J. Exp. Biol. (1971), 54. 103-118 I 0 - j

With 6 text-figures

Printed in Great Britain

BIRD RESPIRATION: FLOW PATTERNSIN THE DUCK LUNG

BY WILLIAM L. BRETZ AND KNUT SCHMIDT-NIELSENDepartment 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 fromthat of mammals and has therefore attracted a great deal of interest. Briefly, the avianrespiratory 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 bellowsto move gases over the exchange surfaces of the lungs (Fig. 1 A). The gas exchangedoes not take place in alveoli but in air capillaries, and the finest branches of thebronchi permit through-flow of air. The air sacs are poorly vascularized and appar-ently do not participate in gas exchange. In spite of a large body of anatomical informa-tion the important question of how air flows in the complex system of passagewaysin the bird lung has remained open.

Description of the system; terminology

A comprehensive review ' Structural and functional aspects of avian lungs and airsacs' by A. S. King covers most work done prior to 1965 (King, 1966). Anotherexcellent 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 givenby defining three levels of bronchi: (1) the Primary bronchus ( = mesobronchus) whichis the large passageway leading from the trachea all the way through the lung to theposterior air sacs. (2) Secondary bronchi which branch off from the primary bronchus.These are (a) the craniomedial secondary bronchi which connect to the anterior airsacs as well as to the lung parenchyma, and (b) the caudodorsal secondary bronchi,which connect to the lung parenchyma. (3) Tertiary bronchi (= parabronchi) arebranches at the level where gas exchange with the blood takes place, and with theirsurrounding air capillaries they make up the bulk of the lung parenchyma. The tertiarybronchi, as was said above, are supplied from the secondary bronchi. In addition,there are recurrent connexions ( = recurrent bronchi) from the air sacs, which leadinto the lung and connect to tertiary bronchi.

To simplify our discussion we have reduced this complexity to a diagram of onelung with its air sacs and connexions as given in Fig. 1B. Gas exchange between airand blood takes place in those parts that contain tertiary bronchi; the remainingpassageways are non-exchange conduits and sacs. There are no obvious anatomicalvalves 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 bulkflow of air through the lung tissue, rather than in a tidal back-and-forth flow as in themammalian lung. The existence of several possible routes between the primarybronchus, the lung parenchyma and the air sacs raises the question of which pathwaysthe air follows in response to different physiological demands.

Lung/ \

Tr

a '

. b

" . c . .

' . • . " . • • n&in

! . • ra .' . ".;

• ' . • . ' . ' . • • • . • " • P B . ' • - .

• \1 ml.l:..).$•:.':.

hcaB

• • d • '

• • .

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 boldarrows indicate direct craniomedial connexions between the primary bronchus and theanterior air sacs; the two posterior bold arrows indicate the direct connexions between theprimary bronchus and the posterior air sacs; the three dorsally directed hollow arrows indicatecaudodorsal secondary bronchi branching from the primary bronchus. The lines emphasizedwith ' ticks' outline areas where gas exchange with the blood may take place. Passageways: Tr =trachea, PB = primary bronchus, CrB = craniomedial secondary bronchi, CaB = caudodorsalsecondary bronchi, R = recurrent connexions between air sacs and lung. TB = tertiarybronchi, which are the finest branches and form connexions between the various secondarybronchi.

For example, during exercise, there is an increased demand for air flow over thegas-exchange surfaces (i.e. through the tertiary bronchi). In contrast, when the birdis 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 ofthe tertiary bronchi. Both cases could differ from the air-flow pattern when demandson the system are minimal (rest at moderate ambient temperatures).

The specific flow pattern during any type of respiration is of utmost importance tothe bird, for the composition of the air which is exposed to exchange with the blooddepends on the route along which air flows during the respiratory cycle (as well as onsuch variables as tidal volume and respiratory frequency).

Previously proposed flow patterns

Previously proposed hypotheses for air flow during resting respiration in birdsinclude nearly all theoretically possible directions and patterns. Some of the majorcontributions are depicted in diagrammatic form in Fig. 2.

Dotterweich (1930, 1933) studied the deposition of inhaled carbon particles on thewalls of the lung passageways in finches, pigeons and ducks, and made analyses ofair-sac gas compositions in ducks. He proposed (Fig. 2 A, F) that during inspirationthe air flows through the direct connexions from the primary bronchus to the posteriorair sacs while the anterior sacs are filled by air moving from the lung parenchyma. Thecraniomedial secondary bronchi are assumed ' closed' during inspiration so that thereis no air flow from the primary bronchus directly to the anterior sacs. During expirationair flows from the posterior sacs through the tertiary bronchi towards the craniomedialsecondary bronchi and into the primary bronchus; from the anterior sacs air flowsthrough the craniomedial secondary bronchi into the primary bronchus. This patternrequires some sort of control mechanism to prevent air flow cranially in the mainportion of the primary bronchus during expiration (marked x in Fig. 2F).

In 1936 Dotterweich constructed a glass model of the avian system of lungs andair sacs and observed the patterns of air flow indicated in Fig. 2 B, G. These patternsdiffer somewhat from his earlier theories, in particular for the expiratory phase, buthe felt that the patterns of flow in his model closely represented those in the avian lung.

Vos (1934) measured gas compositions at various sites in the respiratory system ofthe duck, and repeated some of Dotterweich's carbon-deposition experiments. Heconcluded that during inspiration both anterior and posterior sacs fill simultaneouslyby air flow through their direct connexions with the primary bronchus (Fig. 2C).During expiration air from the posterior sacs flows through the tertiary bronchi to thecraniomedial secondary bronchi and into the primary bronchus; the anterior sacsempty directly through the craniomedial secondary bronchi into the primary bronchus(Fig. 2 F). During inspiration there is insignificant flow through the bulk of the tertiarybronchi, and during expiration there is insignificant flow cranially in the primarybronchus.

Zeuthen (1942) studied changes in gas composition at various sites in the chickenlung after inhalation of hydrogen and air mixtures. He proposed reciprocating flowpatterns as indicated in Fig. 2D, H, but he felt that there might be some differencesbetween the volumes flowing in the various passage-ways during inspiration and ex-piration.

Hazelhoff (1951) studied the movement and deposition of airborne particles in thepassageways of the lungs of crows, chickens, pigeons and herons, and also experimented

i o6 W. L. BRETZ AND K. SCHMIDT-NIELSEN

with a glass model to investigate patterns of air flow. He proposed the concept ofunidirectional flow cranially in the tertiary bronchi during both inspiration andexpiration, 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 slightflow caudally in the primary bronchus during expiration.

Inspiration

A. Dotterweich, 1933; Hazelhoff, 1951; Conn &Shannon, 1968;' Schmidt Nielsen et a/. 1969

Expiration

F. Dotterweich, 1933; Vos, 1934; Haielhoff,' 1951; Conn & Shannon, 1968

B. Dotterweich, 1936 G. Dotterweich, 1936; Shepard et af. 1959

••. • ."pTi'-n

'; . " " " ) . . . 1 • • '

\ :X :.i I - ' . 1 .

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 avianrespiratory system. Arrows indicate air flow either specifically proposed or implicit in thevarious hypotheses, crosses indicate insignificant air flow or no air flow. For identification ofthe regions of the lung, compare with Fig. i.

Shepard et al. (1959) analysed the gas composition of samples withdrawn from therespiratory system of chickens, and concluded that during inspiration air flows throughthe tertiary bronchi to the air sacs, and during expiration air flows through the directconnexions 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 proposethat during inspiration air flows to the anterior sacs from the tertiary bronchi, whilethe posterior sacs fill through their direct connexions with the primary bronchus(Fig. 2A). During expiration the posterior sacs empty through the tertiary bronchialroute and the anterior sacs empty through the craniomedial secondary bronchi directlyinto the primary bronchus (Fig. 2 F).

Schmidt-Nielsen et al. (1969) studied the ostrich and included observations onpanting as well as on resting birds. Their observations indicated that during inspirationair passes directly to the posterior sacs via the primary bronchus while the anteriorsacs receive air from the tertiary bronchi (Fig. 2 A). The fact that the panting ostrichdid not become severely alkalotic, although the air-sac COg concentrations were verylow, suggests that a large fraction of the respiratory air is shunted past the lung.

These previously proposed patterns of air flow are, without exception, inferencesdrawn from indirect approaches. With the many conflicting theories in mind, we feltthat by determining directly the direction of air flow at specific sites (e.g. the primarybronchus, the craniomedial secondary bronchi, and the caudodorsal secondarybronchi), 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 localfarmers, 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, respiratoryrate, body temperature, and recordings of air-flow direction could be made on animalsthat were (a) anaesthetized, (b) unanaesthetized and resting quietly at room tempera-ture, and (c) panting due to an ambient heat load. The experiments on panting wereintended to force the animal to hyperventilate, and were not intended to be a study ofthermoregulation as such.

Measurements on unimplanted animals were made in order to establish a basis forevaluating 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 andcontinuously ventilated at a rate of 595 1 min"1. The relative humidity ranged between55% at 230 C and 27% at 400 C. An adjustable cloth sling supported the animal ina position similar to normal standing posture with the head extended (Fig. 3). Weconsider an upright position important, and some results previously reported may bemisleading because the birds were kept on their backs or sides.

Tidal volumes and respiratory rates were determined by measuring the pressuredifferential across a low-resistance screen mounted in the opening of a hood sealedaround 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) per-mitted continuous recording of this pressure differential on one channel of a SanbornSeries 7700 polygraph. The output of the carrier pre-amplifier was integrated (Sanbornintegrating pre-amplifier, Model 350-3700A) and recorded on an adjacent channel ofthe polygraph. Respiratory rate could be determined from the pressure recording, andthe time integral of the positive portion of the pressure differential was proportionalto the inspired volume (inspired volume was considered equivalent to tidal volume).This system was calibrated against known reciprocating volumes of air flow generatedby a Harvard Respirator (Model 665), and had an accuracy of ± 5 % of the maximumreciprocating volume (100 ml) at all frequencies tested (10-125 cyles min"1).

r i~-

>-—_

Hood formeasuringrespiratoryvolumes

—s=^ "̂-~

%

Implantationsite for airflow directionprobe

\ \

Rectalthermistorprobe

Fig. 3. Restraint and support of experimental animal. Shaded areas indicate tape holdinganimal to a support rod along its back. Dashed line indicates the outline of a cloth sling usedfor 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 measure-ments. Our probe contained two heated microthermistors (Fenwal BC32J1), con-nected with two identical Wheatstone bridges (Fig. 4). The thermistors were mountedso that when the probe was positioned axially in an air conduit, either the distal or theproximal thermistor was relatively more shielded than the other, depending on thedirection of air flow. The two heated thermistors would therefore have different ratesof heat dissipation during air flow. The difference was reflected in the output potentialsof the bridges to which they were connected. Comparison of the slopes of the twobridge outputs permitted the determination of air-flow direction past the probe. Theoutputs were recorded on two adjacent channels of a Sanborn Series 7700 polygraph,using Sanborn low-level pre-amplifiers (Model 350-1500A) equipped with Sanborn350-2B d.c. plug-in units.

Body temperatures were measured to ± 0-2° C with calibrated thermistor probesinserted 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 Equithesinintramuscularly) was fastened to a support rod with masking tape (Fig. 3). The denseplumage in the ventral thoracic region provided a thick, compressible cushion betweenthe 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. Thismethod of restraint was used to prevent movements of the neck which could displacethe implanted air-flow direction probe.

\ v, V y> .

—P

Fig. 4. Straight and recurved air-flow direction probes. D = distal thermistor, P = proximalthermistor. The leads from each thermistor of a probe connect to separate but identicalWheatstone bridges. Total probe length about 35 cm. Scale: 2 x .

The air-flow probes were implanted in the lung via a midneck tracheostomy. Thepositioning of the probe at an appropriate site in the passageways was achieved byfeel and was confirmed by dissection at the end of the experiment. The required depthof insertion was estimated from the bird's external anatomy. The primary bronchuscurves dorsally just caudally from the craniomedial bronchial orifices, and this couldbe felt when the distal end of the probe reached this point. This was the most usefulclue for positioning a straight probe in the primary bronchus. The recurved probeswere 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 move-ment until the probe was caught in a secondary bronchus (once this happened theprobe could usually be repositioned only in a more caudal bronchus). The exactplacement of the probe depended on a certain degree of luck, and frequently theplacement was not as intended (as was discovered upon later dissection). After place-ment the leads were taped against the neck to prevent caudal or cranial slipping fromthe position of the probe in the lung, and the incision was closed with wound clipsand bandaged.

Experimental procedure

After implantation of the probe the bird was placed in an adjustable sling in thetemperature-controlled chamber. Recordings of tidal volume, air-flow directions, andchamber 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

n o W. L. BRETZ AND K. SCHMIDT-NIELSEN

withheld). Then recordings were made while the animal was resting quietly at roomtemperature (23-250 C). To induce panting, chamber temperature was then quicklyraised to 350 C. If after 30 min at 350 C the animal had not begun to pant, the ambienttemperature was raised to 400 C, which always induced panting. Tidal volume andair-flow directions were continuously recorded. Immediately after the animal beganto pant the heating element of the chamber was turned off and its temperature wasallowed to return to room temperature while recordings were continued until bodytemperature had returned to normal (its level prior to the heat load) in about halfan 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 proce-dure 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 withthe 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 wasattempted on 22 animals. Eleven of the experiments were successful and 11 failed dueto malfunctioning or to poor positioning of the implanted probe.

Fig. 5 A is a representative output recording from the two channels of a probe placedin the upper, unbranched portion of a primary bronchus. This is a trivial case for theunderstanding of flow direction, but it is useful in showing the interpretation of arecording when it is known that volume of flow is equal in both directions. Duringinspiration the proximal thermistor is unshielded to air flow and the distal thermistoris shielded. The proximal thermistor therefore displays a greater change in the signal.During exhalation the situation is reversed, the distal thermistor is now unshieldedand gives the greater signal.

Fig. 5 B is a recording from a recurved probe positioned in the third caudodorsalsecondary bronchus of the left lung. The proximal thermistor was unshielded withrespect to flow from the primary bronchus into the secondary bronchus, and the distalthermistor was unshielded with respect to flow in the opposite direction. During bothphases of the respiratory cycle, the rate of change of the signal from the proximalthermistor was greater than that from the distal thermistor (the attenuation for theproximal thermistor was 5 x that for the distal), indicating that during both inspirationand expiration the proximal thermistor was unshielded with respect to air flow, whilethe distal thermistor remained shielded. Thus, during both phases of the respiratorycycle air was flowing from the primary bronchus into this secondary bronchus. Thisparticular recording was from an unanaesthetized bird with a respiratory rate of19-5 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 primarybronchus of the right lung at the level where the caudodorsal secondary bronchusbranches off. The proximal thermistor was unshielded with respect to flow caudallyin 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 proximalthermistor was greater than that from the distal thermistor (the attenuation of thechannel for the proximal thermistor was 2-5 x that for the distal), indicating thatduring 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 inthis part of the primary bronchus, as both thermistors returned towards balance. Atthe time of this recording the bird was anaesthetized, with a respiratory rate of 30cycles 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 indicatedto the right of each recording. (A) Probe located in primary bronchus. Attenuation equal forproximal and distal channels. (B) Probe located in caudodorsal secondary bronchus. Attenua-tion 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 ofinspiration 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 waspositioned 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 craniomedialsecondary bronchus (once in the right lung and once in the left lung), or in a caudo-dorsal secondary bronchus (once in the right lung and twice in left lungs). Althoughthe probes could not be calibrated to yield absolute flow rates, comparisons betweeninspiratory 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). Informationused in Fig. 6 was obtained from both males and females; no difference in air-flowpatterns was observed between sexes.

Inspirator/ patterns Expiratory patternsResting

Panting

Anaesthetized

Fig. 6. Directions of air flow in the duck lung. Solid symbols (arrows and crosses) indicate theresults of this study. Dashed arrows indicate directions inferred from previous studies, andwhich are consistent with our findings (see Discussion). Differences in flow between inspirationand expiration at a given site are suggested by the length of the arrows. For identification ofregions of the lung, see Fig. i.

Effects of implantation of probes

It is important for the interpretation of the recordings to know whether the implanta-tion of the probes has pronounced effects on respiratory function. The probes weredesigned 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 normalpatterns, we would expect this to result in detectable changes in such parameters asrespiratory rate and tidal volume.

We therefore compared respiratory rate, tidal volume, and body temperature ofnine ducks (mean wt 27 kg) implanted with air-flow direction probes and of eightunimplanted 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 minutevolume was at its maximum. In all instances the difference between mean values formplante d and unimplanted animals was not statistically significant, as indicated byStudent'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.)

AnaesthetizedImplantedUnimplanted

RestingImplantedUnimplanted

PantingImplantedUnimplanted

Resp. rate(cycles min"1)

I49±3'2—

i3 '3±i '4l6-I ±1-2

iiS"7±i4'9i3o-4±ii-9

Tidal volume(ml)

568 ±6-4—

75"4±5'672-2 ±7-9

34O±3-434-1 ±4'6

DISCUSSION

Body temp(°C)

40-9 ±0-2—

4I-2±O-24i-6±o-i

42'S±o-342'4±O-2

Previous experimental studies

Although there are interspecific variations in the anatomy of the avian respiratorysystem, the general arrangement of lung passageways and air sacs is similar in mostbirds. It therefore seems reasonable to compare our data and those of other investi-gators for the purpose of obtaining a generalized picture. In view of the considerableconfusion and many contradicting theories in this field it is particularly useful to notethat many previous results are in accord with our findings.

Gas-composition data. The normal gas composition at various sites in the respiratorysystem has been established for a variety of birds (duck, chicken, goose, pigeon andostrich) during resting respiration or under anaesthesia (Dotterweich, 1933; Vos,1934; Makowski, 1938; Scharnke, 1938; Graham, 1939; Zeuthen, 1942; Shepard etal. 1959; Cohn, Burke & Markesberg, 1963; Cohn & Shannon, 1968; Schmidt-Nielsen et al. 1969). Considering the similarity of the results of the different investi-gators, the lack of agreement among the numerous theories concerning air-flowpatterns is surprising.

In general, the posterior air sacs contain gas that has a higher 0 2 and lower C02

content than the gas in the anterior sacs. End-tidal gas is similar to the gas in theanterior sacs. During panting the anterior sacs contain gas with a composition whichresembles that in the posterior sacs at rest, while the posterior sacs during pantingmore closely approach atmospheric air.

Many authors have reported such results, and they can be interpreted in the follow-ing way. On inspiration the posterior sacs receive most of the air present in the deadspace plus inhaled fresh air that has not been exposed to gas-exchange surfaces. Theanterior sacs on inspiration receive primarily air that comes from the lung and hasundergone gas exchange. During panting the greatly increased ventilation for purposesof evaporative cooling results in a washout of the entire respiratory system, givinghigher 0 2 and lower C02 concentrations in both posterior and anterior air sacs.

8 EXB54

i i 4 W. L. BRETZ AND K. SCHMIDT-NIELSEN

Several investigators measured gas compositions at various sites in birds which hadinhaled 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 thepreceding paragraph, although the investigators have not always interpreted theirresults in this way.

Pressure data. Baer (1896) and Soum (cited from Zeuthen, 1942) measured simul-taneous increases during inspiration, and decreases during expiration, in the pressurein both anterior and posterior air sacs. Such synchronous pressure changes have beenobserved 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 synchron-ously, and that substantial movement of air from one sac to another during a givenphase of the respiratory cycle is improbable.

Deposition of paniculate matter. The deposition of inhaled or insufflated particulatematter (e.g. finely divided carbon or barium sulphate) on the walls of the passagewaysin the respiratory system was studied by Dotterweich (1930), Vos (1934), Walter(1934), Graham (1939) and Hazelhoff (1951). Except for Walter, these investigatorsfound similar patterns of non-uniform deposition. These studies suggest that duringinspiration much of the air must flow into the direct connexions to the posterior airsacs and the caudodorsal secondary bronchi, with little or no flow into the craniomedialsecondary bronchi. Furthermore, it appears that during expiration there must beconsiderable flow from the posterior air sacs through their recurrent connexions intothe tertiary bronchi of the lung, and that air flow cranially in the primary bronchussomehow must be blocked just cranially to the orifices of the caudodorsal secondarybronchi. In Walter's experiments there was a uniform distribution of particulatematter 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, allowingair to flow into the respiratory system via the interclavicular air sac.) Although theydid not propose a definite pattern, their results suggest that there is a relatively complexair flow in the lung, rather than simple reciprocal movements as proposed by Scharnke(1938) and Zeuthen (1942). We see no contradiction between their results and ourproposed pattern of flow.

Calder & Schmidt-Nielsen (1966, 1968) studied the result of high ventilation ratesdue to panting (induced by heat load), on the P c 0 , of the arterial blood in nine speciesof birds. Their data suggest that the exchange surfaces of the lung are over-ventilatedduring panting, relative to the need for oxygen, resulting in excessive loss of COa andrespiratory 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 gas-exchange surfaces during panting.

Bird respiration 115

Discussion of present study

Our experiments have yielded information about the direction of air flow at threesites 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 air flows caudally in the primary bronchus,and from the primary bronchus into the caudodorsal secondary bronchi. The anteriorair sacs are filled during inspiration primarily by air that has passed over gas-exchangesurfaces of the lung, while the posterior air sacs receive dead-space air and a con-siderable portion of the inspired air directly through non-exchanging conduits, i.e.the primary bronchus. The flow of air through the craniomedial secondary bronchidirectly to the anterior sacs is small, and air flowing into the caudodorsal secondarybronchi must flow through the tertiary bronchi towards the anterior air sacs. Theposterior sacs could not receive much of the inspired air through their recurrentconnexions with the tertiary bronchi, for this route would expose the air to gas exchangewith the blood. The recurrent connexions of the interclavicular and anterior thoracicsacs 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 thetertiary bronchi, and in the craniomedial secondary bronchi towards the primarybronchus. The expired air must flow from the posterior sacs through the tertiarybronchi and craniomedial secondary bronchi to reach the primary bronchus. Therecurrent connexions between the posterior sacs and the tertiary bronchi must be veryimportant during this phase of respiration, for very little air flow is detectable in themain part of the primary bronchus. Air expired from the anterior sacs probably passesthrough the most direct route to the primary bronchus, with the recurrent connexionsbeing of little importance during expiration.

(2) Panting respiration. The patterns of air flow during panting are very similar tothose of resting respiration. During inspiration there is no indication of flow into thecraniomedial secondary bronchi, and the anterior sacs must be filled with air flowingfrom the lung. During expiration there is a small flow cranially in the primary bronchus,and air expired from the posterior sacs must flow to the tertiary bronchi through thecaudodorsal secondary bronchi as well as through their recurrent connexions.

(3) Anaesthetized respiration. In this case also the patterns of air flow are similar tothose of resting respiration. The inspiratory flow into the craniomedial secondarybronchi is somewhat stronger than during resting respiration, but otherwise thepatterns are the same.

The patterns of air flow do not appear to be fundamentally different for the threemodes of respiration investigated (resting, panting and anaesthetized). This does notexclude, however, that there can be substantial differences in mass flow of air in partsof the system for different modes of respiration.

Important features of proposed patterns. Two characteristics of the patterns that wepropose deserve special attention.

8-2

n 6 W. L. BRETZ AND K. SCHMIDT-NIELSEN

1. Air flow in the tertiary bronchi, which connect the craniomedial and caudodorsalsecondary bronchi, is unidirectional. Air flows from the caudodorsal secondary bronchithrough the tertiary bronchi to the craniomedial secondary bronchi during bothinspiration and expiration, although the inspiratory flow along this pathway is weakerthan the expiratory flow. This arrangement of air flow through the lung parenchyma(where gas exchange with the blood occurs) would permit a countercurrent exchangesystem in the avian lung, as suggested by Schmidt-Nielsen et al. (1969), providedthat the blood vessels are arranged appropriately around the tertiary bronchi and aircapillaries.

2. There is no fundamental change in the pattern of air flow during resting respira-tion and during panting. There is a small expiratory flow cranially in the primarybronchus while the bird is panting, but this does not shunt a sufficient amount of therespired air away from gas-exchange surfaces to prevent respiratory alkalosis, asCalder & Schmidt-Nielsen (1968) demonstrated in the panting Pekin duck and ineight other species.

Possible control of air-flow patterns. We feel that the patterns of air flow describedfor the Pekin duck are likely to be determined by the anatomical design of the lungand the effects of this design on the dynamics of fluid flow.

The Reynolds number is useful for characterizing the nature of fluid flow. Itexpresses the ratio of the shear stress in a fluid due to turbulence, to the shear stressdue to viscosity. In the equation for the Reynolds number,

u is the velocity of flow, / is a characteristic length, and y is the kinematic viscosityof 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 therespiratory cycle).

The value of u at the beginning of the primary bronchus was computed to be95 cm s~x during resting respiration and 333 cm s - 1 during panting (calculated frommean values for tidal volume and respiratory rate shown in Table 1, a diameter of theprimary bronchus of 0-5 cm (mean of 10 ducks), and the assumption that hah7 of thetidal volume flowed to each lung).

During resting respiration R = 280, and during panting R = 940. For flow in aconduit 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 duringpanting.

The air velocities and Reynolds numbers in the secondary and tertiary bronchimust be considerably lower than in the primary bronchi, for the total cross-sectionof the respiratory system increases rapidly where the secondary bronchi branch fromthe primary bronchus.

Beyond saying that the air flow in the bird lung is laminar, low-velocity, and drivenby very low-pressure differentials, there is little that can be said about the fluiddynamics 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 inthe boundary layer of air flow, e.g. the edges of the orifices in the wall of the primarybronchus. Fluid dynamic phenomena such as this could be a primary factor in con-trolling the patterns of flow that we have described. Investigation into the methodsby 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 inthe respiratory system of birds. The probes did not significantly affect the respiratoryrates, tidal volumes, or body temperatures of birds implanted with the probes ascompared to unimplanted birds.

2. Air-flow directions were determined in the primary bronchus, the craniomedialsecondary bronchi, and the caudodorsal secondary bronchi in the lungs of duckswhich were either unanaesthetized and at rest, anaesthetized, or panting due toheat load.

3. The recorded air-flow directions suggested the following patterns of air flow inthe duck lung for resting respiration.

During inspiration air flows to the posterior air sacs directly from the primarybronchus (the most direct route), without passing through the tertiary bronchi, whileair flows towards the anterior air sacs via the caudodorsal secondary bronchi and thetertiary bronchi (thus by-passing the most direct route, the craniomedial secondarybronchi connecting these sacs to the primary bronchus).

During expiration air flows from the anterior sacs to the primary bronchus via thecraniomedial secondary bronchi (the most direct route), but from the posterior sacsthrough the tertiary bronchi and through branches of the craniomedial secondarybronchi to the primary bronchus (by-passing the most direct route, the portion of themesobronchus posterior to the craniomedial bronchi).

4. The patterns established for panting and anaesthetized respiration were verysimilar to those described for resting respiration. There was no indication of aneffective shunt operating during panting to avoid excessive ventilation of the exchangesurfaces of the lung.

5. Flow in the tertiary bronchi appeared to be in the same direction during bothinspiration and expiration (from the caudodorsal secondary bronchi towards thecraniomedial secondary bronchi). Such unidirectional flow would permit the operationof a counter-current exchange system, provided that the blood vessels are arrangedappropriately around the parabronchi.

This work was supported by NIH Training Grant 2T1 HE5219, an NSF Pre-doctoral 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).

n 8 W. L. BRETZ AND K. SCHMIDT-NIELSEN

REFERENCES

BAER, M. (1896). Beitr3ge zur Kenntnis der Anatoroie und Physiologic der Athemswerkzeuge bei denVfigeln. Z. wist. Zool. 61, 420-98.

BIGGS, P. M. & KING, A. S. (1957). A new experimental approach to the problem of the air pathwaywithin the avian lung. J. Physiol. Land. 138, 282-9.

CALDER, W. A. & SCHMIDT-NIELSEN, K. (1966). Evaporative cooling and respiratory alkalosis in thepigeon. Proc. natn. Acad. Sci. U.SJl. 55, 750-6.

CALDER, W. A. & SCHMIDT-NIELSEN, K. (1968). Panting and blood carbon dioxide in birds. Am. J.Phytiol. 315, 477-8*-

COHN, J. E., BURKE, L. & MARKESBERY, H. (1963). Respiration in unanesthetized geese. Fedn. Proc.*». 397-

COHN, J. E. & SHANNON, R. (1968). Respiration in unanesthetized geese. Resp. Pkyriol. 5, 259-68.DOTTERWEICH, H. (1930). Versuch Qber den Weg der Atemluft in der Vogellunge. Z. vergl. Pkysiol.

11, 271-84.DOTTERWEICH, H. (1933). Ein weiterer Beitrag zur Atmungsphysiologie der V6gel. Z. vergl. Physiol.

18, 803-9.DOTTERWBICH, H. (1936). Die Atmung der V6gel. Z. vergl. Pliytiol. 23, 744-70.FRANCOIS-FRANK, M. (1906). Etudes graphiques et photographiques de mechanique respiratorie com-

paree. C.r. Soc. Biol. 61, 174-6.GRAHAM, J. D. P. (1939). The air stream in the lung of the fowl..7- Physiol. Land. 97, 133-7.GRAHN, A. R., PAUL, M. H. & WESSEL, H. U. (1969). A new direction-sensitive probe for catheter-tip

thermal velocity measurements. J. appl. Physiol. 37, 407-12.HAZKLHOFF, E. H. (1951). Structure and function of the lung of birds. Poult. Sci. 30, 3-10. (Reprinted

from: Venl. geuxme Vergad. Afd. Natuurk. K. ned. Akad. Wet. 53, 391-400, 1943.)KINO, A. S. (1966). Structural and functional aspects of the avian lungs and air sacs. In International

Review of General and Experimental Zoology, Vol. 2. New York: Academic Press.LASIEWSKI, R. C. Avian respiratory function. In Avian Biology, Vol. 2. Eds. D. S. Farner and J. R.

King. New York: Academic Press. (In the Press.)MAKOWSKI, J. (1938). Beitrag zur Klfirung des Atmungsmechanismus der Vflgel. PflUger's Arch. get.

Phyriol. 340, 407-18.SCHARNKE, H. (1938). Experixnentelle Beitrflge zur Kenntnis der Vogelatmung. Z. vergl. Phyriol. 35,

548-83.SCHMIDT-NIELSEN, K., KANWISHER, J., LASIEWSKI, R. C , COHN, J. E. & BRETZ, W. L, (1969). Tem-

perature regulation and respiration in the ostrich. Condor 71, 341—52.SHEPARD, R. H., SLADEN, B. K., PETERSON, N. & ENNS, T. (1959). Path taken by gases through the

respiratory system of the chicken. J. appl. Pkyriol. 14, 733~5-STREETER, V. L. (1966). Fluid Mechanics. New York: McGraw-Hill, Inc.VICTOROW, C. (1909). Die kiihlende Wirkung der Luftsacke bei Vflgeln. PflOger't Arch. ges. Physiol.

136, 300-22.Vos, H. J. (1934). Ober den Weg der Atemluft in der Entenlunge. Z. vergl. Physiol. 31, 552-78.WALTER, W. G. (1934). BeitrSge zur Frage uber den Weg der Luft in den Atmungsorganen der VOgel.

Archs. neerl. Physiol. 19, 529-37.ZEUTHEN, E. (1942). The ventilation of the respiratory tract in birds. K. danske Vidensk. Seltk. Biol.

Medd. 17, 1-51.