/. exp. Biol. 142, 373-385 (1989)
printed in Great Britain © The Company of Biologists Limited 1989
373
GAS EXCHANGE AND AIR-SAC COMPOSITION IN THE
UNANAESTHETIZED, SPONTANEOUSLY BREATHING GOOSE
BY PETER SCHEID, M. ROGER FEDDE* AND JOHANNES PIIPER
Institut fur Physiologie, Ruhr-Universitdt, Bochum, FRG and
Abteilung Physiologie, Max-Planck-Institut fiir experimentelle Medizin,
Gb'ttingen, FRG
Accepted 15 November 1988
Summary
Gas exchange variables were measured in unanaesthetized domestic geese fitted
with rubber facemasks and indwelling air-sac and arterial catheters. The results
were analysed on the basis of functional models.
1. Ventilation was characterized by low frequency (8-4 min"1) and high tidal
volume (29-3 ml kg"1).
2. Average values (± S.E.) of arterial blood variables were as follows:
Po2 = 12-9 ± 0-2 kPa, PCO2 = 4-2±0-2kPa, pH = 7-52 ±001. Body temperature
was 41-4 ±0-2°C.
3. The gas exchange ratio (calculated with reference to inspired gas) of caudal
air sacs (average 1-09) was higher, and that of cranial air sacs (0-73) lower, than
that of mixed-expired (0-82) or end-expired gas (0-78). This pattern can be
explained by a higher effective ventilation/perfusion ratio in the neopulmo than in
the paleopulmo.
4. During inspiration, the neopulmo was estimated to contribute about 7 % to
the overall inspiratory O2 uptake, and about 18% to the CO2 output. Total
inspiratory gas exchange was twice that during expiration.
5. Arterial P ^ was close to, but Pco? lower than, the partial pressure in cranial
air sacs and in end-expired gas. This can be explained on the basis of a crosscurrent gas exchange system with unequal distribution of ventilation to perfusion
between functional compartments.
Introduction
After the experimental confirmation of unidirectional gas flow through the avian
lung, a number of theoretical and experimental studies have been devoted to
further analysis of gas exchange in avian lungs (reviewed by Scheid, 1979, 1982).
Only a few experimental studies have been conducted on unanaesthetized birds,
although it is accepted that anaesthesia affects respiration. Measurements of
ventilation and of respiratory gases in expired air, in air sacs and in blood have
been performed in unanaesthetized, lightly restrained pigeons (Bouverot et al.
Ikey words: air sacs, birds, blood gases, diffusing capacity, parabronchial gas exchange,
respiratory air flow.
374
P . S C H E I D , M. R. F E D D E AND J. PUPER
1976), ducks (Bouverot et al. 1979; Jones & Holeton, 1972), hens (Piiper et al.
1970) and geese (Cohn & Shannon, 1968). Notable are the studies on ducks (Kiley
et al. 1979) and hens (Brackenbury et al. 1981, 1982) running on the treadmill.
None of these experiments was designed, however, for a complete analysis of gas
exchange on the basis of the currently accepted pattern of respiratory gas flow and
the cross-current model for parabronchial gas exchange.
In this study, we investigated avian gas exchange by simultaneous analysis of
CO2 and O 2 in the various air sacs, in expired gas and in arterial blood. This
allowed partitioning of CO2 output and O 2 uptake between paleopulmo and
neopulmo and between inspiration and expiration. Particular attention was paid to
maintaining the awake birds in resting conditions with as little disturbance as
possible.
Materials and methods
Measurements were performed on 11 Embden breed domestic geese (Anser
anser) weighing 3-5-7-6kg (average 5-0kg). Initially, measurements were made
during one or more days on intact, awake, resting geese. The birds were then
anaesthetized, and indwelling air-sac and vascular catheters were installed. The
animals were allowed to recover for at least 2 days before measurements,
including determination of air-sac gas concentration and arterial blood values on
birds in the awake, resting state, were resumed. The birds were deprived of food
for approximately 12 h before measurements, but water was always available up to
the time of measurement.
Indwelling air-sac catheters were inserted under halothane anaesthesia (1-2%
in O 2 ). Perspex tubes, 4-10 cm long, with an inside diameter of 8 mm, were tightly
sealed in the clavicular, left cranial thoracic, left caudal thoracic and left
abdominal air sacs. The air-sac membranes were tied around the tubes, and the
skin was sutured to form an airtight seal. A Perspex cap was screwed to the tube to
seal the sac. Intramuscular injections of antibiotic (Ampicillin) were given to help
prevent infection.
Prior to measurement of air-sac gas concentrations, the cap on each air-sac
cannula was removed and a plastic rod, in which was embedded a PE50 catheter,
was inserted into the air sac and sealed in place by a cap and two rubber washers.
The polyethylene catheter could be connected to the input of a mass spectrometer
(Scheid, 1983) to provide continuous measurements of air-sac gas composition.
Necropsy of the birds following the experiments verified the correct placement of
the catheters.
A polyethylene catheter was placed in the left brachial artery for sampling of
arterial blood.
Measurements
On the days of the experiments, the birds were blindfolded and lighth|
restrained in a metal stand in such a way as to allow normal breathing movements.
Gas exchange in the goose
375
Fig. 1. Set-up for measurement of gas exchange in the awake goose. For details, see
text. V, flow, measured by pneumotachograph; Fi, FE', fractions (of O2 and CO2) in
gas flowing to the face mask and obtained from the nostril. Air sacs with indwelling
Perspex tubes: Clav, clavicular; CrTh, cranial thoracic; CdTh, caudal thoracic; Abd,
abdominal.
Two polyethylene catheters (PE50) were taped to the bill (Fig. 1). One was
inserted into the left nostril for measurement of expired P ^ and Pco? profiles; the
other was placed in the dorsal midline, proximal to the nostrils, for measurement
of inspired gas composition. A foam rubber facemask was placed over the bill and
secured with rubber bands around the back of the head. The mask was sealed
airtight to the face with machine grease. The polyethylene catheters were
connected to the input capillary of the mass spectrometer for measurement of
fractional concentrations of CO2 and O2 in inspired and end-expired gas.
The mask contained a mid-dorsal port through which room air was passed at a
constant flow (5-61min~ 1 ) that was maintained slightly above peak inspiratory
flow to prevent reinhalation of expired gas. The air passed over the bill and exited
at the tip of the mask through a hose connected to a Fleisch pneumotachometer
(size 0) and a Godart-Statham differential manometer.
The constant-flow signal was subtracted from the pneumotachogram by an
analog computer (Electronic Associates, Inc., model TR-20) and deviations from
this flow, caused by inspiration and expiration, were integrated to yield the tidal
volume (VT). The output signals from the mass spectrometer and the analog
omputer were recorded on a multichannel pen recorder (Gould-Brush, model
11).
Gas flowing out of the mask was collected into a 201, gas-tight bag, and the
376
P. S C H E I D , M. R. F E D D E AND J. PHPER
volume was measured in a calibrated spirometer. To check that no air leaked from
the mask, the inflow line was detached from the mask, the bird was temporarily
supplied with air from a second source, and gas flow from the detached inflow line
was directly measured with the spirometer.
Protocol
Determinations of ventilation and gas exchange were made on nine geese before
installation of the air-sac and vascular catheters. These measurements were
repeated on successive days in five of the birds. Up to three sets of measurements
were accomplished on a given day. Following cannulation, measurements including air-sac gas and blood gas determinations were made on seven birds, of which
five had been studied before air-sac cannulation. These measurements were
repeated on five successive days in one bird, and on two or more days in five birds.
The measurement sessions lasted from 2 to 4 h and they were discontinued if the
goose was not perfectly quiet.
Calculations
Partial pressures of O 2 and CO 2 and pH in arterial blood samples were
measured at body temperature with a conventional electrode system (BMS III,
Radiometer, Copenhagen, Denmark). This electrode system and the mass
spectrometer were calibrated with gases provided by precision gas-mixing pumps
(Type M30l/a-F, Wosthoff, Bochum, FRG). Blood gas correction factors for Po2
were determined for each experiment by equilibrating blood samples with gases of
known partial pressure. Body temperature was monitored using a thermistor
inserted 10cm into the colon. Fractions of respiratory gases were converted to
partial pressures at the animal's body temperature and the actual barometric
pressure, which averaged 99-7 kPa (S.D. =0-4kPa).
O 2 uptake (MQJ) and CO 2 output (McO2) were calculated using the inspired and
bag gas concentration difference, the volume of gas collected, and the time of
collection. Total (inspired) ventilation (Vi) was measured from the sum of the
inspired tidal volumes (Vi) during the collection period. Mixed expiratory
concentrations (FE) were calculated from the relationship:
FE = Fi - (Fi - F B ) V B / V I ,
(1)
where VB is the total gas volume collected in the bag, and Fi and FB are the
fractional concentrations of inspired and bag gas, respectively.
The Bohr dead space (VD) for CO 2 was calculated from the relationship:
VD/VT = (FE - F E ' ) / ( F I - FE') ,
(2)
where VT is the mean tidal volume, and FE' is the fractional concentration in endexpired gas, read from the mass spectrometer output when sampling through
catheter in the nostril, and averaged over this collecting period.
Gas exchange in the goose
311
The gas exchange ratio, R, for mixed-expired, end-expired and air-sac gases
(site x) with reference to inspired gas was determined according to the relationship:
where F , ^ was calculated as 1—FxCo2~ F xO2 . It is important to note that R denotes
the ratio CO 2 output/O 2 uptake only when applied to mixed-expired gas and, with
reasonable approximation, when applied to end-expired gas. R for air sacs is a
formal index from which information on the CO 2 output/ O 2 uptake ratio for the
paleopulmo and neopulmo during inspiration and expiration can be derived (see
Discussion).
Mean values were calculated for all measurements in a given bird before and
after air-sac cannulation. Overall mean values were calculated by averaging the
means from individual birds, giving each mean the same weight irrespective of the
number of measurements involved. This calculation of an overall mean meant that
birds with a large number of measurements did not influence the results more than
those with fewer measurements. A f-test was used to determine if mean values
before and after cannulation were significantly different. A one-way analysis of
variance was applied to determine if differences among arterial, cranial air-sac and
end-expired P C O 2 and P Oz values were significant (PsSO-05).
Results
After implanting indwelling air-sac and arterial cannulae, respiratory frequency
(f) and ventilation (Vi) were significantly decreased, and body temperature was
significantly increased (Table 1). No other measured variables were significantly
changed by the cannulation procedure. Most values were less variable after the
cannulations.
The CO 2 and O 2 partial pressures and the exchange ratios in expired gas and in
air sacs are shown in Table 2. There were only minor (but consistent) differences
between the air sacs of the cranial group (i.e. clavicular and cranial thoracic air
sacs) and between those of the caudal group (i.e. caudal thoracic and abdominal
air sacs), but there were large differences between the cranial and the caudal airsac groups. The cranial air sacs had higher Pco2> lower P O2 and lower R values than
the caudal air sacs. R values for end-expired and for mixed expired gases were
intermediate between those for caudal and cranial air sacs, but closer to the latter.
P CO2 was significantly lower in arterial blood than in end-expired (by 0-7 kPa on
average) and cranial air-sac gas (by 0-9 kPa on average) (Table 3). Significant
differences between cranial air-sac and end-expired PCO2 w e r e n o t observed. P O2
in arterial blood was not significantly different from that in cranial air-sac or endftxpired gas, but end-expired Po2 was significantly higher than that in the cranial air
sac.
378
P. SCHEID, M. R. FEDDE AND J. PEEPER
Table 1. Gas exchange variables in nine geese before and seven geese after
implantation of indwelling air sac and vascular cannulae; five geese were investigated both before and after cannulation
Variable
Before cannulation
1
1
Vi, l(BTPs)min~ kg~
f, min"1
0-34 ± 0-03 (38)
14-0 ±1-9 (38)
31-4 ±2-2 (38)
11-1 ±0-7 (38)
0-42 ± 0-04 (38)
0-35 ± 0-02 (38)
0-40 ± 0-03 (38)
2-8 ±0-2 (38)
15-9 ±0-2 (38)
0-84 ± 0-02 (38)
4-9 ±0-2 (38)
13-2 ±0-3 (38)
0-77 ± 0-02 (38)
40-6 ±0-2 (29)
VT, ml (BTPS) kg" 1
VD, ml (BTPS) kg" 1
VD/VT
MCOJ, mmolmin^kg" 1
M^, mmolmin~1kg~l
PEcc^, kPa
PEo,, kPa
RE
PE' C O 2 , kPa
PE'OI, kPa
RE'
Body temperature, °C
After cannulation
0-24 ±002*:(176)
8-4 ±0-8* (172)
29-3 ±4-4 (178)
11-4 ±0-2 (32)
0-37 ±0-02 (31)
0-31 ±0-01 (32)
0-37 ±0-01 (32)
3-l±0-l (32)
15-5 ±0-1 (32)
0-82 ± 0 0 1 (32)
4-8 ±0-1 (64)
13-4 ±0-1 (64)
0-78 ± 0-01 (64)
41-4 ±0-1* (35)
Overall mean values calculated as the arithmetic mean of individual birds ( ± S . E . ) ; in
brackets, total number of measurements.
Average body mass, 4-9 kg.
See text for an explanation of the abbreviations.
* Mean significantly different from that before cannulation, P=s0-05.
Table 2. Partial pressure of CO2 and O2 and exchange ratio (R), calculated
according to equation 3, for expired gas and air sacs in seven geese
Inspired
End-expired
Mixed-expired
Clavicular
Cranial thoracic
Caudal thoracic
Abdominal
Pco, (kPa)
Po, (kPa)
R
N
0
19-2 ±0-0
13-4 ±0-1
15-5 ±0-1
12-3 ±0-2
12-7 ±0-2
16-5 ±0-2
17-0 ±0-3
—
0-78 ±0-01
0-82 ±0-01
0-73 ± 0-01
0-73 ±0-02
1-03 ±0-05
1-16 ±0-06
—
64
32
46
32
52
24
4-8 ±0-1
3-l±01
5-2 ± 0 1
5-0 ± 0 1
2-6 ±0-2
2-4 ±0-2
Overall mean values as in Table 1 (±S.E.).
N, number of measurements.
Discussion
Physiological state
Measurements of respiration in unanaesthetized animals are physiologically
more meaningful than values measured under anaesthesia. However, there are
problems because of confinement of the animal, leading to unsteady condition^
and departures from undisturbed resting values. Although there was no evidence
Gas exchange in the goose
379
Table 3. Partial pressures (in kPa) of CO2 and O2 in arterial blood, cranial air sacs
( = clavicular and cranial thoracic) and end-expired gas, and arterial blood pH in
seven geese
Arterial
Cranial air sacs
End-expired
4-2 ±0-2
5-1 ±0-1*
4-9 ±0-1*
12 •9 ±0-2
12 •6 ±0-2
13 •3 ±0-1**
PH
N
7-52 ± 0-01
—
—
16
78
64
Overall mean values ± S.E. N, number of measurements.
*Mean significantiy different from arterial blood, P=SO-O5.
**Mean significantly different from cranial air sacs, P=£0-05.
that the geese habituated to the experimental situation, the values measured later,
i.e. in cannulated animals, may more closely represent resting values of undisturbed geese. This is supported by the smaller variation of respiratory values after
cannulation than before.
The arterial Pcc>2> Po2 a n ^ pH were in the range of values measured in awake,
unanaesthetized birds (Table 4). The specific O 2 uptake was somewhat lower than
values measured in other geese and in ducks.
Analysis of gas exchange based on inspired, expired and air-sac gas
In the following analysis we will use the simplified functional avian lung-air sac
model of Fig. 2, and will make the following, in part problematic, assumptions.
(1) The model contains a single cranial and a single caudal air sac, whose PCOj
and Poj are taken as averages of the values for clavicular and cranial thoracic air
sacs, and for caudal thoracic and abdominal air sacs, respectively (Table 5).
Table 4. Oxygen uptake and arterial blood gases and pH measured in unanaesthetized, unrestrained birds
Species
Chicken*
Duck, muscovy*
Duck, Pekin**
Duck, Pekin**
Duck, Pekin**
Goose, bar-headed**
Goose, bar-headed**
Goose, domestic
(mmol min
kg" 1 )
—
0-84
0-72
—
0-56
0-37
x
Paco.
(kpg
4-4±0-l
5-l±0-l
4-l±0-l
3-7±0-l
40 ±0-3
2-9 ±0-1
4-3 ±0-1
4-2 ±0-2
Pao,
(kPa)
10-9 ±0-3
10-9 ±0-1
12-5 ±0-4
12-5 ±0-1
pHa
Reference
1
7-52 ±0-01
1
7-49 ± 0-01
2
7-47 ±0-02
3
7-46 ±001
12-7 ±0-1
12-4 ±0-1
12-9 ±0-2
7-55 ±0-02
7-47 ±0-04
7-52 ±0-01
4
2
3
5
References: 1, Kawashiro & Scheid (1975); 2, Faraci et al. (1984); 3, Black & Tenney (1980);
4, Shams & Scheid (1987); 5, this study.
• Blood sampled by a remote-controlled device in completely unrestrained animals.
•* Blood sampled through catheters with birds inside a box in which they were free to move.
380
P. S C H E I D , M. R . F E D D E AND J. PIIPER
Moreover, it is assumed that there are no differences in air-sac gases between the
two sides of the body.
(2) Steady-state gas exchange is assumed, in spite of the very low breathing
frequency. In particular, respiratory variations of air-sac gas composition are
Fig. 2. Model for calculations of gas exchange in the neopulmo and paleopulmo
during inspiration (A) and expiration (B). The air flow is shown by the arrows. The
shaded areas show the paleopulmo (pp) and neopulmo (np). CrS, cranial air sacs, CdS,
caudal air sacs; I, mixed or effective inspired; E e p , end-parabronchial during
expiration; E', end-expired (in the trachea); M, gas exchange rate during inspiration
(insp) or expiration (exp).
Table 5. Partial pressure values (in kPa) measured and derived in the analysis of
gas exchange (see Discussion)
End-expired
Cranial air-sac
• Caudal air-sac
Effective inspired
End-parabronchial
during expiration
PE'
Pcrs
PcdS
PI
PE e p
co2
O2
N2
4-8
5-1
2-5
1-8
4-5
13-4
12-6
16-8
17-2
14-2
73-6
74-1
72-5
72-8
73-1
N2 partial pressures calculated from O2 and CO 2 values with a mean barometric pressure of
99-7 kPa and a mean body temperature of 41-4°C, corresponding to H 2 O partial pressure cd
7-9 kPa.
™
Gas exchange in the goose
381
neglected, as are gas concentration gradients within the air sacs, although they
have been shown to exist in ducks (Torre-Bueno et al. 1980).
(3) Gas exchange is assumed to occur in the parabronchi only, not in the air
sacs. This appears justified since, according to Magnussen et al. (1976), only about
2 % of CO 2 exchange and less than 5 % of O 2 exchange occurred in the air sacs of
the muscovy duck.
(4) Perfect unidirectional flow by aerodynamic valving is assumed, meaning
that (a) during inspiration there is no flow through the ventrobronchi into the
cranial air sacs, as confirmed by Powell et al. (1981) for the duck and by Banzett et
al. (1987) for the goose, and (b) during expiration there is no shunting of gas from
the caudal air sacs through the main bronchus (a shunt of about 12% was
estimated in muscovy ducks by Powell et al. 1981).
(5) An equal partitioning of ventilation to cranial and caudal air sacs is
assumed, based on experimental results obtained in spontaneously breathing
muscovy ducks (Scheid et al. 191 A).
Inspiratory phase
Because end-expired gas (E') remains in the dead space (VD) from the
preceding expiration, the mean partial pressures in the gas before entering the
parabronchi, i.e. the effective inspired partial pressures, PI, are:
PT =
PE' + ( 1 - ^ ) P I .
(4)
The PT values shown in Table 5 are obtained using the values from Tables 1 and 2.
When N2 equilibrium (no net transfer) is assumed, the gas transfer rate (of CO2
and O2) in a gas-exchanging compartment (paleopulmo or neopulmo) during
inspiration, Minsp, is:
M insp = Vin/3g(Pin - P out fN2) ,
(5)
where the subscripts in and out refer to the inflow and outflow ends of the
respective gas-exchanging compartment; /Jg is the gas phase capacitance coefficient (= 8-55 ml P 1 kPa" 1 at the mean body temperature of 41-4°C; Piiper et al.
1971), and fN2 is the 'N2 correction' factor:
lN2=(Pin/PoutW
(6)
According to assumption 5, Vin to both neopulmo and paleopulmo is half of the
total ventilation, V. The transfer rate in the neopulmo is thus:
Mnp.insp = ^V/Sg(PT - PcdsW
(7)
and that in the paleopulmo:
M pp , insp = ^V/3g(Pl - PCrSfN2) ,
(8)
where CdS and CrS refer to the caudal and cranial air-sac groups. It should be
382
P. S C H E I D , M. R . F E D D E AND J. PIIPER
noted that equation 7 does not require that all gas inspired into caudal air sacs
should pass through the neopulmo (see Fig. 2).
With the values from Table 5, equations 7 and 8 yield the following values for
fractional neopulmonic transfer during inspiration, M np /(M np -l-M pp ): CO 2 , 18 %;
O 2 , 7 %. The combined values of MiDsp for the neopulmo and paleopulmo suggest
that 59 % of the total CO 2 output and 65 % of the total O 2 uptake occurred during
inspiration.
According to equation 5, the exchange ratio is:
D _ (iNrPput Pjn)cO2
(Pin ~ fN2Pout)o2
/n\
With the values from Table 5, one obtains the following inspiratory R values: for
the neopulmo, 1-9; for the paleopulmo, 0-66; for the whole lung, 0-75. The high R
value for the neopulmo indicates it has a high V/Q ratio. From inspection of the
V/Q lines calculated for domestic ducks by Hastings & Powell (1986), one can
estimate from these R values that the V/Q ratio should be about 2-2-5 times
higher in the neopulmo than in the paleopulmo, and this is in agreement with our
findings.
Expiratory phase
During expiration, approximately equal gas flows are assumed to exit from
caudal air sacs via the lungs (both paleopulmo and neopulmo) and from the cranial
air sacs (assumptions 4 and 5, above). Therefore, the end-parabronchial partial
pressures during expiration (PEep) may be calculated as the average value between
Pcrs an<3 P E ' (Table 5). The R value calculated for the paleopulmo during
expiration, using the Pcds a n d P£ep values and equation 9, is 0-73. This value is
very similar to the value calculated above for the paleopulmo during inspiration,
0-75.
Unfortunately, the role of neopulmonic and paleopulmonic gas exchange
cannot be separated for the expiratory phase, because this would require
measurement at the entrance to the paleopulmonic parabronchi. But it is possible
to estimate the total gas exchange occurring during expiration (Mexp), using a
relationship that corresponds to equation 5 and considering that the flow from the
caudal air sacs through the neopulmo and then through the paleopulmo is again
half of the total ventilation:
VS(PPEepfN2).
(10)
The results indicate that 29 % of the total CO 2 output and 33 % of the total O 2
uptake occurred during expiration. Although inspiratory and expiratory CO 2
exchange add up to only 88 % of the total, the disagreement is not too large in view
of the assumptions made and of the experimental errors. For O 2 , the rates add up
to 98 %.
The data further suggest that about two-thirds of gas exchange occurred during
Gas exchange in the goose
383
inspiration and one-third during expiration. This is somewhat surprising since
inspiratory time was only half expiratory time. However, the gas entering
neopulmonic and paleopulmonic parabronchi during the inspiratory phase is
closer in composition to the inhaled air than it is during the expiratory phase.
Arterial blood vs end-expired and cranial air-sac gas
In their study on the anaesthetized goose, Cohn & Shannon (1968) found endtidal and clavicular air-sac Pco 2 to be very similar to arterial Pcch a n d concluded
that the parabronchial air flow was unidirectional. The flow pattern proposed by
these authors has indeed later been corroborated by more direct techniques (see
Scheid, 1979). We consistently measured values of arterial Pco 2 that were
significantly below end-tidal and clavicular Pco2> however. A lower value for
arterial than end-expired Pco 2 Q a s a l s o been reported in earlier studies on avian
gas exchange (Piiper et al. 1970; Scheid & Piiper, 1972; Powell et al. 1978). This
arterial-to-end-expired Pcch difference, 'anomalous' from a mammalian point of
view, is predictable as a result of the functional cross-current arrangement of air
and blood flow in avian lungs (Scheid, 1979).
Based on the average Pcc^ difference of -0-9 kPa (Table 3) between arterial
blood and cranial air-sac gas, end-parabronchial PCQ; appears to be close to the
mixed venous Pco2- A higher Pco2 m end-expired gas than in mixed venous blood
has been reported in the chicken in hypercapnia (Davies & Dutton, 1975; Meyer
et al. 1976), and can be explained by the action of the Haldane effect in a crosscurrent avian lung model (Meyer et al. 1976).
In contrast to Pco2> there was no significant difference between the P O z of
arterial blood and end-expired or cranial air-sac gas. In a cross-current system, a
negative end-expired-to-arterial P O2 difference (APO2) is possible. However, the
unequal distribution of ventilation to perfusion (V/Q inhomogeneity), which has
been shown by the multiple inert gas elimination technique to be present in bird
lungs (Powell & Wagner, 1982), can easily increase this A P ^ to zero or to a
positive value. Indeed, in most studies on birds breathing air, a positive value of
APQ 2 has been found (Piiper et al. 1970; Jones & Holeton, 1972). It is important to
note that the effect of a given V/Q inhomogeneity is much stronger on A P ^ than
on APccb' except in the case of very high V/Q corresponding to functional dead
space ventilation (Powell & Wagner, 1982).
In addition to the influence of V/Q inhomogeneities, diffusion limitation
offered by the gas exchange tissue and by pulmonary capillary blood is also
expected to produce a positive value of APo2, and a less negative or even positive
value of APccv
In conclusion, the partial pressures of CO 2 and O 2 measured in the air sacs,
expired gas and arterial blood can be explained on the basis of the currently
accepted model of gas flow pattern in avian lungs. Neopulmonic gas exchange is
Estimated to constitute a small fraction of overall gas exchange, particularly for
O2.
384
P. S C H E I D , M. R. F E D D E AND J. PIIPER
We thank Drs R. E. Burger, J. A. Estavillo, J. Geiser and R. K. Gratz for their
help in part of the experiments. This study was supported by a Senior Scientist
Award from the Alexander von Humboldt-Stiftung to MRF and, in part, by a
grant-in-aid from the American Heart Association, Kansas Affiliate, Inc. Contribution no. 87-125-3 from the Kansas Agricultural Experiment Station, Kansas
State University, Manhattan, KS66506, USA.
References
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