J. Exp. Biol. (1971), 54. 103-118
With 6 text-figures
Printed in Great Britain
I0-j
BIRD RESPIRATION: FLOW PATTERNS
IN THE DUCK LUNG
BY WILLIAM L. BRETZ AND KNUT SCHMIDT-NIELSEN
Department of Zoology, Duke University, Durham, North Carolina 27706, U.S.A.
(Received 3 July 1970)
INTRODUCTION
The respiratory system of birds is structurally and functionally very different from
that of mammals and has therefore attracted a great deal of interest. Briefly, the avian
respiratory system consists of paired lungs, where gas exchange with the blood occurs,
and of several large air sacs (grouped as anterior and posterior sacs) that act as bellows
to move gases over the exchange surfaces of the lungs (Fig. 1 A). The gas exchange
does not take place in alveoli but in air capillaries, and the finest branches of the
bronchi permit through-flow of air. The air sacs are poorly vascularized and apparently do not participate in gas exchange. In spite of a large body of anatomical information the important question of how air flows in the complex system of passageways
in the bird lung has remained open.
Description of the system; terminology
A comprehensive review ' Structural and functional aspects of avian lungs and air
sacs' by A. S. King covers most work done prior to 1965 (King, 1966). Another
excellent review, covering the most recent contributions, has been prepared by R. C.
Lasiewski (in the Press).
A description of the gas conduits in the avian respiratory system can best be given
by defining three levels of bronchi: (1) the Primary bronchus ( = mesobronchus) which
is the large passageway leading from the trachea all the way through the lung to the
posterior air sacs. (2) Secondary bronchi which branch off from the primary bronchus.
These are (a) the craniomedial secondary bronchi which connect to the anterior air
sacs as well as to the lung parenchyma, and (b) the caudodorsal secondary bronchi,
which connect to the lung parenchyma. (3) Tertiary bronchi (= parabronchi) are
branches at the level where gas exchange with the blood takes place, and with their
surrounding air capillaries they make up the bulk of the lung parenchyma. The tertiary
bronchi, as was said above, are supplied from the secondary bronchi. In addition,
there are recurrent connexions ( = recurrent bronchi) from the air sacs, which lead
into the lung and connect to tertiary bronchi.
To simplify our discussion we have reduced this complexity to a diagram of one
lung with its air sacs and connexions as given in Fig. 1B. Gas exchange between air
and blood takes place in those parts that contain tertiary bronchi; the remaining
passageways are non-exchange conduits and sacs. There are no obvious anatomical
valves that might direct the flow of air between the different parts of the system.
104
W. L. BRETZ AND K.
SCHMIDT-NIELSEN
Possible functional significance
The existence of tertiary bronchi, which are tubes open at both ends, permits bulk
flow of air through the lung tissue, rather than in a tidal back-and-forth flow as in the
mammalian lung. The existence of several possible routes between the primary
bronchus, the lung parenchyma and the air sacs raises the question of which pathways
the air follows in response to different physiological demands.
Lung
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Fig. i. The avian respiratory system. (A) Lateral view of one lung and its associated air sacs.
(B) Simplified schematic diagram. Anterior air sacs: a = cervical, 6 = interclavicular, c =
pre-thoracic. Posterior air sacs: d = post-thoracic, e = abdominal. The three anterior bold
arrows indicate direct craniomedial connexions between the primary bronchus and the
anterior air sacs; the two posterior bold arrows indicate the direct connexions between the
primary bronchus and the posterior air sacs; the three dorsally directed hollow arrows indicate
caudodorsal secondary bronchi branching from the primary bronchus. The lines emphasized
with ' ticks' outline areas where gas exchange with the blood may take place. Passageways: Tr =
trachea, PB = primary bronchus, CrB = craniomedial secondary bronchi, CaB = caudodorsal
secondary bronchi, R = recurrent connexions between air sacs and lung. TB = tertiary
bronchi, which are the finest branches and form connexions between the various secondary
bronchi.
For example, during exercise, there is an increased demand for air flow over the
gas-exchange surfaces (i.e. through the tertiary bronchi). In contrast, when the bird
is under heat stress, a maximum amount of air might flow over the sites of evaporation
Bird respiration
105
with an unchanged flow over the sites of gas exchange (to prevent respiratory alkalosis),
thus shunting air through the primary bronchus and avoiding excessive ventilation of
the tertiary bronchi. Both cases could differ from the air-flow pattern when demands
on the system are minimal (rest at moderate ambient temperatures).
The specific flow pattern during any type of respiration is of utmost importance to
the bird, for the composition of the air which is exposed to exchange with the blood
depends on the route along which air flows during the respiratory cycle (as well as on
such variables as tidal volume and respiratory frequency).
Previously proposed flow patterns
Previously proposed hypotheses for air flow during resting respiration in birds
include nearly all theoretically possible directions and patterns. Some of the major
contributions are depicted in diagrammatic form in Fig. 2.
Dotterweich (1930, 1933) studied the deposition of inhaled carbon particles on the
walls of the lung passageways in finches, pigeons and ducks, and made analyses of
air-sac gas compositions in ducks. He proposed (Fig. 2 A, F) that during inspiration
the airflowsthrough the direct connexions from the primary bronchus to the posterior
air sacs while the anterior sacs are filled by air moving from the lung parenchyma. The
craniomedial secondary bronchi are assumed ' closed' during inspiration so that there
is no airflowfrom the primary bronchus directly to the anterior sacs. During expiration
airflowsfrom the posterior sacs through the tertiary bronchi towards the craniomedial
secondary bronchi and into the primary bronchus; from the anterior sacs air flows
through the craniomedial secondary bronchi into the primary bronchus. This pattern
requires some sort of control mechanism to prevent air flow cranially in the main
portion of the primary bronchus during expiration (marked x in Fig. 2F).
In 1936 Dotterweich constructed a glass model of the avian system of lungs and
air sacs and observed the patterns of air flow indicated in Fig. 2 B, G. These patterns
differ somewhat from his earlier theories, in particular for the expiratory phase, but
he felt that the patterns offlowin his model closely represented those in the avian lung.
Vos (1934) measured gas compositions at various sites in the respiratory system of
the duck, and repeated some of Dotterweich's carbon-deposition experiments. He
concluded that during inspiration both anterior and posterior sacs fill simultaneously
by air flow through their direct connexions with the primary bronchus (Fig. 2C).
During expiration air from the posterior sacsflowsthrough the tertiary bronchi to the
craniomedial secondary bronchi and into the primary bronchus; the anterior sacs
empty directly through the craniomedial secondary bronchi into the primary bronchus
(Fig. 2 F). During inspiration there is insignificant flow through the bulk of the tertiary
bronchi, and during expiration there is insignificant flow cranially in the primary
bronchus.
Zeuthen (1942) studied changes in gas composition at various sites in the chicken
lung after inhalation of hydrogen and air mixtures. He proposed reciprocating flow
patterns as indicated in Fig. 2D, H, but he felt that there might be some differences
between the volumes flowing in the various passage-ways during inspiration and expiration.
Hazelhoff (1951) studied the movement and deposition of airborne particles in the
passageways of the lungs of crows, chickens, pigeons and herons, and also experimented
io6
W. L. BRETZ AND K. SCHMIDT-NIELSEN
with a glass model to investigate patterns of air flow. He proposed the concept of
unidirectional flow cranially in the tertiary bronchi during both inspiration and
expiration, with significant flow in the primary bronchus only during inspiration
(Fig. 2 A, F). He also felt, on the basis of his glass models, that there could be a slight
flow caudally in the primary bronchus during expiration.
Expiration
Inspiration
A. Dotterweich, 1933; Hazelhoff, 1951; Conn &
Shannon, 1968;' Schmidt Nielsen et a/. 1969
B. Dotterweich, 1936
F. Dotterweich, 1933; Vos, 1934; Haielhoff,
' 1951; Conn & Shannon, 1968
G. Dotterweich, 1936; Shepard et af. 1959
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C. Vos, 1934
H. Zeuthen, 1942
D. Zeuthen. 1942
E. Shepard eta/. 1959
Fig. 2. Diagrammatic presentation of previously proposed patterns of air flow in the avian
respiratory system. Arrows indicate air flow either specifically proposed or implicit in the
various hypotheses, crosses indicate insignificant air flow or no air flow. For identification of
the regions of the lung, compare with Fig. i.
Shepard et al. (1959) analysed the gas composition of samples withdrawn from the
respiratory system of chickens, and concluded that during inspiration airflowsthrough
the tertiary bronchi to the air sacs, and during expiration air flows through the direct
connexions between the air sacs and the primary bronchus (Fig. 2E, G).
Cohn & Shannon (1968) combined data from pressure measurements and gas-
Bird respiration
107
composition analyses from various sites in the goose respiratory system to propose
that during inspiration air flows to the anterior sacs from the tertiary bronchi, while
the posterior sacs fill through their direct connexions with the primary bronchus
(Fig. 2A). During expiration the posterior sacs empty through the tertiary bronchial
route and the anterior sacs empty through the craniomedial secondary bronchi directly
into the primary bronchus (Fig. 2 F).
Schmidt-Nielsen et al. (1969) studied the ostrich and included observations on
panting as well as on resting birds. Their observations indicated that during inspiration
air passes directly to the posterior sacs via the primary bronchus while the anterior
sacs receive air from the tertiary bronchi (Fig. 2 A). The fact that the panting ostrich
did not become severely alkalotic, although the air-sac COg concentrations were very
low, suggests that a large fraction of the respiratory air is shunted past the lung.
These previously proposed patterns of air flow are, without exception, inferences
drawn from indirect approaches. With the many conflicting theories in mind, we felt
that by determining directly the direction of air flow at specific sites (e.g. the primary
bronchus, the craniomedial secondary bronchi, and the caudodorsal secondary
bronchi), the problem of the air-flow patterns in the avian lung could be resolved.
METHODS
Experimental animals
Adult domestic Pekin ducks (Anas platyrhynchos) were purchased from local
farmers, maintained in an outside pen with a gravel-bottomed pool and running water,
and provided ad libitum with mixed grain. The birds weighed from 1-9 to 3 -2 kg
(mean, 2*6 kg), and their sex was determined after the termination of an experiment.
Experimental design
These experiments were designed so that measurements of tidal volume, respiratory
rate, body temperature, and recordings of air-flow direction could be made on animals
that were (a) anaesthetized, (b) unanaesthetized and resting quietly at room temperature, and (c) panting due to an ambient heat load. The experiments on panting were
intended to force the animal to hyperventilate, and were not intended to be a study of
thermoregulation as such.
Measurements on unimplanted animals were made in order to establish a basis for
evaluating the effect of implantation of the air-flow direction probe.
Equipment
All of the experiments were conducted in a chamber regulated to ±0-5° C and
continuously ventilated at a rate of 595 1 min"1. The relative humidity ranged between
55% at 230 C and 27% at 400 C. An adjustable cloth sling supported the animal in
a position similar to normal standing posture with the head extended (Fig. 3). We
consider an upright position important, and some results previously reported may be
misleading because the birds were kept on their backs or sides.
Tidal volumes and respiratory rates were determined by measuring the pressure
differential across a low-resistance screen mounted in the opening of a hood sealed
around the neck of the bird (Fig. 3). A Sanborn differential pressure transducer
io8
W. L. BRETZ AND K.
SCHMIDT-NIELSEN
(Model 270) connected to a Sanborn carrier pre-amplifier (Model 350-1100C) permitted continuous recording of this pressure differential on one channel of a Sanborn
Series 7700 polygraph. The output of the carrier pre-amplifier was integrated (Sanborn
integrating pre-amplifier, Model 350-3700A) and recorded on an adjacent channel of
the polygraph. Respiratory rate could be determined from the pressure recording, and
the time integral of the positive portion of the pressure differential was proportional
to the inspired volume (inspired volume was considered equivalent to tidal volume).
This system was calibrated against known reciprocating volumes of air flow generated
by a Harvard Respirator (Model 665), and had an accuracy of ± 5 % of the maximum
reciprocating volume (100 ml) at all frequencies tested (10-125 cyles min"1).
r
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>-—_
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Hood for
measuring
respiratory
volumes
Implantation
site for air
flow direction
probe
\ \
Rectal
thermistor
probe
Fig. 3. Restraint and support of experimental animal. Shaded areas indicate tape holding
animal to a support rod along its back. Dashed line indicates the outline of a cloth sling used
for support.
Air-flow directions were measured with implanted probes of our own design,
similar to the probe described by Grahn, Paul & Wessel (1969) for blood-flow measurements. Our probe contained two heated microthermistors (Fenwal BC32J1), connected with two identical Wheatstone bridges (Fig. 4). The thermistors were mounted
so that when the probe was positioned axially in an air conduit, either the distal or the
proximal thermistor was relatively more shielded than the other, depending on the
direction of air flow. The two heated thermistors would therefore have different rates
of heat dissipation during airflow.The difference was reflected in the output potentials
of the bridges to which they were connected. Comparison of the slopes of the two
bridge outputs permitted the determination of air-flow direction past the probe. The
outputs were recorded on two adjacent channels of a Sanborn Series 7700 polygraph,
using Sanborn low-level pre-amplifiers (Model 350-1500A) equipped with Sanborn
350-2B d.c. plug-in units.
Body temperatures were measured to ± 0-2° C with calibrated thermistor probes
inserted to 10 cm depth in the hind gut.
Bird respiration
109
Preparation of experimental animals
Prior to implantation of the probe, the anaesthetized bird (2-5 ml kg"1 Equithesin
intramuscularly) was fastened to a support rod with masking tape (Fig. 3). The dense
plumage in the ventral thoracic region provided a thick, compressible cushion between
the tape and the body so that respiratory movements were not unduly restricted.
Additional tape held each wing in a natural folded position against the body. This
method of restraint was used to prevent movements of the neck which could displace
the implanted air-flow direction probe.
\, vV
y>
.
—P
Fig. 4. Straight and recurved air-flow direction probes. D = distal thermistor, P = proximal
thermistor. The leads from each thermistor of a probe connect to separate but identical
Wheatstone bridges. Total probe length about 35 cm. Scale: 2 x .
The air-flow probes were implanted in the lung via a midneck tracheostomy. The
positioning of the probe at an appropriate site in the passageways was achieved by
feel and was confirmed by dissection at the end of the experiment. The required depth
of insertion was estimated from the bird's external anatomy. The primary bronchus
curves dorsally just caudally from the craniomedial bronchial orifices, and this could
be felt when the distal end of the probe reached this point. This was the most useful
clue for positioning a straight probe in the primary bronchus. The recurved probes
were positioned primarily by the principle of 'two steps forward, one step back'.
They were pushed in 3-4 mm increments and pulled back gently between each movement until the probe was caught in a secondary bronchus (once this happened the
probe could usually be repositioned only in a more caudal bronchus). The exact
placement of the probe depended on a certain degree of luck, and frequently the
placement was not as intended (as was discovered upon later dissection). After placement the leads were taped against the neck to prevent caudal or cranial slipping from
the position of the probe in the lung, and the incision was closed with wound clips
and bandaged.
Experimental procedure
After implantation of the probe the bird was placed in an adjustable sling in the
temperature-controlled chamber. Recordings of tidal volume, air-flow directions, and
chamber and body temperatures were made while the animal was still anaesthetized.
A minimum of 12 h was allowed for recovery from the anaesthetic (food and water
no
W. L. BRETZ AND K. SCHMIDT-NIELSEN
withheld). Then recordings were made while the animal was resting quietly at room
temperature (23-250 C). To induce panting, chamber temperature was then quickly
raised to 350 C. If after 30 min at 350 C the animal had not begun to pant, the ambient
temperature was raised to 400 C, which always induced panting. Tidal volume and
air-flow directions were continuously recorded. Immediately after the animal began
to pant the heating element of the chamber was turned off and its temperature was
allowed to return to room temperature while recordings were continued until body
temperature had returned to normal (its level prior to the heat load) in about half
an hour.
The bird was painlessly killed (while still restrained) at the end of the experiment,
and dissected to establish the exact placement of the air-flow direction probe.
Measurements were also made on unimplanted animals, following the above procedure closely. The birds were restrained with the support rod while unanaesthetized.
After they had been allowed i - i h to calm down in the experimental chamber with
the hood in place, resting and panting measurements were made as described above.
RESULTS
Air-flow direction
The determination of air-flow direction at specific sites in the duck lung was
attempted on 22 animals. Eleven of the experiments were successful and 11 failed due
to malfunctioning or to poor positioning of the implanted probe.
Fig. 5 A is a representative output recording from the two channels of a probe placed
in the upper, unbranched portion of a primary bronchus. This is a trivial case for the
understanding of flow direction, but it is useful in showing the interpretation of a
recording when it is known that volume of flow is equal in both directions. During
inspiration the proximal thermistor is unshielded to air flow and the distal thermistor
is shielded. The proximal thermistor therefore displays a greater change in the signal.
During exhalation the situation is reversed, the distal thermistor is now unshielded
and gives the greater signal.
Fig. 5 B is a recording from a recurved probe positioned in the third caudodorsal
secondary bronchus of the left lung. The proximal thermistor was unshielded with
respect to flow from the primary bronchus into the secondary bronchus, and the distal
thermistor was unshielded with respect to flow in the opposite direction. During both
phases of the respiratory cycle, the rate of change of the signal from the proximal
thermistor was greater than that from the distal thermistor (the attenuation for the
proximal thermistor was 5 x that for the distal), indicating that during both inspiration
and expiration the proximal thermistor was unshielded with respect to air flow, while
the distal thermistor remained shielded. Thus, during both phases of the respiratory
cycle air was flowing from the primary bronchus into this secondary bronchus. This
particular recording was from an unanaesthetized bird with a respiratory rate of
19-5 cycles min"1 and a tidal volume of 75 ml.
The example shown in Fig. 5 C is from a straight probe positioned in the primary
bronchus of the right lung at the level where the caudodorsal secondary bronchus
branches off. The proximal thermistor was unshielded with respect to flow caudally
in the primary bronchus; the distal thermistor was unshielded with respect to flow
Bird respiration
111
cranially. During inspiration the rate of change of the signal from the proximal
thermistor was greater than that from the distal thermistor (the attenuation of the
channel for the proximal thermistor was 2-5 x that for the distal), indicating that
during this phase the proximal thermistor was unshielded, while the distal was shielded.
During expiration it appears that there was very little air flow in either direction in
this part of the primary bronchus, as both thermistors returned towards balance. At
the time of this recording the bird was anaesthetized, with a respiratory rate of 30
cycles min"1 and a tidal volume of 48 ml.
1
1
1
2 0mV
E
E E
I
I
I
100 mV
E
E
E
Fig. 5. Recordings from air-flow direction probes. Chart speed and sensitivity are indicated
to the right of each recording. (A) Probe located in primary bronchus. Attenuation equal for
proximal and distal channels. (B) Probe located in caudodorsal secondary bronchus. Attenuation for proximal channel is 5 x that for distal. (C) Probe located in primary bronchus.
Attenuation for proximal channel is 2-5 x that for distal. I and E represent beginning of
inspiration and expiration, respectively.
Composite diagram of air-flow patterns
Similar interpretation of recordings from probes positioned in the primary bronchus,
in the craniomedial secondary bronchi and in the caudodorsal secondary bronchi,
yields the air-flow diagrams shown in Fig. 6. In six experiments a straight probe was
positioned in the primary bronchus (three times in right lungs, and three times in left
112
W. L. BRETZ AND K. SCHMIDT-NIELSEN
lungs). In five experiments a recurved probe was positioned either in a craniomedial
secondary bronchus (once in the right lung and once in the left lung), or in a caudodorsal secondary bronchus (once in the right lung and twice in left lungs). Although
the probes could not be calibrated to yield absolute flow rates, comparisons between
inspiratory and expiratory flows at a given site could be made semiquantitatively (i.e.
inspiratory flow was greater than, equal to, or less than expiratory flow). Information
used in Fig. 6 was obtained from both males and females; no difference in air-flow
patterns was observed between sexes.
Inspirator/ patterns
Expiratory patterns
Resting
Panting
Anaesthetized
Fig. 6. Directions of airflowin the duck lung. Solid symbols (arrows and crosses) indicate the
results of this study. Dashed arrows indicate directions inferred from previous studies, and
which are consistent with ourfindings(see Discussion). Differences inflowbetween inspiration
and expiration at a given site are suggested by the length of the arrows. For identification of
regions of the lung, see Fig. i.
Effects of implantation of probes
It is important for the interpretation of the recordings to know whether the implantation of the probes has pronounced effects on respiratory function. The probes were
designed to give a minimal obstruction, and their cross-section was less than 20%
of the passageways in which they were positioned. If the probes alter the normal
patterns, we would expect this to result in detectable changes in such parameters as
respiratory rate and tidal volume.
We therefore compared respiratory rate, tidal volume, and body temperature of
nine ducks (mean wt 27 kg) implanted with air-flow direction probes and of eight
unimplanted ducks (mean wt 2-6 kg) (Table 1). Resting values were obtained at room
Bird respiration
113
temperature, immediately prior to the heat load, and panting values when minute
volume was at its maximum. In all instances the difference between mean values for
mplante d and unimplanted animals was not statistically significant, as indicated by
Student's t test (P> o-i).
Table 1. Effects of implantation of air-flow direction probes in duck lungs
(Values are from nine implanted birds and eight unimplanted. Means ±s.E.)
Anaesthetized
Implanted
Unimplanted
Resting
Implanted
Unimplanted
Panting
Implanted
Unimplanted
Resp. rate
(cycles min"1)
Tidal volume
(ml)
Body temp
(°C)
I49±3'2
568 ±6-4
40-9 ±0-2
—
—
—
i3'3±i'4
l6-I ±1-2
75"4±5'6
72-2 ±7-9
4I-2±O-2
4i-6±o-i
iiS"7±i4'9
i 3 o-4±ii-9
34O±3-4
34-1 ±4'6
42'S±o-3
42'4±O-2
DISCUSSION
Previous experimental studies
Although there are interspecific variations in the anatomy of the avian respiratory
system, the general arrangement of lung passageways and air sacs is similar in most
birds. It therefore seems reasonable to compare our data and those of other investigators for the purpose of obtaining a generalized picture. In view of the considerable
confusion and many contradicting theories in this field it is particularly useful to note
that many previous results are in accord with our findings.
Gas-composition data. The normal gas composition at various sites in the respiratory
system has been established for a variety of birds (duck, chicken, goose, pigeon and
ostrich) during resting respiration or under anaesthesia (Dotterweich, 1933; Vos,
1934; Makowski, 1938; Scharnke, 1938; Graham, 1939; Zeuthen, 1942; Shepard et
al. 1959; Cohn, Burke & Markesberg, 1963; Cohn & Shannon, 1968; SchmidtNielsen et al. 1969). Considering the similarity of the results of the different investigators, the lack of agreement among the numerous theories concerning air-flow
patterns is surprising.
In general, the posterior air sacs contain gas that has a higher 0 2 and lower C0 2
content than the gas in the anterior sacs. End-tidal gas is similar to the gas in the
anterior sacs. During panting the anterior sacs contain gas with a composition which
resembles that in the posterior sacs at rest, while the posterior sacs during panting
more closely approach atmospheric air.
Many authors have reported such results, and they can be interpreted in the following way. On inspiration the posterior sacs receive most of the air present in the dead
space plus inhaled fresh air that has not been exposed to gas-exchange surfaces. The
anterior sacs on inspiration receive primarily air that comes from the lung and has
undergone gas exchange. During panting the greatly increased ventilation for purposes
of evaporative cooling results in a washout of the entire respiratory system, giving
higher 0 2 and lower C0 2 concentrations in both posterior and anterior air sacs.
8
EXB54
ii4
W. L. BRETZ AND K. SCHMIDT-NIELSEN
Several investigators measured gas compositions at various sites in birds which had
inhaled or were injected with abnormal gas mixtures (Vos, 1934; Zeuthen, 1942;
Scharnke, 1938; Shepard et al. 1959; Cohn et al. 1963; Schmidt-Nielsen et al. 1969).
The results of these experiments are consistent with the conclusions outlined in the
preceding paragraph, although the investigators have not always interpreted their
results in this way.
Pressure data. Baer (1896) and Soum (cited from Zeuthen, 1942) measured simultaneous increases during inspiration, and decreases during expiration, in the pressure
in both anterior and posterior air sacs. Such synchronous pressure changes have been
observed by other investigators as well (Francois-Frank, 1906; Victorow, 1909; Cohn
& Shannon, 1968; Schmidt-Nielsen et al. 1969), and are rather low (± 10 cm HaO),
both during the inspiratory and expiratory phases of resting respiration.
These data indicate that the anterior and posterior air sacs fill and empty synchronously, and that substantial movement of air from one sac to another during a given
phase of the respiratory cycle is improbable.
Deposition of paniculate matter. The deposition of inhaled or insufflated particulate
matter (e.g. finely divided carbon or barium sulphate) on the walls of the passageways
in the respiratory system was studied by Dotterweich (1930), Vos (1934), Walter
(1934), Graham (1939) and Hazelhoff (1951). Except for Walter, these investigators
found similar patterns of non-uniform deposition. These studies suggest that during
inspiration much of the air must flow into the direct connexions to the posterior air
sacs and the caudodorsal secondary bronchi, with little or noflowinto the craniomedial
secondary bronchi. Furthermore, it appears that during expiration there must be
considerable flow from the posterior air sacs through their recurrent connexions into
the tertiary bronchi of the lung, and that air flow cranially in the primary bronchus
somehow must be blocked just cranially to the orifices of the caudodorsal secondary
bronchi. In Walter's experiments there was a uniform distribution of particulate
matter throughout the respiratory system.
Other information. Several other experiments yielded interesting data. Biggs & King
(1957) explored the effects of 'humeral breathing' on respiration in the chicken. (In
'humeral breathing' the trachea is blocked and the humerus is cannulated, allowing
air to flow into the respiratory system via the interclavicular air sac.) Although they
did not propose a definite pattern, their results suggest that there is a relatively complex
airflowin the lung, rather than simple reciprocal movements as proposed by Scharnke
(1938) and Zeuthen (1942). We see no contradiction between their results and our
proposed pattern of flow.
Calder & Schmidt-Nielsen (1966, 1968) studied the result of high ventilation rates
due to panting (induced by heat load), on the P c 0 , of the arterial blood in nine species
of birds. Their data suggest that the exchange surfaces of the lung are over-ventilated
during panting, relative to the need for oxygen, resulting in excessive loss of COa and
respiratory alkalosis. Using similar techniques on the ostrich, Schmidt-Nielsen et al.
(1969) concluded that in this bird the respired air must be shunted away from gasexchange surfaces during panting.
Bird respiration
115
Discussion of present study
Our experiments have yielded information about the direction of air flow at three
sites in the duck lung (the primary bronchus, the craniomedial secondary bronchi,
and the caudodorsal secondary bronchi) during three different modes of respiration
(anaesthetized, unanaesthetized and resting quietly, and panting due to heat load).
On the basis of these results and the experimental work previously done by others,
we propose the following pattern of air flow (Fig. 6).
(1) Resting respiration. During respiration airflowscaudally in the primary bronchus,
and from the primary bronchus into the caudodorsal secondary bronchi. The anterior
air sacs are filled during inspiration primarily by air that has passed over gas-exchange
surfaces of the lung, while the posterior air sacs receive dead-space air and a considerable portion of the inspired air directly through non-exchanging conduits, i.e.
the primary bronchus. The flow of air through the craniomedial secondary bronchi
directly to the anterior sacs is small, and air flowing into the caudodorsal secondary
bronchi must flow through the tertiary bronchi towards the anterior air sacs. The
posterior sacs could not receive much of the inspired air through their recurrent
connexions with the tertiary bronchi, for this route would expose the air to gas exchange
with the blood. The recurrent connexions of the interclavicular and anterior thoracic
sacs could be an important route for filling these sacs during inspiration.
During expiration there is very little air flow cranially in the primary bronchus.
There is considerable flow both in the caudodorsal secondary bronchi towards the
tertiary bronchi, and in the craniomedial secondary bronchi towards the primary
bronchus. The expired air must flow from the posterior sacs through the tertiary
bronchi and craniomedial secondary bronchi to reach the primary bronchus. The
recurrent connexions between the posterior sacs and the tertiary bronchi must be very
important during this phase of respiration, for very little air flow is detectable in the
main part of the primary bronchus. Air expired from the anterior sacs probably passes
through the most direct route to the primary bronchus, with the recurrent connexions
being of little importance during expiration.
(2) Panting respiration. The patterns of air flow during panting are very similar to
those of resting respiration. During inspiration there is no indication of flow into the
craniomedial secondary bronchi, and the anterior sacs must be filled with air flowing
from the lung. During expiration there is a smallflowcranially in the primary bronchus,
and air expired from the posterior sacs must flow to the tertiary bronchi through the
caudodorsal secondary bronchi as well as through their recurrent connexions.
(3) Anaesthetized respiration. In this case also the patterns of air flow are similar to
those of resting respiration. The inspiratory flow into the craniomedial secondary
bronchi is somewhat stronger than during resting respiration, but otherwise the
patterns are the same.
The patterns of air flow do not appear to be fundamentally different for the three
modes of respiration investigated (resting, panting and anaesthetized). This does not
exclude, however, that there can be substantial differences in mass flow of air in parts
of the system for different modes of respiration.
Important features of proposed patterns. Two characteristics of the patterns that we
propose deserve special attention.
8-2
n6
W. L. BRETZ AND K. SCHMIDT-NIELSEN
1. Airflowin the tertiary bronchi, which connect the craniomedial and caudodorsal
secondary bronchi, is unidirectional. Airflowsfrom the caudodorsal secondary bronchi
through the tertiary bronchi to the craniomedial secondary bronchi during both
inspiration and expiration, although the inspiratory flow along this pathway is weaker
than the expiratory flow. This arrangement of air flow through the lung parenchyma
(where gas exchange with the blood occurs) would permit a countercurrent exchange
system in the avian lung, as suggested by Schmidt-Nielsen et al. (1969), provided
that the blood vessels are arranged appropriately around the tertiary bronchi and air
capillaries.
2. There is no fundamental change in the pattern of air flow during resting respiration and during panting. There is a small expiratory flow cranially in the primary
bronchus while the bird is panting, but this does not shunt a sufficient amount of the
respired air away from gas-exchange surfaces to prevent respiratory alkalosis, as
Calder & Schmidt-Nielsen (1968) demonstrated in the panting Pekin duck and in
eight other species.
Possible control of air-flow patterns. We feel that the patterns of air flow described
for the Pekin duck are likely to be determined by the anatomical design of the lung
and the effects of this design on the dynamics offluidflow.
The Reynolds number is useful for characterizing the nature of fluid flow. It
expresses the ratio of the shear stress in a fluid due to turbulence, to the shear stress
due to viscosity. In the equation for the Reynolds number,
u is the velocity of flow, / is a characteristic length, and y is the kinematic viscosity
of the fluid (Streeter, 1966).
For computing R for passageways in the avian lung, / is considered to be the diameter
(cm) of the passageway, y is o-i 69 cm2 s - 1 (air saturated with water vapour at 400 C),
and u is the mean velocity (cm s -1 ) of flow during a pulse of air (one phase of the
respiratory cycle).
The value of u at the beginning of the primary bronchus was computed to be
95 cm s~x during resting respiration and 333 cm s - 1 during panting (calculated from
mean values for tidal volume and respiratory rate shown in Table 1, a diameter of the
primary bronchus of 0-5 cm (mean of 10 ducks), and the assumption that hah7 of the
tidal volume flowed to each lung).
During resting respiration R = 280, and during panting R = 940. For flow in a
conduit characterized by R<20OO to 4000, flow is laminar rather than turbulent.
Flow in the primary bronchus must therefore be laminar both at rest and during
panting.
The air velocities and Reynolds numbers in the secondary and tertiary bronchi
must be considerably lower than in the primary bronchi, for the total cross-section
of the respiratory system increases rapidly where the secondary bronchi branch from
the primary bronchus.
Beyond saying that the air flow in the bird lung is laminar, low-velocity, and driven
by very low-pressure differentials, there is little that can be said about the fluid
dynamics without far too much conjecture. Local turbulences can form and persist
Bird respiration
117
in laminar, low-velocity air flow, generally as vortices behind surface irregularities in
the boundary layer of air flow, e.g. the edges of the orifices in the wall of the primary
bronchus. Fluid dynamic phenomena such as this could be a primary factor in controlling the patterns of flow that we have described. Investigation into the methods
by which air flow in the avian lung are controlled should be extremely challenging.
SUMMARY
1. A heated thermistor probe was designed to determine the direction of air flow in
the respiratory system of birds. The probes did not significantly affect the respiratory
rates, tidal volumes, or body temperatures of birds implanted with the probes as
compared to unimplanted birds.
2. Air-flow directions were determined in the primary bronchus, the craniomedial
secondary bronchi, and the caudodorsal secondary bronchi in the lungs of ducks
which were either unanaesthetized and at rest, anaesthetized, or panting due to
heat load.
3. The recorded air-flow directions suggested the following patterns of air flow in
the duck lung for resting respiration.
During inspiration air flows to the posterior air sacs directly from the primary
bronchus (the most direct route), without passing through the tertiary bronchi, while
air flows towards the anterior air sacs via the caudodorsal secondary bronchi and the
tertiary bronchi (thus by-passing the most direct route, the craniomedial secondary
bronchi connecting these sacs to the primary bronchus).
During expiration air flows from the anterior sacs to the primary bronchus via the
craniomedial secondary bronchi (the most direct route), but from the posterior sacs
through the tertiary bronchi and through branches of the craniomedial secondary
bronchi to the primary bronchus (by-passing the most direct route, the portion of the
mesobronchus posterior to the craniomedial bronchi).
4. The patterns established for panting and anaesthetized respiration were very
similar to those described for resting respiration. There was no indication of an
effective shunt operating during panting to avoid excessive ventilation of the exchange
surfaces of the lung.
5. Flow in the tertiary bronchi appeared to be in the same direction during both
inspiration and expiration (from the caudodorsal secondary bronchi towards the
craniomedial secondary bronchi). Such unidirectionalflowwould permit the operation
of a counter-current exchange system, provided that the blood vessels are arranged
appropriately around the parabronchi.
This work was supported by NIH Training Grant 2T1 HE5219, an NSF Predoctoral Fellowship, and NIH Postdoctoral Fellowship 1 FO2 GM43875-01 (WLB);
and NIH Research Grant HE-02228 and NIH Research Career Award 1-K6-GM-21,
522 (KSN).
n8
W. L. BRETZ AND K. SCHMIDT-NIELSEN
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