, gas exchange may occur through the skin (see sect. 1113’). This also decreases the
overall pulmonary exchange ratio (cf. 43).
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range (15, 125). More studies will be needed to assess whether the temperature dependence of maximum 00, is limiting for the activity of reptiles in
their normal habitat.
Despite the ability of reptiles to increase vo2 by several times, aerobic
metabolism may account for less than half of the energy expenditure measured at the highest metabolic rate (54, 68, 135). When, for example, the
water snake Natrix rhombifera
was stimulated
to maximal activity for 10
min, anaerobic metabolism accounted for as much as 86% of total energy
consumption (68). Coulson and Herbert (33) have pointed out that most animals are provided with similar amounts of usable muscle glycogen to provide
fuel for a burst of intensive muscular activity. Therefore the anaerobic power
available for a short, intensive activity burst is not very different for a 70kg crocodile or a 70-kg human. If activity is prolonged, however, the lower
aerobic capacity of the reptile will lead to development of a considerable O2
debt, which will be repaid very slowly. For example, elevated VO, indicated
repayment of an O2 debt in an alligator for no less than 12 h after cessation
of exercise (35). Recovery time depends on the weight-specific
VO,
of the
animals and will be most time-consuming
in large reptiles because weightspecific 00, decreases with increased body weight (35).
The capacity for increasing VO, relative to resting values may depend
on body weight. Bennett and Dawson (16) compiled data for VO, in reptiles
with M values ranging from 4 to 795 g and found that the ratio of maximum
vo2
to resting vo2 was independent
of M, i.e., the exponents for scaling of
resting vo2 and maximum To2 values are the same. This conclusion may be
premature because the resting and maximum 00, values were not derived
for the same combination
of species and because the analyzed weight range
was limited. In addition the conclusion conflicts with data for scaling of vo2
in large chelonians such as the Aldabra giant tortoise [Testudo gigantea (79)]
and the green sea turtle [Chelonia mydas (126)]. In these chelonians the
capacity to expand metabolism increases with body weight. More intraspecies
studies are needed to establish if scaling of vo2 in these chelonians is unique.
242
M. L. GLASS
AND
S. C. WOOD
Vohme
63
D. Di$ikag
Capacity of the Lungs
In 1909, Bohr (20) derived equations to describe the diffusive conductance
of a pulmonary membrane. For To2 an equation states TO, = DL~~ APo2,
where DL~~ is the O2 diffusing capacity of the pulmonary
membrane
and
APO, is the mean difference in PO, between alveolar gas and pulmonary
capillary blood. Thus a low DL o2 relative to vo2 could lead to large PO,
differences between alveolar gas and arterial blood. The DL value increases
with surface area and is inversely related to diffusion distance (cf. 43). Morphometric measurements
have provided estimates of DL values and show a
difference of an order of magnitude in the DL values of reptiles and mammals (120).
It is possible to measure DL directly by a method introduced by Krogh
and Krogh (lOl), but in that technique DL is measured for carbon monoxide
(CO) and not for OZ. Crawford et al. (37) measured DL~~ in small chelonians
and reported values ranging from 0.033 to 0.114 ml CO kg-l mine1 Torr-l,
corresponding
to 535% of values for mammals of similar size (145). This
order of magnitude is very likely correct, but it is problematic that Crawford
et al. only measured DL co at one temp,erature (ZO-23°C) because reptiles are
functional over a wide range of body temperatures.
A recent study reports
that DL~~ in lizards increases markedly with temperature
(62); this emphasizes that all variables in pulmonary function of reptiles must be reported
at specified body temperatures.
At 35-37OC the DL~~ value of lizards is about
20% of values for similar-sized
mammals (62). This value closely matches
a fivefold difference in resting vo2. Thus the ratio of DL~O to 60, is much
the same in lizards and mammals.
Clearly it would be more useful to know the DL values for respiratory
gases (02 and C02) than to know the values for CO, but direct measurements
are complicated (cf. 4). Recently obtained direct measurements of pulmonary
variables in the tegu lizard Tupinambis teguixin show that DL~~ increases
with temperature
and is of the same-order of magnitude as DL~~(61).
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l
l
l
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Some non-steady-state
conditions influence the pulmonary RE. 1) Breath
holding causes a gradual decrease in RE. Conversely, RE increases during
breathing activity (see sect. IIIG).
2) Changes in activity level affect RE because COZ is released during exercise and replenished during recovery (89,
i26). This situation may in part result from a decrease in NVP during exercise, but it could also be caused by metabolic changes. 3) Transient effects
of temperature
changes influence RE (cf. 16). 4) Altered feeding status may
decrease values for RE as a consequence of changes in acid-base status; such
changes are caused by the large amounts of acid needed for digestion in
reptiles that swallow whole animals or large chunks of meat (34).
Thus several explanations
should be considered if low RE values are
measured in reptiles. In addition such measurements
should be performed
over prolonged periods, preferably days, to establish if steady-state conditions exist or if low RE values are transient.
January
1983
RESPIRATION
IN
REPTILES
243
E. Ventilation-Perfusion
Matching
Pulmonary gas exchange is ineffective if perfusion of the lung is not
matched quantitatively
with ventilation
(cf. 148). Therefore it is significant
that pulmonary perfusion is also periodic in reptiles. Perfusion is greatest
during and immediately after breathing, and it decreases during breath holds
(26,28,93,141,149,151,152).
These changes in perfusion of the lungs correlate
well with adjustments of heart rate and stroke volume. However, perfusion
of the lungs also depends on selective redistribution
of cardiac output between systemic and pulmonary
circulation (cf. 151). The anatomical basis
is incomplete separation of systemic and pulmonary circulations. Thus the
ventricle is incompletely divided in noncrocodilian
reptiles (cf. 151). During
breath holds, blood is progressively shunted away from the pulmonary circulation (right-to-left
shunt), whereas during breathing
activity the net
blood shunt may be reversed. The decrease in pulmonary
perfusion during
breath holds is partly related to a progressive increase of pulmonary resistance that is cholinergically
mediated in chelonians (25). Matching of ventilation and perfusion during breathing activity may involve stretch receptors in the lungs rather than chemoreceptors.
In Pseudemgs sctipta artificial
ventilation
of the lungs causes increased perfusion.
In contrast, sudden
changes in alveolar gas composition have no effect on perfusion (92).
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Once values for DL~~ are established for various reptiles, one must still
ask whether DL~$ is a useful variable in describing reptilian gas exchange.
This question remains because the PACT- Paoz value is determined not only
by the diffusive conductance of the pulmonary gas exchanger but also by the
central cardiovascular admixture of systemic venous blood into the systemic
arteries (see sect. IIIE).
The PACT- PaoZ value may be as large as 45-50 Torr
in chelonians (28) and may exceed 60 Torr in sea snakes (140). Mitchell et
al. (114) have recently reported PACT - Pao, values of lo-20 Torr in resting
lizards. These values could be explained on basis of poor DL values, as Mitchell’s group suggested. But because present data on DL in reptiles indicate
values that are not particularly
low relative to To2 (62), it seems more likely
that large PACT- PaoZ values develop as a consequence of central cardiovascular mixing of blood. In addition the shunting of blood within the pulmonary circulation could prevent equilibration
between a fraction of pulmonary arterial blood and alveolar gas.
In a recent study of the sea snake Laticauda culobina,
Seymour (139)
concluded that large PACT- Paoz values primarily
result from shunting of
blood within the pulmonary
circulation and from central vascular mixing
of blood, whereas the diffusive resistance of the pulmonary
membrane is
relatively unimportant
in creating PO, differences. Some caution is required
in generalizing
these results because the reptiles are a diverse group and
because further information
on temperature
effects is desirable for evaluation of the causes for nonequilibration
between alveolar gas and systemic
arterial blood.
244
M.L.GLASSAND
S.C.WOOD
Vohme
63
F. Nonpulmonary
Gas Exchange
In 1960, Mertens (110) stated that the skin of reptiles is “almost impervious to water” and “of scant importance for respiration.”
These statements compared reptiles with amphibians, which lose water from the skin
at rates of the same magnitude as those for free water surfaces (138) and
which may also have high rates of cutaneous respiration
(cf. 43).
This schematic distinction between amphibians and reptiles is not valid
in light of studies published since 1960. Romer (134) discussed fossil evidence
that Carboniferous
amphibians were completely scaled. He suggested that
the highly water-permeable
skin of modern amphibians
represents a specialized secondary condition. Moreover reptilian
integuments
are not impermeable to water. This is especially true for species that occupy aquatic
habitats.
No less than 70-90% of total evaporative water loss may be cutaneous
in caimans and in Pseudemys scripta (cf. 17). Respiratory
gases may also
permeate the skin. Nonpulmonary
CO2 elimination
is substantial
in many
aquatic reptiles. For example, the nonpulmonary
CO2 elimination
is 65% of
total COZ output in the aquatic turtle Trionyx mucita (85), and up to 94%
of COB output is cutaneous in the sea snake PeZamis pZaturus (65). Nonpulmonary O2 uptake is usually a small fraction of total uptake. This observation
agrees with a general principle: in bimodal breathers the nonpulmonary
CO2
output is greater than nonpulmonary
O2 uptake (cf. 43). In the aquatic snake
Acrochordus javanicus cutaneous respiration
accounts for up to 33% of CO2
elimination but 8% of O2 uptake (144). In the freshwater turtle Sternothaerus
minor (at 22°C) and in the sea snake PeZamis pZaturus (30°C) the extrapul-
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The concept of ~/QL is a complicated idea to apply to reptiles because
these ratios can be based on mean long-term
values for ventilation
and
perfusion, or, alternatively,
on values measured only during breathing activity. The value for ~/QL ratio in mammals is close to unity. A temperatureindependent
value of 1.2 during breathing
has been reported for Varanus
exanthematicus,
which has the reputation
of being an active mammallike
lizard (154, 156). Larger deviations from a 1:l ratio are found in turtles (26,
98). Note that ~/QL may change with temperature.
Several studies report
that pulmonary
perfusion increases in proportion
to 60, when the body
temperature
of a reptile increases (62, 98, 156; R. N. Gatz, M. L. Glass, and
S. C. Wood, manuscript in preparation).
In most reptiles ventilation increases
less than 00, with increases in body temperature,
i.e., the ACRs are inversely
related to temperature
(cf. 83). Kinney’ and colleagues (98) studied the consequences of these relationships
in Pseudemysjbridana,
in which an overall
~/QL value decreased from 1.16 at 10°C to 0.62 at 35OC. These changes in
~/QL indicate that when body temperature
changes, ventilation
and pulmonary perfusion are independently
regulated relative to vo2.
January
RESPIRATION
1983
IN
REPTILES
245
G. Gas Exchange in Periodic Breathing
Weight-specific lung volumes of reptiles are often large relative to those
of mammals (37,62). Consequently the lungs may serve as a significant store
during breath holds. In the alligator the pulmonary
O2 store is 85% of the
total (6). A calculation further illustrates the significance of the pulmonary
O2 store. Crawford et al. (37) found a lung volume of 160 ml/kg in the semiaquatic turtle Pseudemys scripta and an O2 transfer from alveolar gas to
blood of 0.9 ml kg-’ min-’ at ZO-23OC. With an alveolar PACT of about 120
Torr during ventilation
preceding its dives (27), the turtle can dive with an
initial O2 store of about 24 ml/kg, which, if fully depleted, would suffice for
O2 delivery to the blood for 27 min. The pulmonary O2 store usually is not
fully used, and voluntary dives in Pseudemys end when PACTfalls to about
22 Torr (1). The O2 demands may be smaller than those Crawford et al. (37)
measured,“especially
in turtles resting at low temperatures,
where the pulmonary O2 store may meet aerobic demands for hours (I).
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monary O2 uptake is sufficient to prolong underwater
survival time (9, 65),
but the increase is only 1 h or less with the water Po2 at 150 Torr.
In vertebrates that rely on a combination
of pulmonary and cutaneous
gas exchange, the latter becomes relatively more important
at low body
temperatures
(cf. 43) because the values for cutaneous gas exchange are
relatively independent
of temperature,
whereas pulmonary
vo2
and ho2
increase with body temperature
(cf. 83). Some turtles can remain submerged
for months if the water temperature
is close to the freezing point (29). A
recent study (147) shows that the low metabolic needs of turtles at temperatures close to freezing may be covered by anaerobic stores alone, but surnonvival is significantly
promoted if water PO, is high, thus permitting
pulmonary O2 uptake.
The integuments
of land-dwelling
reptiles are much less permeable to
water than those of aquatic species. This condition limits cutaneous evaporation (17) but also reduces cutaneous gas exchange. At 20°C only about
3% of CO2 output is cutaneous in the tortoise Testudo dendricuzata (85). In
the chuckawalla (SaurmaZus obesus, a desert lizard) about 4% of CO2 output
and less than 2% of O2 uptake take place through the skin at 25°C (38). Even
in land-dwelling
reptiles, however, cutaneous CO2 elimination
may become
important
at low temperatures.
In the box turtle Terrapene ornata a large
fraction of CO2 output is cutaneous when the turtles are hibernating
at
5OC (58).
Nonpulmonary
gas exchange in reptiles is not always cutaneous. Pharyngeal respiration
occurs during submergence in the soft-shelled
turtle
Trionyx spinifer and can be seen as rapid movements of the hyoid apparatus
(47). Such specialized sites for nonpulmonary
gas exchange may have been
overlooked in studies that assumed nonpulmonary
gas exchange occurs only
through the skin.
246
M. L. GLASS
AND
S. C. WOOD
Volume
63
IV.
EFFECTS
OF TEMPERATURE
ON CONTROL
A. Concepts of Constant Relative
Alphastat Regulation
OF BREATHING
AlkCclinity and
In many ectothermic vertebrates the arterial pH (pH,) decreases with
an increase in body temperature.
Some researchers interpret this effect as
a preservation of constant relative alkalinity, i.e., OH-/H+ (77, 78,129,130).
Because the ionization constant of water (K. = [H+][OH-1) increases with
temperature,
constant water OH-/H+ requires increases in [H+] and [OH-]
with temperature.
Since [H+] = [OH-], the neutral pH of water (PA&) at any
temperature
is defined as pN, = 0.5 pK,. A constant relative alkalinity requires that arterial pH at any temperature
be equal to the neutral pH of
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Numerous studies describe pulmonary gas exchange during breath holds
in reptiles (1, 6, 18, 28, 45, 60, 67, 106, 140). All agree in reporting a gradual
decrease in the pulmonary
RE value with breath holding, i.e., the amount
of O2 transferred
from alveolar gas to blood is replaced by decreasing
amounts of C02. This effect of breath holding on RE is consistent with data
for mammals (cf. 115). During breath holding in mammals the CO2 gradient
between mixed venous blood and alveolar gas gradually decreases because
of the cessation of CO2 removal from the lung. This in turn reduces COZ
entry into the alveolar gas from the blood. Oxygen continues to be removed
from the alveolar gas via the pulmonary circulation to meet the requirements
of aerobic metabolism. As a result the lungs shrink, which concentrates CO2
in the alveoli and increases PA coZ. This further diminishes the partial pressure of CO2 (Pco~) difference between mixed venous blood and alveolar gas
and reduces CO2 entry into the alveolar compartment.
Thus a self-perpetuating cycle is in operation (cf. 115).
This explanation of gas exchange during breath holds applies to reptiles,
although the existence of cutaneous respiration
may complicate the interpretation. In Pseudemys at 20°C only about 10% of CO2 output is nonpulmonary (85). This amount is too small to explain decreases in RE during
breath holds (dives) to values as low as 0.2, and it strongly indicates CO2
loading in tissues (2). This interpretation
receives support from measurements of gas exchange during postdive ventilation
(1,28). Initially RE is low,
but it increases during breathing, indicating a gradual release of tissue CO2
stores. This observation again emphasizes the difficulty of applying the concept of steady state to reptiles and the caution that overall values for gas
exchange should be based on measurements over hours or days. The decrease
of RE during dives in the turtle CheZys fimbriata
has been attributed
to
nonpulmonary
COZ elimination
(106). To find out if CO2 is stored in tissues
or eliminated in the water, however, it is necessary to measure RE over a
prolonged period.
January 1983
RESPIRATION
IN
REPTILES
247
B. Consequences fbr Ventilution
From
und Gus Exchunge
equation pH = pK’ + log ([HCO;]/
of COZ in blood, both pK’ and CVCO~
decrease with increased temperature
(132). A regulated decrease of pH with
increase of body temperature,
however, can only result from alterations
of
the [HCO,]/Pco,
ratio. Blood [HCOJ could be regulated by ion exchange in
the kidneys or by an exchange between the intra- and extracellular
compartments (71). Several studies on reptiles report that plasma [HCO,] does
not change with temperature,
however, in which case the decrease in pH
requires that the arterial PCO~ (Pace,) increase with temperature
(78). The
alveolar Pco2 (PA& and Pa coZvalues depend on the ratio of VA to pulmonary
ko2 (cf. 83). This is expressed in the relationship
iTA/bC02
= RT/PA~~~,
where R is the gas constant and T is absolute temperature.
The ~~~~~ value
rises if iTA/h02
decreases. As we have said, the VE value is usually measured
instead of VA. Furthermore
To2 is more frequently measured than VCO, and
the effects of temperature
on the ACRs are reported.
Measurements of acid-base status in freshwater turtles (Pseudemys sp.)
are thought to support the concepts of constant relative alkalinity and alphastat regulation (86, 88, 98). Plasma [HCOJ is not influenced by temperature changes, whereas Paco2increases with temperature
owing to the decrease in the ACRs. For example, when the body temperature
of Pseudemys
scripta increased from 10 to 3O”C, vo2 increased (QIO = 1.8), whereas v did
not change significantly.
As a result, Pa coZ increased with 14.1 Torr to 31.9
Torr, while pH, decreased from 7.76 to 7.56 (88). The ACRs also decrease
with temperature
in the lizards Lace&a sp. (118) and Iguana iguana (56,
160), in the snake Thamnophis elegans (74), and in Alligator mississippienCVCO~
l
the Henderson-Hasselbalch
Pco~), where CYCO~
is the solubility
sis (40).
At high body temperatures,
an elevated
~~~~~ may lead to the disad-
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water plus a constant (C), or pH, = pNW + C. Differentiating
with respect
to temperature
gives dpH,/dT
= dpH,/dT
N -0.018.
Reeves (131) suggested that constant arterial OH-/H+ reflects regulation
of net protein charge. This regulation requires pH changes with temperature
that are similar but not identical to those for constant OH-/H+ (132). The
theory is based on a closed-system model in which CO, content is assumed
to be constant, and it predicts that constant net protein charge is preserved
in all body compartments
(108,131). Reeves (131) emphasized that constant
net protein charge optimizes enzyme activity
when body temperature
changes. This theoretical prediction has recently received some experimental
support (70, 161). Constant net protein charge implies constant fractional
dissociation of imidazole groups of proteins (constant cw-imidazole). Reeves
therefore used the term a@hns~at regulation for his model of vertebrate acidbase control.
248
M. L. GLASS
AND
S. C. WOOD
Volume
63
vantage that PA o2 is low. This is clear from the relationship
PACE,N PIED,
- PA~,/RE, where PI,, is the partial pressure of inspired O2 (cf. 148). In the
turtle Pseudemys jbridana
the pulmonary venous O2 content is decreased
at high body temperatures
because low PACTvalues prevent saturation of the
pulmonary capillary blood (98).
C. Exceptions to Alphastat
Relative Alkalinity
Regulation
and Constant
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The time courses of regulatory
responses of acid-base regulation were
largely neglected until 1976, when Jackson and Kagen (86) found that adjustments of ACRs and pH to temperature
changes in Pseudemys scripta
were immediate and similar to those reported earlier. However, the longterm or seasonal effects of temperature
on gas exchange, ventilation,
and
acid-base balance have been studied only recently and appear to be different.
During winter the body temperature
of the box turtle Terrapene ornata is
frequently 5OC or less (103). At 5OC the breathing frequency is 3 breaths/
h as a mean value for a 24-h period, but overnight breath holds do occur
(58). The ACRs of Terrapene increase with temperatures
below 15”C, which
is the minimum temperature
for activation of hibernating
box turtles (103).
At temperatures
greater than 15OC the ACRs decrease with increased body
temperature.
Figure 2 shows the effects of temperature
on ACRs for several
turtle species. The comparison emphasizes that the reported temperature
effects are highly divergent at lower temperatures,
whereas the results are
consistent at ZO-35°C. It is presently not clear whether the diversities of
responses at low temperatures
are species-specific or are due to differences
in exposure time to cold. Long-term
measurements
are frequently
required
for a full evaluation of the regulatory responses of reptiles; this is especially
true at low body temperatures.
In some lizards the relationships
between body temperature
and pH,
are different from those predicted for constant OH-/H+ and alphastat regulation. The deviations occur within temperature
ranges that include preferred body temperatures
(14, 153, 154, 157). Wood et al. (154) measured
ventilation,
gas exchange, and blood acid-base status in Varanus exanthematicus. Measurements were performed at night on resting undisturbed
animals. In Varanus the pH, values and ACRs did not change between 25 and
35OC. Thus ventilation
increases in proportion to vo2, and PaoZ is high (93.5
Torr) at 35OC. Wood et al. (153) argued that this is an advantage to an active
predatory lizard with high preferred body temperature
(37°C).
Davies (40) suggested that conflicting results on acid-base balance are
due to errors in the experiments on lizards. Wood and colleagues (157), however, have recently repeated measurements
on Varanus, but these experiments were based on heating and cooling during the daytime. Over the range
January
1983
RESPIRATION
IN
. Pseudemys floridana
A Chrysemys picta bellii
l
Chelonia mydas
80
20
0
I
0
I
10
1
1
1
20
Temperature
I
I
30
1“c)
FIG. 2. Relationships
between
air convection
requirements
(ACRs)
and
for various
turtle
species.
Note that results
are consistent
at higher
body
highly
divergent
at lower temperatures.
[Data from: n Jackson
et al. (88); v
A M. L. Glass, R. G. Boutilier,
and N. Heisler,
manuscript
in preparation;
l
o Glass et al. (58).]
body temperature
temperatures
but
Kinney
et al. (98);
Jackson
et al. (87);
of 15-38OC the pH, value decreased with temperature
but only by 0.005 units/
OC. This change is much too small to be consistent with constant relative
alkalinity or alphastat regulation.
Such results indicate that current concepts on temperature-dependent
acid-base regulation
need some revision.
Moreover note that some studies may seem to support constant relative
alkalinity but may also be interpreted
differently.
Thus in the turtle Pseudemys scripta the ApH/AT value for arterial blood was -0.010 units/“C between 10 and 30°C (88), whereas the predicted change for constant relative
alkalinity is a ApH/AT value of -0.018 units/“C (78).
Presently no explanation is available for these deviations from current
theories on temperature-dependent
acid-base regulation in reptiles. We feel
that the development of consistent models will require further experiments
involving exposure to temperatures
consistent with the ecology of the animals. A recent study by Ackermann
and White (2) emphasizes this point.
In the marine iguana AmbZgrhynchus &status, pH, decreases by 0.015 units/
OC when body temperature
increases from 24 to 35OC. At temperatures
below
24”C, however, pH, changes little with temperature.
Temperatures
between
24 and 35OC appear to be consistent with the ecology of the species.
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a
249
REPTILES
250
V.
CONTROL
M. L. GLASS
OF BREATHING
A. Ventilator9
I
AT
AND
CONSTANT
S. C. WOOD
BODY
TEMPERATURE
Responses to Carbon Dioxide Inhalation
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Reptiles at a given body temperature
regulate acid-base status by adjustments of VA relative to pulmonary ko2,
i.e., ~A/~co~
= RT/PA,,,
(cf.
43). The gain of this regulatory system is indicated by the ventilatory
responses to imposed increases in Pacoz and ~~~~~ caused by CO2 inhalation.
Effects of increased PCO~ on VA are difficult to measure, and VE or ACRs
are normally studied.
The ventilatory responses to COZ inhalation are diverse among reptiles.
Chelonians and crocodilians increase VT and overall f values in response to
elevated inspired Pu)~ (PI& (41,52,57,87,88).
This may produce pronounced
increases in VIX or ACR. In I?ww&w~~~~sscriJ)tcx,,for example, the ACRs increased U-fold in response to inhalation of 6% CO2 (88). Such positive ventilatory responses to COZ inhalation are also typical of birds (cf. 21) and
mammals (cf. 97) and are easily explained from a functional point of viewi.e., increased ventilation promotes CO2 elimination and opposes the rise of
~~~~~ and Pace,.
In aquatic reptiles, CO2 may also cause reductions in the duration of
breath holds. In Pseudemys the ratio VP/(VP + NVP) increases when CO2
is inspired (52). Dive duration in the turtle Pebmedusa subrufa is reduced
when ~~~~~ increases (57). Likewise the turtle Chrgsemys picta responds to
COZ inhalation by increasing f through a shortening of breath holds (113).
In Crocodylus niZoticus a shortening of breath holds is the only mechanism
that produces a positive frequency response to hypercapnia (60).
Most studies on the control of breathing in snakes and lizards report
paradoxical responses to inspiration of C02. The value of VT increases, but
f is depressed (59, 66, 118, 122, 146). In Lace&a viridis the depression of f
leads to a decrease in ventilation
relative to base-line values preceding COZ
inhalation (118). This response seems meaningless because a decrease in
ventilation diminishes the clearance of metabolically produced COB, thereby
increasing the concentrations
and PCO~ values in tissues. Therefore the responses of lizards and some snakes to CO2 inhalation possibly are different
from those produced by a metabolic elevation in Pacoz and PACES.
Recently Glass and co-workers (63) reported a positive frequency response to CO2 inhalation for the lizard Varanus exanthematicus. In Varanus
both f and VT increased markedly during COZ inhalation, leading to a sevenfold increase in ventilation
with an increase in PACT, of 15 Torr. The
relationship between PA coZand ventilation is highly reproducible in Varanus
in contrast to the relationships
between the subparameters
(VT and f) and
PACES.It is difficult to predict whether the ventilatory response results from
increased for from enlargement of VT. This is consistent with data on turtles,
indicating that VT and f are independently
regulated (cf. 84), a condition
that resembles the situation in birds (cf. 21).
January
1983
RESPIRATION
IN
251
REPTILES
The ventilatory responses of reptiles to COZ inhalation may be very fast
(55, 57, 84). In the tegu lizard Tupinambis nigropunctatus
a decrease in intrapulmonary
PCO~causes breath holding within 0.8-1.4 s (55). This indicates
a peripheral location of the receptor system, i.e., the receptors must be located close to the alveolar gas compartment
(see sect. vC).
B. Anoxia and Hypoxia: Tolerance and
Regulatory Responses
l
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Reptiles, (especially turtles) are very tolerant of anoxia. At their normal
active body temperature,
chelonians may survive for hours or days without
O2 (7,18,80,94,133).
Reptiles share this amazing tolerance with amphibians
(104), whereas anoxia is deadly within minutes to endotherms at their normal
body temperatures
(7). The anoxia tolerance of ectotherms is due in part to
low metabolic needs leading to a slow depletion of resources for anaerobic
metabolism. Decreased metabolism in hypothermic
mammals may also permit survival for hours without O2 (19). When reptiles are at body temperatures close to the freezing point, anaerobic glycolysis may provide sufficient
energy for several months (147).
The lack of O2 causes drastic changes in the animal’s acid-base status.
Clark and Miller (31) measured a decrease in brain pH from 7.2 to 6.4 in
Pseudemys scripta after the animal had been anoxic for 15 h at 22OC. Longterm survival of Chrysemys picta beZZii at 3OC was associated with the increase of plasma lactate to values exceeding 200 mmol liter-’ (147).
As we have said, depletion of aerobic reserves (mainly intrapulmonary
02) is very slow during breath holds in reptiles. Therefore it is relevant to
ask whether the tolerance to anoxia becomes important
for a reptile in its
normal habitat. Especially interesting in that context is the study by Ultsch
and Jackson (147) on the freshwater
turtle Chrysemys pi&a bellii, which is
unusually tolerant of anoxia and low temperatures
(142). Ultsch and Jackson
correlate this tolerance with the northern distribution
of this turtle, which
inhabits areas where lakes are covered with ice for prolonged periods.
Moberly (116) described another example of the survival value of anoxic
tolerance. The common iguana (Ig&ana iguana) will attempt to escape into
water when threatened by predators and may stay submerged for more than
4 h. The high blood lactate levels at the end of such dives indicate a strong
dependence on anaerobic metabolism.
In spite of this tolerance of anoxia, reptiles normally regulate ventilation
to avoid a lack of oxygen. The values of PACT and Paoz depend on ventilation
and VO, as expressed by a relationship
that for RE = 1 becomes PACT
= PI - RT(~o&A)
(43,
128).
Consequently
~~~~ rises when TE and VA
02
increase relative to TO,. Chelonians increase ventilation
in response to large
decreases in Pa 02, i.e., hypoxia (5, 10, 22, 26, 52, 57, 82). In aquatic species the
ventilatory response to hypoxia may include a decrease in NVP (cf. 159) and
252
M. L. GLASS
AND
S. C. WOOD
Vokurri~c? 63
an increase in the ratio VP/(VP + NVP), i.e., duration of ventilatory periods
relative to total time (52). Hypoxia also causes cardiovascular
changes. The
responses involve an increase in heart rate and an increase in pulmonary
perfusion (22, 26). The combination
of ventilatory
and cardiovascular
responses is effective in preserving normal vo2. In Chelydra seripentina the 00~
value remained constant when the ambient O2 concentration
decreased from
21to 2% (22).
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The ventilatory
responses to hypoxia have been studied in only a few
nonchelonian
reptiles. Nielsen (119) reported that ventilation
is depressed
by hypoxia in the lizard Lacerta. In contrast, ventilation
increased with
decreased Pro, in Varanus exanthematicus
(63). Snakes increase ventilation
in response to hypoxia (59, 66). For the aquatic snake Acrochordus, Glass
and Johansen (59) reported a positive ventilatory
response to hypoxia caused
by a reduction in NVP. Data on the ventilatory
responses of crocodilians to
hypoxia are scarce and largely qualitative, but CrocodyZus niZoticus increased
ventilation
mainly by shortening breath holds (60).
In reptiles the relationship
between ventilation
and PI,, usually resembles a hyperbolic function, i.e., the effect of hypoxia on ventilation
is small
unless inspired PIN, is considerably reduced. This resembles the mammalian
ventilatory response to hypoxia, which has been studied extensively (cf. 97).
In mammals a consequence of the shape of the response curve is that the
role of a Paz-mediated drive to ventilation
is relatively small unless PIN, is
considerably reduced, as at high altitude (cf. 148). In reptiles a hypoxic stimulus may not be important
unless Pa o2 is very low. For example, ventilation
in Acrochordus changes little if ambient PO, is decreased from 155 to 74 Torr,
whereas ventilation
doubles with decreases to 37 Torr (59). A Po2-mediated
ventilatory
drive may still be important
in normal respiratory
control because PACT and Paoz values may fall to low values during breath holding,
especially in diving reptiles (1, 59, 155).
The conventional method for measuring ventilatory responses to hypoxia
requires that a steady state be achieved, i.e., ventilation must reach a steady
value at each level of hypoxia. This causes various si de effects that may
mask a response (43). An alternative approach is to measure transient ventilatory responses after a single inhalation of pure OZ. Bench .etrit et al.
used this technique to study ventilatory chemoreflexes in the tortoise Testudo
horsJie+!di. Inhalation
of pure O2 depresses or arrests ventilation
within seconds. Consequently a tonic Po2-dependent stimulus to breathing is present
during normoxic conditions. Techniques less refined than the single-breath
method confirm that O2 breathing
depresses ventilation
in reptiles (52, 57,
59, 63).
At low body temperatures
the ventilatory
responses of chelonians to a
given concentration
of inspired O2 are much reduced relative to responses
at higher body temperatures
(10, 82). This effect may depend on several
factors: Demands for O2 are smallest at low temperature,
and therefore a
relatively smaller amount of O2 is extracted from the lung when tempera-
January
1983
RESPIRATION
IN
253
REPTILES
300
C‘c.3
-
80
-i
E.
0,
x
200 ci>
L
t-
m
2
.-E
100 5
.-E
9
0
0
20
40
PO,
60
80
(To4
FIG. 3. Ventilatory
responses
to hypoxia
in the freshwater
turtle
Chrysemys
picta be&%.
Pulmonary
ventilation
is shown
as function
of arterial
PO,. Highest
value corresponds
to normoxie conditions,
i.e., inspiration
of room air, whereas
lower values
result
from inspiration
of
hypoxic
gases. Relationships
are depicted
for 3 body temperatures.
Note pronounced
temperature
dependence
of ventilatory
responses.
Increased
temperature
causes shift to the right
of the
hemoglobin
02-binding
curve,
thus impairing
O2 transport
at low arterial
PO,. (From
M. L.
Glass, R. G. Boutilier,
and N. Heisler,
manuscript
in preparation.)
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
tures are low (82). Moreover the O2 affinity of the blood increases with lowering of the body temperature,
thereby facilitating
O2 transport
at low
PACT and Pao, values (cf. 124). Consequently the effects of a given decrease
in PI,, will be least severe at low temperatures.
As Wood and Lenfant (159)
have shown, however, a full evaluation of such relationships
requires that
the blood gas picture be known. Recently ventilatory
responses to hypoxia
were measured in the freshwater
turtle Chrysemys picta be&i along with
and
pH,.
Furthermore
the VO, and 02-binding curves were depao,, pace,,
termined (M. L. Glass, R. G. Boutilier, and N. Heisler, manuscript in preparation). The study emphasizes the temperature-dependence
of the ventilatory responses to hypoxia. Thus at IOOC ventilation
did not increase until
Pao, fell to 5 Torr. In contrast, at 30°C ventilation
approximately
doubled
as Pao, decreased from 60 to 30 Torr (Fig. 3). These responses correlate with
the ability of the turtle to maintain normal To2 despite a decrease in Pao,.
254
M. L. GLASS
AND
S. C. WOOD
Vohme
63
C. Receptor Sys t erms
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
Investigators
have studied several receptor systems in relation to the
chemical control of breathing in reptiles, but only a few species have been
examined. Therefore it is difficult to generalize concerning such receptor
systems. Moreover some data suggest the systems may be different for various groups of reptiles.
The most extensive data on PO, receptors are available for the tortoise
Testudo horsfieZdi (10). In Testudo bilateral vagotomy abolishes ventilatory
responses to hypoxia and hyperoxia, which suggests that Po2-sensitive receptor systems are innervated by the vagus nerves and provide a tonic drive
to breathing. Some evidence indicates that the receptors are screening pulmonary arterial blood, but their exact location is not known (10).
In mammals, Po2-sensitive receptors are located at the bifurcations
of
the external and internal carotids (32, 73), whereas the carotid bodies are
situated at the common cdrotid in birds (150). A careful anatomical study
(3) failed to demonstrate
carotid bodies in reptiles. However, Frankel et al.
(52) claim an ovoid structure is situated at the bifurcation
of the carotid
arteries in Pseudemys, but they have not provided evidence for the functional
role of this structure.
Although only a few species have been studied, the available information
on CO2 and pH receptors suggests interesting perspectives. The presence of
intrapulmonary
CO2 receptors in lizards is well established (50), and Hitzig
and Jackson (76) have discovered central nervous pH receptors in turtles.
Moreover there is some evidence for peripheral COZ receptors in the tortoise
Testudo horsfieldi (11).
The presence of intrapulmonary
COZ receptors in the lizard Tupinambis
teguixin was first proposed by Gatz et al. (55), who measured an immediate
decrease in ventilation
with abrupt lowering of PACT,. An intrapulmonary
location for the receptors for this response was strongly indicated because
vascular isolation of the lung did not abolish the ventilatory
response. Later
studies confirmed that CO2 receptors cover large pulmonary
areas in Tupinambis (136) and that output of these receptors increased with decreases in
PACT, (50). The CO2 receptors are insensitive to stretch of the lung in contrast
to pulmonary
mechanoreceptors
in Tupinambis.
These mechanoreceptors
may also be sensitive to changes in PACES,but they are not as sensitive as
the CO2 receptors (50). Carbon dioxide-sensitive
mechanoreceptors
are also
located in turtle lungs but seem to be of limited importance
in ventilatory
responses to CO2 inhalation
(95, 111, 112). In Chqysemys picta the mechanoreceptors are involved in the regulation
of VT, whereas the response to
CO2 inhalation primarily
consists of a shortening of the NVPs (95, 113).
The intrapulmonary
CO2 receptors of Tupinambis have not been reported
for other reptiles. Intrapulmonary
COZ receptors are well established in
birds, however (21, 137). The avian and lacertilian intrapulmonary
CO2 receptors may be functionally
similar, whereas the mechanoreceptors
in turtle
January
1983
RESPIRATION
IN
REPTILES
255
VI.
CONCLUSIONS
Substantial progress has occurred over the past decade in understanding
respiration
and its control in reptiles. Information
has accumulated concerning values for variables in respiratory function. A large difference in O2
requirements
between reptiles and endothermic
vertebrates
is clearly reflected on all levels of aerobic metabolism.
The lower O2 requirements
of
reptiles imply that values for pulmonary ventilation
and perfusion are also
low by mammalian
standards and that continuous ventilation
of the lungs
is not required to supply sufficient Oz. Instead breathing
activity is interrupted by breath-hold
periods. Correspondingly
pulmonary
perfusion and
gas exchange are periodic, with peak perfusion occurring during breathing
activity. The cyclic character of ventilation
and pulmonary perfusion implies
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
lungs belong to a type widespread among vertebrates with pulmonary ventilation (49).
Central nervous receptors sensitive to the acid-base status of the cerebrospinal fluid (CSF) have been extensively studied in mammals (cf. 97)
but were unknown in ectothermic vertebrates until recently, when such receptors were reported in Pseudemys scripta (75, 76). Subnormal pH values
of the CSF in Pseudemys cause a pronounced increase in ACRs (76). Significantly the magnitude of this response was independent of body temperature (76). The information
from this specifically pH-sensitive receptor system overrides the peripheral receptor’s input to the central nervous system
(76). The ventilatory
response to the decreased pH of the CSF occurs by an
elevated f value. Values for VT, however, also increase during CO2 inhalation.
This suggests that VT and f in Pseudemys are regulated by independent
receptor systems (75).
The studies on central receptors in Pseudemys provide important
keys
to the relative roles of receptors, but more studies are needed to quantify
their relative importance and in particular to relate receptor function to the
normal breathing patterns of the animals. Furthermore
(as is often the case
in reptilian physiology) too few species have been too little studied.
An important
question must still be answered: Do reptiles possess a
receptor system that functions in relation to an increase of ventilation
with
temperature?
Reeves (131) proposed that such receptors could be sensitive
to the net protein charge of the blood, which should remain constant despite
variations in body temperature.
A recent study by Davies et al. (41) reports that the alligator defends
net protein charge at all body temperatures.
The increase in ACRs for a
given change in net protein charge of arterial blood proved to be independent
of body temperature.
This may provide an important key, but not all reptiles
regulate net protein charge when body temperature
changes; furthermore
the alphastat receptors have not yet been located.
256
M. L. GLASS
AND
S. C. WOOD
Volume
63
We thank
Professor
Kjell Johansen
for useful comments
on several
versions
of the manuscript.
We are also grateful
for comments
by Dr. D. C. Jackson
and Dr. D. P. Toews.
We also
acknowledge
assistance
from Kirsten
Horup
in preparing
the manuscript.
M. L. Glass was the recipient
of a fellowship
from the Alexander
von Humboldt-Stiftung
during
much of the time needed to prepare
this review.
REFERENCES
1. ACKERMANN,
R. A., AND F. N. WHITE. Cyclic carbon
dioxide exchange in the turtle Pseudemys scripta Physiol. Zool. 52: 378-389, 1979.
2. ACKERMANN,
R. A., AND F. N. WHITE. The effects of
temperature and acid-base balance and ventilation of the
marine iguana. Respir. Physiol 39: 133-147, 1980.
3. ADAMS, W. E. The Comparative Morphology of the Carotid Body and Carotid Sinus. Springfield, IL: Thomas,
1958.
4. ADARO, F., P. SCHEID, J. TEICHMANN, AND J. PIIPER.
A rebreathing method for estimating pulmonary Ds:
theory and measurements in dog lungs. Respir. Physiol.
18: 43-63, 1973.
5. ALTLAND,
P. D. AND M. PARKER. Effects of hypoxia
upon the box turtle. Am J Physiol. 180: 421-427, 1955.
6. ANDERSEN, H. T. Physiological adjustments to prolonged diving in the American alligator, Alligator mississippiensis. Acta Physiol Scund 53: 23-45, 1961.
7. BELKIN, D. A. Anoxia: tolerance in reptiles. Science 139:
492-493, 1963.
8. BELKIN, D. A. Variations in heart rate during voluntary
diving in the turtle Pseudemys concinna Copeia 1964:
321-336, 1964.
9. BELKIN, D. A. Aquatic respiration and underwater survival of two freshwater
turtle species. Respir. Physid
4: 1-14, 1968.
10. BENCHETRIT,
G., J. ARMAND, AND P. DEJOURS. Ventilatory chemoreflex drive in the tortoise Testudo horsfieldi. Respir. Physiol 31: 183-191, 1977.
11. BENCHETRIT,
G., AND P. DEJOURS. Ventilatory
COa
drive in the tortoise Testudo hors&e,!.& J. Exp. Biol 87:
229-236, 1980.
12. BENEDICT, F. G. The Physiology of Large Reptiles.
Washington, DC: Carnegie Inst., Publ. 425, 1932.
13. BENNETT, A. F. A comparison of activities of metabolic
enzymes in lizards and rats. Comp. Biochxm. Physiol B
42: 637-647, 1972.
14. BENNETT, A. F. Ventilation in two species of lizards
during rest and activity. Comp. Biochem Physiol. A 42:
653-671, 1973.
15. BENNETT, A. F., AND W. R. DAWSON. Aerobic and anaerobic metabolism during activity in the lizard, Dips+
saurus dorsalis. J. Camp. Physiol. 81: 289-299, 1972.
16. BENNETT, A. F., AND W. R. DAWSON. Metabolism. In:
Bio&y of the Reptilia. Physiology A, edited by C. Gans
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
that measurements
must be performed over prolonged periods. Prolonged
measurements are also needed to assess the metabolic status of the animal.
Moreover data should be obtained at several body temperatures,
because
variables such as pulmonary
diffusing capacity, perfusion, and ventilation
all increase along with O2 uptake when body temperature
increases. Interspecies comparisons are thus impossible unless the temperature
dependence
of the compared variables is known.
Reptiles are different from mammals or birds in being highly tolerant
of a lack of 0,; in addition, reptiles tolerate variations in acid-base status
that would be fatal to endotherms. In spite of this ability, reptiles possess
regulatory systems to monitor acid-base status and blood oxygenation.
Recently several receptor systems have been reported in relation to these regulatory responses, but the relative roles of these systems are incompletely
known. These include intrapulmonary
CO2 receptors, PO, receptors, and central nervous pH receptors.
During the past decade several studies have addressed general theories
concerning effects of changes in body temperature
on acid-base regulation
in ectotherms. Studies on acid-base regulation in alligators and turtles agree
to some extent with predictions of these theories, whereas data on some
lizards do not conform. Therefore it seems that further experimental
work
is needed to evaluate and modify current theories.
January
17.
18.
19.
20.
22.
23.
24,
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
RESPIRATION
and W. R. Dawson. New York: Academic, 1976, vol. 5, p.
127-224.
BENTLY, P. J. Osmoregulation. In: BioZogy of the Rep
tibia. PhysioZogy A, edited by C. Gans and W. R. Dawson.
New York: Academic, 1976, vol. 5, p. 365-413.
BERKSON, H. Physiological adjustments to prolonged
diving in the Pacific green turtle (Chelonia mydus ugas&ii). Comp. B&hem, PhysioL 18: 101-119, 1966.
BIeRCK, G., B. JOHANSSON, AND H. SCHMID. Reactions of hedgehogs, hibernating and non-hibernating,
to
inhalation of oxygen, carbon dioxide and nitrogen. Actu
PhysioL Scand 37: 71-83, 1956.
BOHR, C. uber die spezifische Titigkeit
der Lungen bei
der respiratorischen
Gasaufnahme und ihr Verhalten zu
der durch die Alveolenwand stattfindenden Gasdiffusion.
Skand Arch. Physiol 22: 221-280, 1909.
BOUVEROT, P. Control of breathing in birds compared
with mammals. Physiol Rev. 58: 604-655, 1978.
BOYER, D. R. Hypoxia: effects on heart rate and respiration in the snapping turtle. Science 140: 813-814,1963.
BROWN, C. R., AND J. P. LOVERIDGE.
The effect of
temperature on oxygen consumption and evaporative
water loss in Crocodylus n&.&us. &nap. Biochem PhysioL A 69: 51-57, 1981.
BURGGREN, W. W. A quantitative
analysis of ventilation tachycardia
and its control on two chelonians,
Pseudemys scripta and Testudo graeca J Exp. BioL 63:
367-380,1975.
BURGGREN, W. W. The pulmonary circulation of the
chelonian reptile: morphology,
haemodynamics
and
pharmacology. J. Comp. PhysioL 116: 303-323, 1977.
BURGGREN, W. W., M. L. GLASS, AND K. JOHANSEN.
Pulmonary ventilation: perfusion relationships
in terrestrial and aquatic chelonian reptiles. Can, J. Zod 55:
2024-2034,1977.
BURGGREN, W. W., M. L. GLASS, AND K. JOHANSEN.
Intrapulmonary
variation of gas partial pressures and
ventilation inequalities in chelonian reptiles. J. Comp.
Physiol 126: 203-209, 1978.
BURGGREN, W. W., AND G. SHELTON. Gas exchange
and transport during intermittent breathing in chelonian
reptiles. J. Exp. BioL 82: 75-92, 1979.
CARR, A. Hundbook of Turtles. Ithaca, NY: Cornell Univ.
Press, 1952.
CLARK, B. D., C. GANS, AND H. I. ROSENBERG. Airflow in snake ventilation. Respir. PhysioL 32: 207-212,
1978.
CLARK, V. M., AND A. T. MILLER, JR. Studies on anaerobic metabolism in the fresh-water turtle (Pseudemys
scripta elegans). Camp. B&hem, PhysioL A 44: 55-62,
\
1973.
COMROE, J. H., JR. The peripheral chemoreceptors. In:
Handbook of Physiology. Respiration, edited by W. 0.
Fenn and H. Rahn. Washington, DC: Am. Physiol. Sot.,
1964, sect. 3, vol. 1, chapt. 23, p. 557-583.
COULSON, R. A., AND J. D. HERBERT. Relationship
between metabolic rate and various physiological and
biochemical parameters. A comparison of alligator, man
and shrew. Comp. B&hem, PhysioL A 69: 1-13, 1981.
COULSON, R. A., AND T. HERNANDEZ.
Biochemistrl/
of the Alligator. A Study of Metabolism in Slow Motion.
Baton Rouge, LA: Louisianna State Univ. Press, 1964.
COULSON, R. A., AND T. HERNANDEZ.
Oxygen debt
in reptiles: relationship between the time required for
repayment and metabolic rate. Comp. B&hem
PhysioL
A 65: 453-457, 1980.
CRAGG, P. A. Ventilatory patterns and variables in rest
IN
37.
38.
39.
40.
41
42
43
44
45
46
47
48.
49.
50.
51.
52.
53.
54.
55.
REPTILES
257
and activity in the lizard Lacerta, Comp. B&hem. PhysioL A 60: 399-411, 1978.
CRAWFORD,
E. C., JR., R. N. GATZ, H. MAGNUSSEN,
S. F. PERRY, AND J. PIIPER. Lung volumes, pulmonary
blood flow and carbon monoxide diffusing capacity of turtles. J Comp. PhysioL 107: 169-178, 1976.
CRAWFORD,
E. C., JR., AND R. R. SCHULTETUS.
CUtaneous gas exchange in the lizard Suuromulus obesus.
Cope,iu 1970: 179-180,197O.
DANTZLER, W. H. Renal function (with special emphasis on nitrogen excretion). In: BioZogy of the Reptilicz.
Physiobgy A, edited by C. Gans and W. R. Dawson. New
York: Academic, 1976, vol. 5, p. 447-504.
DAVIES, D. G. Temperature-induced
changes in acidbase status in the alligator, A&g&or mi.ssissippien&. J.
AppL PhysioL: Reqwirat. Environ. Exercise PhysioL 45:
922-926, 1978.
DAVIES, D. G., J. L. THOMAS, AND E. N. SMITH. Effect
of body temperature on ventilatory
control in the alligator. J. AppL PhysioL: Respirat. Environ
Exercbe
Physiol 52: 114-118, 1982.
DAVIES, P. M. C., AND E. L. BENNETT. Non-acclimatory
latitude-dependent metabolic adaptation to temperature
in juvenile natricine snakes. J. Comp. PhysioL 142: 489494,198l.
DEJOURS, P. Principle-s of Comparative Respiratory
PhysioZogy. New York: Elsevier, 1975.
DESSAUER, H. C. Blood chemistry of reptiles: physiological and evolutionary aspects. In: Biobgy of the Rep
tiliu, edited by C. Gans and T. S. Parsons. New York:
Academic, 1970, vol. 3, p. l-54.
DILL, D. B., AND H. T. EDWARDS. Respiration and
metabolism in a young crocodile (Crocodylus acutus Cuvier). Copeia 1931: l-3, 1931.
DUNCKER, H.-R. General morphological principles of
amniotic lungs. In: Respiratory Function in Birds, Adult
and Embyonic, edited by J. Piiper. Berlin: Springer-Verlag, 1978, p. 2-15.
DUNSON, W. A. Aquatic respiration in Trionyx spin+r
aqwr. Herpetologica 16: 277-283, 1960.
ELSE, P. L., AND A. J. HULBERT. Comparison of the
“mammal machine” and the “reptile machine”: energy
production. Am J PhysioL 240 (Regulatory Integrative
Comp. PhysioL 9): R3-R9, 1981.
FEDDE, M. R., AND W. D. KUHLMANN.
Intrapulmonary
carbon dioxide-sensitive
receptors: amphibians to mammals: In: Respiratory Function in Birds, Adult and Emhonic, edited by J. Piiper. Berlin: Springer-Verlag,
1978,
p. 33-50.
FEDDE, M. R., W. D. KUHLMANN,
AND P. SCHEID.
Intrapulmonary
receptors in the Tegu lizard: I. Sensitivity to COz. Respir. PhysioL 29: 35-48,1977.
FORSTER, R. E., AND E. D. CRANDALL. Pulmonary gas
exchange. Annu. Rev. PhysioL 38: 69-95, 1976.
FRANKEL, H. N., A. SPITZER, J. BLAINE, AND E. P.
SCHOENER. Respiratory
responses of turtles (Pseudemys scripta) to changes in arterial gas composition.
Comp. Biochem PhysioL 31: 535-546, 1969.
GANS, C., AND B. D. CLARK. Air flow in reptilian ventilation. Camp. Biocti
PhysioL A 60: 453-459,1978.
GATTEN, R. E., JR. Effects of temperature and activity
on aerobic and anaerobic metabolism and heart rate in
the turtles Pseudemys scriptu and Terrapene orruzta
Camp. Biochem PhysioL A 48: 619-648, 1974.
GATZ, R. N., M. R. FEDDE, AND E. C. CRAWFORD, JR.
Lizard lungs: COz-sensitive receptors in Tupinumbis nigropunctatus. Experientia 31: 455-456, 1975.
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
21.
1983
258
M. L. GLASS
71. HEISLER, N. Bicarbonate exchanges between body compartments after changes of temperature in the larger
spotted dogfish (Scyliorhinus stellaris). Respir. PhysioL
33: 145-X0,1978.
A. M. Energy metabolism as related to
72. HEMMINGSEN,
body size and respiratory surfaces and its evolution. Rep.
Steno. Mem Hosp. Nurd Insulinlub. 9: 7-110, 1960.
HEYMANS, C., J.-J. BOUCKAERT, AND L. DAUTREBANDE. Sinus carotidien et reflexes respiratoires.
II.
Influences respiratoires reflexes de l’acidose, de l’alcalose,
de l’anhydride carbonique, de l’ion hydrogene et de
l’anoxemie. Sinus carotidien et echanges respiratoires
dans les poumons et au dela des poumons. Arch. Ink
Phar??Lac&yn Ther. 39: 400-450, 1930.
HICKS, J. W., M. L. RIEDESEL, AND M. L. GLASS. Ventilation and gas exchange in Thumwphis elegans after
S. C. WOOD
75.
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86
87
88.
89.
90.
91.
92.
Vot!um
63
acute and chronic exposure to various thermal environments (abstr.). J. Co& Wgo. Acud Ski 2: 99-100, 1979.
HITZIG, B. M. Control of ventilation by central respiratory chemosensors in the unanesthetized turtle, Pseudemys scripta ekgans (PhD Thesis). Providence, RI: Brown
Univ., 1977.
HITZIG, B. M., AND D. C. JACKSON. Central chemical
control of ventilation in the unanesthetized turtle. Am
J. PhysioL 235 (Regulatory Integrative Comp. PhysioL 4):
R257-R264, 1978.
HOWELL,
B. J., F. W. BAUMGARDNER,
K. BONDI,
AND H. RAHN.
Acid-base balance in cold-blooded vertebrates as a function of body temperature.
Am J.
PhysioL 218: 600-606, 1970.
HOWELL, B. J., AND H. RAHN. Regulation of acid-base
balance in reptiles. In: Biology of the Reptilia PhysioZogy
A, edited by C. Gans and W. R. Dawson. New York: Academic, 1976, vol. 5, p. 335-364.
HUGHES, G. M., R. GAYMER, M. MOORE, AND A. J.
WOAKES. Respiratory
exchange and body size in the
Aldabra giant tortoise. J. Exp. Bid 55: 651-665, 1971.
JACKSON, D. C. Metabolic depression and oxygen depletion in the diving turtle. J. AppL PhysioL 24: 503-509,
1968.
JACKSON, D. C. The effect of temperature on ventilation
in the turtle Pseudemys scripta ekgans. Respir. PhysioL
12: 131-140,197l.
JACKSON, D. C. Ventilatory response to hypoxia in turtles at various temperatures. Respir. PhysioL 18: 178-187,
1973.
JACKSON, D. C. Respiratory
control and CO2 eonductance: temperature effects in a turtle and a frog. Respir.
PhysioL 33: 103-114, 1978.
JACKSON, D. C. Respiratory
control in air-breathing
ectotherms. In: Research Topics in Physiology. Regulation
of Ventilation and Gas Exchange, edited by D. G. Davies
and C. B. Barnes. New York: Academic, 1978, vol. I, p.
93-130.
JACKSON, D. C., J. ALLEN, AND P. K. STRUPP. The
contribution
of non-pulmonary
surfaces to CO2 loss in
6 species of turtles at 20°C. Camp. Biochem PhysioL A
55: 243-246, 1976.
JACKSON, D. C., AND R. D. KAGEN. Effects of temperature transients on gas exchange and acid-base status
of turtles. Am J PhysioL 230: 1389-1393, 1976.
JACKSON, D. C., D. R. KRAUS, AND H. D. PRANGE.
Ventilatory response to inspired COz in the sea turtle:
effects of body size and temperature. Respir. PhysioL 38:
71-81, 1979.
JACKSON, D. C., S. E. PALMER, AND W. L. MEADOW.
The effects of temperature and carbon dioxide breathing
on ventilation and acid-base status of turtles. Respir.
PhysioL 20: 131-146, 1974.
JACKSON, D. C., AND H. D. PRANGE. Ventilation and
gas exchange during rest and exercise in adult green sea
turtles. J. Comp. PhysioL 134: 315-319, 1979.
JACOBSON, E. R., AND W. G. WHITFORD.
The effect
of acclimation on physiological responses to temperature
in the snakes, Thumnophis proximus and Natrix rhom&j&a Comp. Biochem, PhysioL 35: 439-449,197O.
JAMMES, Y., AND C. GRIMAUD. Ventilation, pulmonary
and cutaneous gas exchange in the awake lizard h&
viridis. Camp. Biochem PhysioL A 55: 279-285, 1976.
JOHANSEN, K., W. W. BURGGREN, AND M. L. GLASS.
Pulmonary stretch receptors regulate heart rate and pulmonary blood flow in the turtle Pseudemys scripta Camp.
B&&em PhysioL A 58: 185-191, 1977.
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
56. GIORDANO, R. V., AND D. C. JACKSON. The effect of
temperature on ventilation in the green iguana. Comp.
Biochem PhysioL 45: 235-238,1973.
57. GLASS, M. L., W. W. BURGGREN, AND K. JOHANSEN.
Ventilation in an aquatic and in a terrestrial
chelonian
reptile. J. Exp. BioL 72: 165-179, 1978.
58. GLASS, M. L., J. W. HICKS, AND M. L. RIEDESEL. Respiratory responses to long-term temperature exposure
in the box turtle, Terrapene ornuta J. Comp. PhysioL 131:
353-359, 1979.
59. GLASS, M. L., AND K. JOHANSEN. Control of breathing
in Acrochordw javanicus, an aquatic snake. PhysioL ZooL
49: 328-340, 1976.
60. GLASS, M. L., AND K. JOHANSEN. Periodic breathing
in the crocodile CrocodyZus niloticus. J. Exp. ZooL 208:
319-326,1979.
Pulmonary oxygen
61. GLASS, M. L., AND K. JOHANSEN.
diffusing capacity of the lizard Tupinumbis teguixin. J.
Exp. ZooL 219: 385-388,1982.
62. GLASS, M. L., K. JOHANSEN, AND A. S. ABE. Pulmonary diffusing capacity in reptiles (relations to temperature and Oz-uptake). J. Camp. PhysioL 142: 509-514,198l.
63. GLASS, M. L., S. C. WOOD, R. W. HOYT, AND K. JOHANSEN. Chemical control of breathing in the lizard
Varanus exunthemuticua. Comp. B&hem
PhysioL A 62:
999-1003,1979.
The
64. GLASS, M. L., S. C. WOOD, AND K. JOHANSEN.
application
of pneumotachography
on small unrestrained animals. Camp. Biock
PhysioL A 59: 425-427,
1978.
in the sea snake
65. GRAHAM, J. B. Aquatic respiration
Pelumis pluturus. Respir. PhysioL 21: l-7, 1974.
66. GRATZ, R. K. Ventilatory response of the diamondback
water snake, Natrix rhomln@ra, to hypoxia, hypercapnia
and increased oxygen demand. J. Comp. PhysioL 129: 105110,1979.
67. GRATZ, R. K., A. AR, AND J. GEISER. Gas tension profile of the lung of the viper, Vipera xunthinu pakstinue.
Respir. PhysioL 44: 165-176, 1981.
Energetics for ac68. GRATZ, R. K.! AND H. HUTCHISON.
tivity in the diamondback water snake, Natrix rhombifma PhysioL Zool. 50: 99-114, 1977.
69 GRIGG, G. C. Metabolic rate, Q10 and respiratory quotient (RQ) in Crocod&s
porosus, and some generalizations about low RQ in reptiles. PhysioL ZooL 51: 354-361,
1978.
70 HAZEL, J. R., W. S. GARLICK, AND P. A. SELLNER.
The effects of assay temperature upon the pH optima of
enzymes from poikilotherms:
a test of the imidazole alphastat hypothesis. J. Comp. PhysioL 123: 97-104, 1978.
AND
Janumy
RESPIRJ~TION
1983
110. MERTENS, R. The World of Amphibians and Reptilea
New York: McGraw-Hill,
1960.
111. MILSOM, W. K., AND D. R. JONES. Are reptilian pulmonary receptors mechano- or chemosensitive?
Nature
London 261: 327~323,1976.
112. MILSOM, W. K., AND D. R. JONES. Pulmonary receptor
chemosensitivity
and the ventilatory response to inhaled
CO, in the turtle. Respir. Physid 37: 101-107, 1979.
113. MILSOM, W. K., AND D. R. JONES. The role of vagal
afferent information
and hypercapnia in the control of
the breathing pattern in chelonia. J. Exp Bid 87: 52-63,
1980.
114. MITCHELL,
G. S., T. T. GLEESON,
AND A. F. BEN-
REPTILES
259
NETT. Pulmonary oxygen transport during activity in
lizards. Respir. Physid 43: 365-375, 1981.
115. MITHOEFER,
J. C. Breath holding. In: Handbud
4f
Phyeidc;;rgy. Respiratian, edited by W. 0. Fenn and H.
Rahn. Washington, DC: Am. Physiol. Sot., 1964, sec. 3,
vol. 2, chapt. 33, p. 1011-1026.
116. MOBERLY, W. R. The metabolic responses of the common iguana, Iguana *no,
to walking and diving. Conzp
B&n&em Physiol27: 21-37,1968.
117. NAIFEH,
K. H., S. E. HUGGINS,
H. E. HOFF, T. W.
HUGG, AND R. E. NORTON. Respiratory
patterns in
crocodilian reptiles. Resp+. Phyeid 9: 31-42, 1970.
118. NIELSEN, B. On the regulation of respiration in reptiles.
1. The effect of temperature and CO, on the respiration
of lizards (Lacertu). J. Em Bid 38: 301-304, 1961.
119. NIELSEN, B. On the regulation of respiration in reptiles.
2. The effect of hypoxia with and without moderate hypercapnia on the metabolism of lizards. J. Exp Bid 39:
107-117, 1962.
120. PERRY, S. F. Quantitative
anatomy of the lungs of the
red-eared turtle, P8faulemps scripta eltgana Respir.
Physid 35: !&G-262,1978.
121. PERRY, S. F., AND H.-R. DUNCKER. Interrelationship
of static mechanical factors and anatomical structure in
lung evolution. J. tip
Ph&d
138: 321~334.1980.
122. POUGH, F. H. Physiological aspects of burrowing of
sand lizards (&nu, &uunw)
and other lizards. hp
Bit&em
Physiol 31: 869-M&1969.
123. POUGH, F. H. Heart rate, breathing and voluntary diving of the elephant trunk snake, AcrocMw
javanicw
Camp Biachem. Phyti
A 44: l&189,1973.
124. POUGH, F. H. Blood oxygen transport and delivery in
reptiles. Am Zool 20: 173-185, 1980.
125. POUGH, F. H. The advantages of ectothermy in tetrapods. Am. Nat 115: 92-1X&1980.
126. PRANGE, H. D., AND D. C. JACKSON. Ventilation, gas
exchange and metabolic scaling of a sea turtle. &q++.
Phyti
27: 369-3’7’7, 1976.
127. RAHN, H. Gas transport from the external environment
to the cell. In: Develqpmen of the Lung, edited by U. S.
deReuck and R. Porter. Boston: Little, Brown, 1967, p. 223.
128. RAHN, H., AND W. 0. FENN. A Graphical Analysis crf
the Respiratory
Gas Exchange. Washington,
DC: Am.
Physiol. Sot., 1955.
129. RAHN, H., AND B. J. HOWELL.
The OH-/H+
concept
of acid-base balance: historical
development. wr.
Physiol 33: 91-97,1978.
130. RANDALL,
W. C., D. E. STULLKEN, AND W. A. HIESTAND. Respiration of reptiles as influenced by the composition of the inspired air. copeia 1944: 136-144, 1944.
131 REEVES, R. B. An imidazole alphstat hypothesis for
vertebrate
acid-base regulation: tissue carbon dioxide
content and body temperature
in bullfrogs. Respir
Phw
14: 219-236, 1972.
132. REEVES, R. B. Temperature-induced
changes in blood
acid-base status: pH and Pa in a binary buffer. J. Appl
Phyti
40: 752-761, 1976.
133. ROBIN, E. D., J. W. VESTER, H. V. MURDAUGH,
JR.,
AND J. E. MILLEN. Prolonged anaerobiosis in a vertebrate: anaerobic metabolism in the fresh water turtle.
J. C&U Cmnp PhvsioL 63: 287-297.1964.
134. ROMER, A. S. Skin breathing-primary
or secondary?
Respir. Physid 14: 183-192, 1972.
135. RUBEN, J. Aerobic and anaerobic metabolism during
activity in snakes. J. tip
Physid
109: 147-157, 1976.
136. SCHEID. P.. W. D. KUHLMANN.
AND M. R. FEDDE.
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
93. JOHANSEN,
K., C. LENFANT, MD D. HANSON. Phylogenetic development of pulmonary circulation. Fe&r
atian proc, Bid 29: 1124-1129,197O.
94. JOHLIN, J. M., AND F. B. MORELAND.
Studies of the
blood picture of the turtle after complete anoxia. J. Bid
them. 103: 107-114,1933.
95. JONES, D. R., AND W. K. MILSOM. Functional characteristics of slowly adapting pulmonary stretch receptors
in the turtle. J. Physid Landon 291: 37-49, 1979.
96. JONGH, H. J. DE, AND C. GANS. On the mechanism of
respiration in the bullfrog Runu cartesbsiana: a reassessment. J. Ado+&
127: 259~290,1969.
97. KELLOGG, R. H. Central chemical regulation of respiration. In: Handbook uf Physidogy. Respiration, edited
by W. 0. Fenn and H. Rahn. Washington,
DC: Am.
Physiol. Sot., 1964, sect. 3, vol. 1, chapt. 20, p. 507-534.
93. KINNEY, J. L., D. T. MATSUURA, AND F. N. WHITE.
Cardiorespiratory
effects of temperature
in the turtle,
Pwudem~jbridana
Reqir. Physid 31: 309~325,1977.
99. KLEMM, R. D., R. N. GATE, J. A. WESTFALL, AND
R. M. FEDDE. Microanatomy
of the lung parenchyma
of a tegu lizard %pinati
nigropunctat~
J. Mnphol
161: 25’7-280, 1979.
loo. KRISTOFFERSON,
R., AND A. SOIVIO. Hibernation in
the hedgehog (Erim
europaeus L.). Anrr. Acud Sci
Fenn Ser. A4 82: l-16,1964.
101. KROGH, A., AND 116.KROGH. Rate of diffusion of CO
into lungs of man. Skand Arch Ph@uL 23: 236-24?,1999.
R. C., AND W. A. CALDER, JR. A prelim102. LASIEWSKI,
inary allometric analysis of respiratory variables in resting birds. R.tspir. Physid 11: 152-166,197l.
103. LEGLER, J. M. Natural history of the ornate box turtle,
Tewxqwne ornata Agassiz. Univ. Kana Mwr Nat Hiat.
Mist Pzdd 11: 527-665,196O.
H. The effect of prolonged submersion on
104. LEIVESTAD,
the metabolic and heart rate in the toad (Bzcfo 6&o). Acta
Univ. Bergensis 5: 1-15, 1960.
C., AND K. JOHANSEN.
Respiration in the
105. LENFANT,
aethiopicwx I. Respiratory
African lung&h Pdopterw
properties of blood and normal patterns of breathing and
gas exchange. J. Exp Bid 49: 437-452,1968.
C., K. JOHANSEN,
J. A. PEDERSEN, AND
106. LENFANT,
K. SCHMIDT-NIELSEN.
Respiration in the fresh water
turtle Ch&sfinrbriata,
Respir. PhysiaL 8: 261-275, 1970.
107. LUCEY, E. C., AND E. W. HOUSE. Effect of temperature
on the pattern of lung ventilation and on the ventilationcirculation relationship in the turtle Pseudemys scriptu
Cbmp Biochem Physid A 57: 239-243,1977.
108. MALAN, A., T. L. WILSON, AND R. B. REEVES. Intracellular pH in cold-blooded vertebrates as a function of
body temperature. Respr. Physid 28: 29-47, 1976.
109. McCUTCHEON,
F. H. The respiratory
mechanism in
turtles. Physd
ZooL 16: 255-269, 1943.
IN
260
M. L. GLASS
AND
Vdume
68
ciples and Aduv,
edited by M. S. Gordon. New York:
Macmillan, 1972, p. 111-159.
151. WHITE, F. N. Circulation. In: Biology @ the Repcilia,
Phm
A, edited by C. Gans and W. R. Dawson. New
York: Academic, 1976, vol. 5, p. 2’75-335.
152 WHITE, F. N., AND G. ROSS. Circulatory changes during
experimental diving in the turtle. AM. J. Phpsid 211: 15
18,1966.
153. WITHERS, P. C. Acid-base regulation as a function of
body temperature in ectothermic toads, a heliothermic
lizard, and a heterothermic
mammal. J. M
Bid
3: 163-171,1978.
154. WOOD, S. C., M. L. GLASS, AND K. JOHANSEN. Effects
of temperature on respiration and acid-base balance in
a monitor lixard. J. &uzp Ph@d
116: 28’7~296.1977.
155. WOOD, S. C., AND K. JOHANSEN.
Respiratory
adaptations to diving in the Nile monitor lixard, Vumnus niloticua J. Cimp Physid 89: 145-X8,1974.
156. WOOD, S. C., K. JOHANSEN,
AND R. N. GATE. Pulmonary blood flow, ventilation/perfusion
ratio, and oxygen transport in a varanid lizard. Am J. Physid (Rep
ulutuq In@pmtive
http
Physid
2): 233: RS-lW3,
WM.
157. WOOD, S. C., K. JOHANSEN,
M. L. GLASS, AND R. W.
HOYT. Acid-base regulation during heating and cooling
.
in the lizard, Vamnw exa&hem&cw
J Appl Ph&ol:
Eizercke Physid
Re8pirat. Envim
50: T19-783,198l.
158. WOOD, S. C., K. JOHANSEN,
M. L. GLASS, AND
G. M. 0. MALOIY. Aerobic metabolism of the lizard Vur.
atczc8exan&m&cu~
effects of activity, temperature and
size. J.
Ph&d
127: 331336.1978.
159. WOOD, S. C., AND C. LENFANT. Respiration: mechanics,
control and gas exchange. In: Bw
d the Rep&&a
Physidogy A, edited by C. Gans and W. R. Dawson. New
York: Academic, 1976, vol. 5, p. 225274.
166. WOOD, S. C., AND W. R. MOBERLY. The influence of
temperature
on the respiratory
properties of iguana
blood. Req.+. Physid lo: 2O-29,197O.
161. YANCEY, P. H., AND G. N. SOMERO. Temperature dependence of intracellular
pH: its role in conservation of
pyruvate apparent Km values of vertebrate lactate dehydrogenases. J.
Ph@ol125: 129-134,1978.
C%nnp
Cbmp
Downloaded from http://physrev.physiology.org/ by 10.220.33.1 on September 12, 2016
Intrapulmonary
receptors in the tegu lizard. II. Functional characteristics
and localization. Beep+. Physid
29: 49-63.1977.
13’7. SCHEID, P., H. SLAMA, R. N. GATZ,AND M. R. FEDDE.
Intrapulmonary
Q
receptors in the duck. III. Functional localization. Be@-. Phw8id 22: 123-136, 1974.
138. SCHMIDT-NIELSEN,
K. Anid
Physidogy. Adaptatian
ud E&-me&.
London: Cambridge Univ. Press, 1975.
139. SEYMOUR, R. S. Gas tensions and blood distribution
in
sea snakes at surface pressure and at simulated depth.
Phjjsiol ZboL 51: 380-4071978.
146. SEYMOUR, R. S., AND M. E. D. WEBSTER. Gas transport and acid-base balance in diving sea snakes. J. E’
ad
191: 169-l&
1975.
141. SHELTON, G., AND W. BURGGREN. Cardiovascular
dynamics of the chelonia during apnoea and lung ventilation. J. Ezp Bti 64~ 323-343,1976.
142. SMITH, H. M., AND D. C. NICKON. Preliminary
experiments on the role of the cloaca1 bursae in hibernating
turtles. Not Hi& Mist 178: l-8,1961.
143. STAHL, W. R. Scaling of respiratory
variables in mammals. J. A&
Phpiol22:
a-460,1967.
144. STANDAERT,
T., AND K. JOHANSEN.
Cutaneous gas
exchange in snakes. J. tip
Ph@oi 89: 313~329,1974.
145. TAKEZAWA,
J., F. J. MILLER, AND J. J. O’NEIL. Singlebreath diffusing capacity and lung volumes in small laboratory mammals. J. Appl Phvsiuk Respimt Envim
Ezerciee Ph+L
48: 1652-1059,1986.
146. TEMPLETON,
J. R., AND W. R. DAWSON. Respiration
in the lixard mp/@s
adlaria Ph@d
ZooL 36: 104126,1963.
147. ULTSCH, G. R., AND D. C. JACKSON. Long-term submergence at 3°C of the turtle, Chtysemys p&a be&i, in
normoxic and severely hypoxic water. I. Survival, gas
exchange and acid-base status. J. Ezp Bid 96: 11-28,
1982.
148. WEST, J. B. Respiratory Phy8idogy-the
Etwntiak
Baltimore, MD: Waverly, 1974.
149. WHITE, F. N. Redistribution
of cardiac output in the
diving alligator. copeia 1963: 567-570,1969.
159. WHITE, F. N. Respiration. In: Animal Phy-:
Prin-
S. C. WO.OD