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1 Department of Medicine, University of California, San Diego, La Jolla 92093-0623; and 2 White Mountain Research Station, University of California, San Diego, La Jolla, California 92093-0689
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Many avian species exhibit an
extraordinary ability to exercise under hypoxic condition compared with
mammals, and more efficient pulmonary O2 transport has been
hypothesized to contribute to this avian advantage. We studied six emus
(Dromaius novaehollandaie, 4-6 mo old, 25-40 kg)
at rest and during treadmill exercise in normoxia and hypoxia (inspired
O2 fraction 
0.13). The multiple inert gas
elimination technique was used to measure ventilation-perfusion (
/
) distribution of the lung and calculate cardiac output and parabronchial ventilation. In both normoxia and hypoxia, exercise increased arterial PO2 and decreased arterial
PCO2, reflecting hyperventilation, whereas pH
remained unchanged. The / distribution was unimodal, with
a log standard deviation of perfusion distribution = 0.60 ± 0.06 at rest; this did not change significantly with either exercise or
hypoxia. Intrapulmonary shunt was <1% of the cardiac output in all
conditions. CO2 elimination was enhanced by hypoxia and
exercise, but O2 exchange was not affected by exercise in
normoxia or hypoxia. The stability of / matching under conditions of hypoxia and exercise may be advantageous for birds flying
at altitude.
inert gases; comparative gas exchange; altitude
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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BIRDS ARE KNOWN FOR THEIR extreme tolerance to hypoxia and the ability to cope with high O2 demands in hypoxia. For example, bar-headed geese use energetically expensive flapping flight to migrate at altitudes that would render an unacclimatized human unconscious (26). In hummingbirds, hovering flight results in the highest mass-specific O2 uptake in an exercising vertebrate, and this can be maintained up to simulated altitudes of 6 km (1). One of the most obvious differences in O2 transport between birds and mammals is the unique structure of their respiratory systems (17). The structure-function relationship of the avian respiratory system has been modeled and is hypothesized to confer an advantage for birds over mammals during exercise at altitude (16, 25). For instance, the cross-current model of gas exchange for avian lungs predicts a negative expired-arterial PO2 (PaO2) difference, whereas the best that can be achieved in mammals is zero.
The quantitative role of cross-current gas exchange in explaining
the abilities of birds at altitude is not clear, however. For example,
in extreme hypoxia, the advantage of cross-current gas exchange,
compared with alveolar gas exchange, is predicted to decrease
(25). At an altitude equivalent to the summit of Mount
Everest, cross-current exchange is predicted to provide an advantage
over alveolar exchange equivalent to descending 700 m
(25). Experiments on birds exercising in normoxia show
that gas exchange is similar to mammals (reviewed by Ref.
17). The only studies on birds exercising in hypoxia that
have measured all of the necessary data to calculate O2
exchange efficiency were done on bar-headed geese and Pekin ducks
running on a treadmill (6, 14). However, maximal
O2 consumption (O2) was not
reached by these flying birds during running exercise, and the measured O2 increased 1.5- to 3-fold, i.e., much
less than the levels expected during flapping flight to reach high altitudes.
Another limitation of previous studies is the inability to distinguish
between the different physiological factors that prevent gas exchange
from operating at ideal levels. The main factors are
ventilation-perfusion (/) heterogeneity and diffusion limitation. Distinguishing between these factors is complicated because / heterogeneity can affect gas exchange
"as if" there were a diffusion limitation. However, the
consequences of / heterogeneity and diffusion limitation
are not necessarily the same under different conditions (e.g., hypoxia
and normoxia), so one cannot extrapolate from experimental measurements
to other interesting situations in nature.
Therefore, this study was designed to quantify O2 exchange
and / heterogeneity in birds exercising in normoxia and
hypoxia. We chose emus because running is their normal mode of
locomotion. Running emus are capable of obtaining
O2 rates (corrected for body mass)
that are equivalent to those for flying birds and are significantly
greater than rates measured during running in birds that normally fly,
e.g., waterfowl (2). Furthermore, their large body
size permits multiple blood samples required for the multiple inert gas
elimination technique (MIGET) for measuring /
heterogeneity. We hypothesized that the avian lung would show improved
efficiency of gas exchange during hypoxic exercise compared with
mammalian lungs.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study was approved by the Animal Subjects Committee of the University of California, San Diego. Starting at 2 wk of age, 11 emus were trained to run on a treadmill (model 8203410H3N, Jaeger, Hoechberg, Germany) wearing a lightweight plastic mask constructed in our laboratory. Six of the emus of either sex, aged 4-6 mo, who were the best runners were selected for further study (weight 32 ± 5 kg, range 25-40 kg).
Surgical preparation. Surgical anesthesia was induced with diazepam (0.1 mg/kg im) followed by isoflurane 4-5% in 100% O2. The birds were intubated and their necks were wrapped lightly with an elastic (Ace) bandage to prevent inflation of the tracheal air sac. This air sac is used for vocalization and acts as increased anatomical dead space if allowed to inflate. Anesthesia was maintained with 2-3% isoflurane. Under sterile conditions, catheters were placed in the carotid artery (PE 90), the left jugular vein at the upper third of the neck (7-Fr, 24 cm), and a wing vein (PE 90). The catheter sites were cleaned, and catheters were flushed with heparin (1,000 IU/ml) and filled with a polyvinyl pyrrolidone (PVP)-heparin-saline solution (0.5 ml 5,000 IU heparin, 9.5 ml saline, 0.3 g PVP) to maintain patency. Animals were allowed to recover at least 24 h before study.
Protocol. On the day of the experiment, a triple-lumen Swan-Ganz catheter with thermistor (size 7-Fr) was inserted into the lumen of the jugular cannula, advanced via the external jugular vein and into the right ventricle, and when possible into the pulmonary artery, with the use of direct pressure monitoring. This catheter was used for sampling of pulmonary mixed venous blood and measurement of blood temperature. The experiments took place in a temperature-controlled ventilated room (21-23°C). Data were collected after at least 20 min of rest and after 5 min of exercise in normoxia and normobaric hypoxia [inspired O2 fraction (FIO2) = 0.13-0.14] at sea level. Running speed was increased to the maximum the bird could sustain (determined during previous training sessions). Each set of measurements included sampling of pulmonary mixed venous blood, arterial blood, and mixed expired gases for the multiple inert gas analyses, blood gases, cardiac output calculations, and metabolic rate measurements.
After normoxic measurements, hypoxic measurements at rest and during exercise were made at a simulated altitude of 3,300-4,000 m by adding nitrogen to a tent surrounding the treadmill to lower the FIO2 to 0.13-0.14. FIO2 and inspired CO2 fraction were monitored continuously by use of a mass spectrometer (Perkin-Elmer, MGA1100, Pomona, CA). Small amounts of nitrogen were added during the hypoxic study to maintain a constant FIO2. Because of logistical constraints, it was necessary to study hypoxia last, so the order of FIO2 was not randomized.Ventilation and metabolic measurements.
A custom-made face mask (without valves) was strapped to the animal's
head, and room air was drawn through the mask at a rate of 80 l/min at
rest and ~160 l/min during exercise by use of a vacuum. This bias
flow rate was determined to be sufficient to collect all expired gas by
testing for CO2 leak by using the mass spectrometer probe
placed at the back of the animal's mask. Room air was drawn around the
animal's face and mixed with the expired gas in a small, lightweight,
heated respiratory tubing (10.5 mm OD, Hans-Rudolph, Kansas City, MO)
leading into a heated mixing chamber. Total flow (i.e., bias and
expired gas) was measured by use of a pneumotachometer
(Fleisch no. 3) and integrated to obtain volume. Gas temperature and
relative humidity were measured in the gas stream adjacent to the
pneumotach. The expired concentrations of O2 and
CO2 were measured with the mass spectrometer during each
inert gas sample collection period, and
O2 and CO2 production (CO2) were calculated.
Multiple inert gas measurements. The MIGET was applied in the usual manner (19, 20, 29). The inert gas solution was prepared in 5% dextrose (7) and infused for ~20 min before collection of the resting samples and during the course of the study at a rate (in ml/min) of ~10% of the bias flow rate (in l/min) (for example, an infusion rate of 8 ml/min was matched to a bias flow of 80 l/min). This infusion rate provides excellent signal-to-noise ratio for all six inert gases at all exercise levels.
Quadruplicate 15-ml samples of mixed expired gas and duplicate 4-ml samples of pulmonary and systemic arterial blood were obtained in gas-tight syringes at rest and during exercise in normoxia and hypoxia for measurement of the steady-state concentrations of the six inert gases (SF6, ethane, cyclopropane, enflurane, ether, and acetone) by using a gas chromatograph (Hewlett-Packard 5890A, Wilmington, DE) (29). Solubility, retention (R, equal to the ratio of arterial to mixed venous partial pressure), and excretions (E, equal to the ratio of mixed expired to mixed venous partial pressure) for the inert gases were determined and corrected for body temperature, and/ distributions were calculated by
assuming a cross-current lung model (19). The second
moment of the vs. / distribution, exclusive of
intrapulmonary shunt (logSD), and the second
moment of the vs. / distribution, exclusive of
dead space (logSD), were used as indicators of
the degree of / heterogeneity, i.e., the greater the
logSD or the logSD, the greater
the / heterogeneity. The residual sum of squares (RSS)
was used as an indicator of the adequacy of fit of the data to the
cross-current model of the lung (19).
There was excessive loss of acetone in the expired gas samples, likely
due to difficulty in heating the mask with high bias flows while it was
on the animal. Therefore, we report data derived from five gases only.
The effect of the elimination of acetone from the analysis is a
decrease in the resolution of / distributions at
/ > 10. Without acetone, the next most soluble gas,
ether, allows the distinction of lung units with approximately
/ 
10 from dead space, which results in a dead
space similar to physiological dead space determined from
CO2 measurements (20). Hence, parabronchial
ventilation (P, analogous to alveolar ventilation in
mammals) was estimated as the product of (1 
dead space/tidal volume) times the bias flow rate, and P
includes any lung units with / < 10. To predict E
without the effect of dilution by dead space gas (E* i.e.,
end-parabronchial values, analogous to alveolar values in mammals), we
used the equation
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Hemodynamic measurements. Cardiac output was calculated from the mixed venous, arterial blood, and mixed expired inert gas concentrations by using the Fick principle of mass balance.
Statistical analyses. Data are presented as means ± SE. Repeated-measures ANOVA was used to statistically test changes in the dependent variables from rest to exercise and during normoxia and hypoxia. Significance was accepted at P < 0.05, two-tailed.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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For technical reasons, metabolic and respiratory parameters, as
well as venous blood gas samples and consequently calculated cardiac
output and / distributions were not obtained in all birds
under all conditions. The numbers of measurements obtained under different conditions are given in Tables
1 and
2.
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Metabolic and cardiorespiratory data.
Metabolic, ventilatory, and hemodynamic data are presented in Table 1.
During normoxia, the emus ran between 1.4 and 2.0 m/s, and both
O2 and
CO2 increased over fivefold. Hypoxia did
not significantly affect CO2 during
rest, although it tended to be higher, consistent with the increased
restlessness we observed in the emus during hypoxia. Both running speed
(1.04 m/s) and CO2 tended to be lower in
hypoxia than in normoxia, but this was not significant. Cardiac output
increased significantly between rest and exercise and between normoxia
and hypoxia, but there was no significant interaction between
O2 level and exercise. Both heart rate and increases in
calculated stroke volume contributed to increases in cardiac output.
Blood gases. Arterial and mixed venous blood gases are reported in Table 2. Exercise in normoxia decreased arterial PCO2 (PaCO2), increased arterial pH, and increased PaO2. Increased O2 extraction in tissues during exercise decreased mixed venous PO2, but this was not statistically significant. At rest, hypoxia caused hyperventilation, as indicated by decreased PaCO2 (P = 0.08). Exercise in hypoxia further increased hyperventilation (i.e., decreased PaCO2) but, arterial and venous pH were not increased in hypoxic exercise, suggesting a metabolic acidosis during hypoxia. Hematocrit decreased with successive blood sampling during the protocol, but these changes were not significant.
/ data.
Table 3 gives the average blood-gas
partition coefficients for the six inert gases used to measure
/ distributions; they are similar to those in other
species. Indexes of / distributions determined from the
MIGET are given in Table 4. The
goodness of fit of measured R and E data to those predicted for the
/ distributions can be judged by the RSS. When six gases
are used in the MIGET, RSS is expected to be >5 only 20% of the time
if the appropriate model of gas exchange is used (e.g., cross-current model in a bird and alveolar model in a mammal, cf. Ref.
19). The RSS decreases if fewer gases are used in the
analysis. With only five gases used to analyze the emu data (see
METHODS), RSS was >5 in 74% of the cases with an alveolar
model. However, RSS with a cross-current model was <2 in 100% of the
data sets. Therefore, inert gas elimination in the emu behaves
according to a cross-current but not an alveolar model, and
/ distributions were determined from the MIGET data by
using a cross-current model.
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/ distributions for an emu under the four conditions
studied. The distributions are centered near the overall
P/ (Table 4), and the mean of the
distributions shifts to a higher / value during exercise
(P < 0.05) and hypoxia (P = 0.07).
/ heterogeneity, as measured by the log standard
deviation of the distributions (logSD), did
not change with exercise or hypoxia, and shunt was <1% of cardiac
output under all conditions (Table 4).
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P, analogous to alveolar ventilation in mammals, can
be estimated from MIGET data as the difference between total measured ventilation and dead space ventilation predicted from the calculated / distribution. In this case, P equals
the difference between the total bias flow and the highest
/ compartment we were able to distinguish, i.e.,
/ > 10 (see METHODS).
P calculated in this way is consistent with the
changes observed in PaCO2 and CO2 (Tables 1 and 2). In normoxia,
P increased from 2.9 ± 0.2 l/min at rest to
20.4 ± 1.7 l/min during exercise. In hypoxia, P increased to 4.0 ± 0.7 l/min at rest and was
19.8 ± 2.0 l/min in exercise. The similar levels of
P in exercise during normoxia and hypoxia result in
a decreased PaCO2 during hypoxic exercise because the emus were not running as fast and
CO2 was lower (see above).
Changes in the overall effective parabronchial /
ratio (P/, Table 4) paralleled
the changes in P. In normoxia, P/ increased from 0.48 ± 0.04 at rest
to 1.66 ± 0.16 in exercise, and in hypoxia
P/ increased from 0.56 ± 0.04 to
1.39 ± 0.02 in exercise. There was a significant effect of
exercise and an interaction between exercise and hypoxia, but the
effect of hypoxia alone was not significant.
Figure 2 shows average R-E differences
for gases with different partition coefficients under the four test
conditions. Excretion values are corrected for dead space determined by
the MIGET analysis (including instrument and physiological dead space),
so the R-E* values plotted correspond to the difference between
arterial and end-parabronchial tensions. R-E* provides an index of the
effects of / heterogeneity on gas exchange, similar to
the effects of heterogeneity on the alveolar-arterial
PO2 difference (A-aDO2) in mammals. In mammals, minimum (or ideal) value for R-E* , or the
A-aDO2, is 0. However, R-E* can assume negative
values, and end-expired PO2 can exceed
PaO2 in birds because of cross-current gas
exchange.
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/
heterogeneity on gas exchange, as evidenced by R-E* becoming more
negative for the measured data points (Fig. 2, A and
B, 
) and the values predicted for the best-fit
/ distributions (Fig. 2, A and B,
dashed curves). Ideal R-E* values predicted for a homogeneous cross-current lung with the overall measured
P/ ratio (Fig. 2, solid curves) are less than
measured heterogeneous values for most gases. Hence, the decrease in
total area between the ideal and measured R-E* curves with exercise in
normoxia (Fig. 2, A vs. B) means that gas
exchange performance is improved by exercise in normoxia. The effects
of exercise during hypoxia (Fig. 2, C vs. D) are
smaller than the effects of exercise in normoxia. This is mainly
because hypoxia at rest improves gas-exchange performance (Fig. 2,
A vs. C), whereas the effects of heterogeneity
during exercise are similar during normoxia and hypoxia (Fig. 2,
B vs. D).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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During exercise, many mammals, including humans, experience
reduced efficiency of pulmonary O2 transport, as evidenced
by an increase in the A-aDO2 for O2
and, in some, a reduction in PaO2
(3). The mechanism of the increased
A-aDO2 is related to both /
inequality and pulmonary diffusion limitation of O2
transport. There are clear-cut species differences in the relative contribution of these two factors. For example, the horse experiences very little increase in / inequality, but the extent of
pulmonary diffusion limitation for O2 combined with
mechanical constraint of ventilation is sufficient to cause marked
arterial hypoxemia (24). Pigs, on the other hand,
experience an increase in / inequality with exercise but
no appreciable diffusion limitation (12). Humans
experience both / inequality and pulmonary diffusion
limitation, although the relative contributions of each to the
A-aDO2 varies between individuals and with
aerobic capacity (11). In many species, both pulmonary
diffusion limitation for O2 and increased /
inequality are worsened by hypoxia and hypoxic exercise
(10).
In contrast, / heterogeneity in emus did not increase
with exercise or with hypoxia. Table 5
summarizes available data on / distribution in
birds, reptiles, and mammals, including humans. During
normoxic exercise, as previously discussed, many mammals demonstrate an
increase in / heterogeneity with exercise, evidenced by
an increase in the logSD. The mechanism of the
increased / heterogeneity during exercise is unknown but
does not appear to be related to the structure of the mammalian lung
per se because it is observed to only a minimal extent in the horse and
is present to a similar degree in humans and reptiles.
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Various mechanisms of the increase in / inequality have
been proposed, including 1) a reduced common dead
space-to-tidal volume ratio and therefore reduced admixture of the
expired air, unmasking existing / heterogeneity present
at rest (27); 2) nonuniform pulmonary
vasoconstriction and increased pulmonary arterial pressure
(4); 3) interstitial edema (22,
23); or 4) ventilatory time-constant inequality
(27). None of these mechanisms have been investigated in
exercising birds; however, the rather nonelastic structure of the avian
lung may reduce the importance of those mechanisms relying on pressure
changes in the pulmonary tissue and/or microenvironment. In addition,
changes in the admixture of expired air as suggested above may be less important in birds because the dead space-to-tidal volume ratio is
relatively high in birds. The fact that racehorses show minimal increases in / heterogeneity with hypoxic exercise
demonstrates that not all alveolar lungs are equally susceptible to
such limitations. Hence it remains to be determined whether all avian
lungs are as immune to such limitations as the emus we studied, to
provide evidence for interstitial pulmonary edema as a possible
mechanism. It should be noted that the levels of exercise sustained by
the animals in this study are less than for animals in the wild. Thus caution should be used when interpreting these results.
Inert gas exchange in normoxic and hypoxic exercise.
In emus, we found smooth unimodal distributions of and
and no significant change in the amount of heterogeneity under different conditions. In contrast, a bimodal /
distribution has been described for anesthetized (normoxic, not
exercising) geese (20). The reasons for the differences
between these two species of birds are unknown but may reflect
differences between awake and anesthetized birds or species
differences. Also, we had limited ability to detect a high
/ mode as described for anesthetized geese because we
only used five gases in our analysis, with ether being the most
soluble. As discussed in METHODS, this limits our ability
to distinguish differences between / ratios >10.
Intrapulmonary shunting was minimal under all conditions, as reported
for geese (20).
/ heterogeneity measured in our emus under
all conditions was similar to that measured for just the main mode in
anesthetized geese, which had a logSD = 0.56 (20). However, despite a constant logSD in all of the measurement conditions, the mean blood flow was directed
to units with higher / ratio during exercise in both normoxia (0.32 ± 0.04 vs. 1.21 ± 0.0) and hypoxia
(0.35 ± 0.06 vs. 0.98 ± 0.06). This is because ventilation
increases to a greater extent than the corresponding increases in
perfusion, so the overall / ratio is increased.
The effect of / heterogeneity on a gas depends
on the gas solubility and can vary with a change in the overall
P/ despite a constant
logSD (28). For example, exercise in
normoxia increases the efficiency of exchange for a gas with partition
coefficient = 1 because R-E* decrease is more negative (Fig.
2A vs. 2B). This approach permits insights into
efficiency of CO2 and O2 gas exchange but only
if the dissociation curves are linear. This is approximated for
CO2 and O2 in hypoxia but not for
O2 in normoxia. Using partition coefficients of 0.6 and 6.0 for O2 and CO2, respectively (28), Fig. 2 predicts no significant change in effects of / on
O2 with exercise in hypoxia and a small decrease in the
effects on CO2. This is consistent with no change in
PaO2 and a small decrease in
PaCO2 in exercise vs. rest in hypoxia (Table
2).
Limitations of the study.
During normoxia, the emus ran between 1.4 and 2.0 m/s. This speed is
lower than the maximal speeds reported for emus running in the wild (14 m/s; Ref. 15) or achieved by emus in other studies (21). There was a small decrement in running speed due to
surgery and anesthesia, but it cannot account for all of the
differences seen between our animals and those in the wild. Running
speed in two birds decreased from 1.81 to 1.67 m/s and from 1.94 to 1.67 m/s after surgery. We suggest that our captive-bred birds were
simply not trained well enough to run faster. Before starting these
experiments, we were advised by other investigators that emus were
difficult to handle and that they would only run on a treadmill
reliably when running in a flock. This was impossible on our small
treadmill. Also, one of us had prior experience with emus suggesting
that they would be difficult to train. On the other hand, data had been
obtained from this species during treadmill exercise, albeit with
difficulty (8). We decided the preparation was worth
pursuing when we had success in running young emus on our treadmill.
However, as they grew and became large enough to study, they became
difficult to handle and difficult to keep on the treadmill even during
rest, and we were not able to make them run faster. Our emus may have
had reduced aerobic capacity from their captive lifestyle also. Our
emus showed a respiratory exchange ratio of 0.93 during normoxic
exercise and 0.96 during hypoxic exercise. It has been our experience
in exercising a variety of animals that it is difficult to exercise
animals at an intensity resulting in a respiratory exchange ratio 
1.
/ ratio of the lung, whereas /
heterogeneity remained unchanged. This behavior may provide an
advantage for birds exercising in hypoxia compared with mammals.
Increased metabolic needs with exercise were met by increased
cardiac output and ventilation, resulting in significantly
decreased PaCO2 in normoxia as well as in
hypoxia. The combined effect of the increased overall / ratio and no increase in heterogeneity resulted in improved
CO2 exchange in hypoxia and exercise, whereas
O2 exchange was not affected by exercise in normoxia or hypoxia.
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ACKNOWLEDGEMENTS |
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We thank Donna Allsopp, Nathalie Garcia, Lennard Gonzales, and Andrew Altman for skillful assistance with the bird training and handling and Mark Olfert, Nick Busan, Jeff Struthers, and Eric Falor for technical support.
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FOOTNOTES |
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This study was supported by the Deutscheforschungsgemeinschaft, by National Institutes of Health Grants HL-17731 and MO1 RR-00827, and by the University of California White Mountain Research Station.
Present address of P. M. Schmitt: Dept. of Internal Medicine, University of California, Davis, One Shields Ave., Davis, CA 95616-8636.
Address for reprint requests and other correspondence: S. R. Hopkins, Dept. of Medicine, Univ. of California, San Diego, 9500 Gilman Drive, 0623A, La Jolla, CA 92093-0623 (E-mail: shopkins{at}ucsd.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
August 16, 2002;10.1152/japplphysiol.01108.2001
Received 5 November 2001; accepted in final form 12 August 2002.
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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) vs. ventilation-perfusion ratio in a representative
emu at normoxic rest (A), normoxic exercise (B),
hypoxic rest (C), and exercise (D).
LogSD