Vol. 56]
1939J
GILBERT,
TheArianLungandAir-Sac
System
THE
AVIAN
LUNG
AND
BY PERRY
W.
AIR-SAC
57
SYSTEM
GILBERT
Plate •
IN the followingpagesthe author has attemptedto reviewbriefly the
main contributions
pertinentto an understanding
of the avianlungand airsac system. Supplementing
this review is a descriptionof a methodfor
castingthe systemusingWoodsAlloy. Castsweremadeof the lungsand
air sacsof the Domesticated
Pigeon(Columba
livia). This bird waschosen
becauseconsiderable
work had alreadybeendoneon its respiratorysystem.
I am indebtedto the Departmentof Zoologyat Dartmouth Collegefor
furnishingme the necessary
equipmentwith which to pursuethe experimental aspectof this problem. I alsowishto thank Dr. N. K. Arnold and
Dr. W. W. Ballardfor their encouraging
enthusiasm
and assistance.
HISTORICAL
For over two and one-half centuries it has been known that there are
certainstructuresaccessory
to the blrd'slung--the air sacs. Harvey (1651)
was the first to describethem carefully. For the next century and a half
investigatorsspeculatedwidely as to the functionof the sacsbut it was not
until 1828that any markedscientificinformationwas obtainedconcerning
them. From this time on, we find the investigatorsfalling into four main
groups--embryological,
histologlcal,morphological
and physiological.
As to the embryologicalobservations,the earliest contributionis by
Rathke (1828) in whichwe find the first figuresof the budsof ecto- and
entobronchi. Selenka(1866) wrote concerning
the developmentof the air
sacsand His, two yearslater, on the laryngo-tracheal
grooveand trachea.
Zumsteinin 1900explainedthe natureof the bronchialtree and the air sacs.
The sacs and their method of growth were further descriSedby Moser
(1902). Juillet (1911) publisheda comprehensive
treatise embracingthe
anatomical, embryological,histological,and comparative study of the
bird's lung. He emphasizedthe important fact that the branchesof the
bronchiin the lungneverendin 'cul-de-sacs,'
but are all in intercommunication, formingcircuitswhich can be traversedby pure air, from one end or
the other, accordingto whether the air comesfrom the air sacsor the
trachea. Thus the lung consistsof a labyrinth of air-containingbranches
interpenetratedby a labyrinth of blood capillaries,each of which is surroundedon all sidesby air. The latest investigations
of an embryological
nature were carriedout by William Locy and Olof Larsell (1916). These
investigatorshave attached much importanceto the 'recurrentbronchi,'
recognizedby Schulzeand Juillet, which springfrom the air sacsand grow
The Av•, Vo•.. 56
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CASTS OF A•R-SAC •YSTEM OF THE I)IGEON
4
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GILBERT,
TheArianLung
andAir-Sac
System
Auk
[Jan.
back into the lungswherethey establishnumerousconnections
with the
bronchial branches.
We will have occasion to refer to the work of these
men later.
The mainhistological
contributions
havebeenadvancedby F. E. Schulze
(1871);M. J. Ross(1899);andOppel(1905).
Campana(1875) wasthe first to makea carefulanalysisof the anatomy
of the bronchialpassages.His investigations
broughtto light the bronchial
circuitswhich unite the variousdivisionsof the bronchiinto a plexusof
intercommunicating
passages.He alsonoticedrecurrentbronchiwithout
understanding
their significance.Huxley (1882)broughtthe termsmesobronchium,ecto-,ento-, and parabronchiinto commonuse. The air sacs
in the adult bird have beenfurther describedby Bruno Miiller (1908) who
workedon the pigeon. In his treatise'On the Air Sacsof the Pigeon'he
givesa mostdetailedandcarefuldescription
of the sacsthemselves
without
involvingthe anatomyof the lungs. Someof his methodsand resultsobtainedwill be referredto below. F.E. Schulze(1911) publishedan excdlent paperon the comparative
anatomyof the air sacsin the adult. Here,
for the first time, the recurrent bronchi were fully describedand their
physiological
officewaspointedout. The mostrecentobservations
on the
morphology
of the bird'slung are containedin the paperof Juillet mentioned above. Here alsomay be found a review of previouswork doneon
the avianlungand air sacs.
Little workhasbeendonethusfar pertainingto the physiologyof the air
sacs. Campana'spaperon the 'Physiologyand Respirationof Birds' is of
chief importanceanatomically. Sincethe time of Harvey the functionof
the air sacshasprovedfertile soilfor speculation.The followingfunctions
have been attributed to them: aid in raising feathers;act as resonatory
organs;lessenspecificgravity of bird; regulatethe body temperature;fix
wingsin a distended
position;have a functionanalogous
to that of a swim
bladder;havea respiratory
function. M'tiller(1908)rejectedall theseideas
andmadethe followingstatement:"I donot considerthe air sacs,including
the air cavitiesof bones,as organshavinga positiveand specialfunction,
but rather asa systemof emptyinterspaces.Their valueliesin their emptiness-that is, in their containingnothingthat offersresistance
or has appreciableweight."
PRESENT STATUS OF AVIAN LUNG AND AIR-SAc SYSTEM
It is throughthe carefulinvestigations
of Schulze(1911),Juillet (1911),
andLoeyandLarsell(1910)that we arrivefinallyat ourpresentconception
of the avian lung and accessory
air sacs. Breathingin birdsis specialized
in relationto flight, to song,and to intenseactivity in general. The lungs,
thoughrelativelysmallandhardlydistensible,
havea largeinternalsurface
'•'ol.
1939
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GILBERT,
TheA•ianLung
andAir-Sac
System
59
for gaseous
exchange.The drivingout of air is assisted
by strokesof the
wings. Expirationis the activepart of the respiratoryprocess,
not inspiration as in mammals.
Justposteriorto the tongueis the glottis,the openinginto the trachea.
The upperpart of the tracheais knownasthe larynx,which,unlikethat of
mammals,possesses
no vocalcords. It is supportedby cartilageswhich
are transformed
representatives
of the branehialarches. The tracheais
supported
by bonyringswhichusuallyforma complete
circuitaroundthe
wind pipe. It is movedby two sternotracheal
musclesattachedto the
anteriorpart of the sternum. The baseof the tracheais enlargedto form
the syrinxor voice-box,
an organfoundin mostbirdsthoughabsentin
ostriches,storksand somevultures. The three upper rings of the two
bronchialtubesalsoaid in the formationof the syrinx. The shortbronehi
divide in a uniquefashionto form the lung. A main stempasses
right
throughas the mesobronehus
and leadsinto the abdominalair sac. The
greaterpart of the mesobronehus
appearsto be dilated. From this enlargedportionsecondary
bronehiarise,someof whichleaddirectlyintothe
air sacs,whileothersmergeinto the highlybranched
parabronehi
(tertiary
bronehi)supplyingthe lung. Theseparabronehiare continuous,
thus
forminga networkof air capillaries--thebronchialcircuit. Buddingoff
from the air sacsare the 'recurrentbronehi'which lead into the lung paren-
chymaandmergewith variousparabronehial
air capillaries."By meansof
the recurrent bronchi and their anastomoseswith other branches of the
bronchial circuits the air-sacsare brought into communicationwith all
partsof the lung. They havedirectcommunication
with bronchus
and
centrallungtubethroughtheir'directorifices'
anda recurrent
communicationthrough
therecurrent
bronehi"
(LoeyandLarsell,1916,part2, p. 21).
Thusthe air sacsare not to be thoughtof altogether,at least,asterminal
sacs;"they maybe regardedas expanded
reservoirs
on the courseof the
bronchialcircuits"(Thomson,1923,p. 129).
It is nowgenerally
accepted
that thereare ninesacsaccessory
to the
arian lung. Fourpairedsacsandone.singlesaccanbe distinguished
as
follows:
(1) Cervicalsacs(paired)--inregionof the napeof the neck.
(2) Interclavicular
sac(single)--adherent
to syrinxand situatedventrally,laterally,andproximally
to it. Numerous
diverticula
arisefromthis
sacincluding
thesubscapulare,
axillare,suprahumerale,
andsternale.
(3) Anteriorintermediate
sacs(paired)--separated
from lungby pulmonarydiaphragm.
(4) Posterior
intermediate
sacs(paired)--asymmetrical,
left sacreaching
fartherposteriorly
andlargerthanright. Left sacextends
beyondlastrib
into abdominalcavity. Right sacextendsbut little or not at all beyond
last rib.
60
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GIZB•RT,
TheArianLung
andAir-Sac
Sy•te•t
[Auk
LJan.
(5) Abdominalsacs(paired)--largestof all sacs;enterabdominalcavity
dorsallyand partially encloseviscera;have severalaccessory
diverticula.
One may find further detail as to the relativesizeand locationof the sacs
in Miiller's (1908)treatiseon the 'Air Sacsof the Pigeon.'
The sacsappearas thin transparentmembranes,with more or lessof a
fibrousconnective-tissue
basement. All the sacs,with the exceptionof the
interclavicular,can be freedof connections
with adjacenttissues. The sacs
are lined with pavementepithelium. Where the sac is attachedto surroundingtissuethe lining cellsbecomecolumnar. Cilia are presentoverthe
entire surfaceof the sacscontainedwithin the body cavity. They are
absent,however,in the prolongations
of the sacsinto the joints and in the
cavitiesof the bones. The function of the cilia is not definitely known but
is believedto be that of removingexfoliatedepitheliumand foreignsubstancesfrom the sacs. Brief histologicalreviewsof the air-sacsystemhave
beensetforth by M. J. Ross(1899)and by Oppel(1905).
The excellenttreatiseon 'The Embryologyof the Bird's Lung' by W. A.
Locy and Olof Larsell(1916)hasshedmuchlight uponthe developmentof
the avian lung and air-sacsystem. They succeeded
in tracingthe development of the lung and air-sacsystemin the chickembryofrom the time the
eggwaslaid up throughtime of hatching. The followingare someof their
interestingobservations.The lung becamedefinablenear the closeof the
third day of incubation. The abdominaland cervicalsacswerethe first to
appearat the end of the seventhday. Thesewerefollowedshortly by the
anterior and posteriorintermediates,the interclavicularbeingthe last to
appear. At the end of the ninth day all sacshad projectedbeyondthe periphery of the lung. The recurrentbronchimadetheir fLrstappearanceafter
ten and one-halfdays of incubation. All the sacsexceptthe cervicalpossessed these recurrent branches.
As to the presentconceptions
concerningthe functionsof the sacs,much
may be said. Locy and Larsellstate: "The lung of birdsis not largein extent, but it is highly vascularand the continuousair current from the air
sacs through the recurrent bronchi makes it an effective apparatus for
aSrationof the blood." The air sacsare alsobelievedto promoteinternal
perspiration,thus aidingin regulatingthe high temperatureof the avian
body. "Most birdstake muchwater, but thereis little water in their urine,
whichis semi-solid,and they have no sweatglandslike mammals. Hence,
the advantageof the internal surfacesof the air sacs,for water-vapour
diffusesfrom the blood into the cavities and passesout by the lungs"
(Thomson,1923,p. 128). Thus the theory of M•ller that the air sacshave
no definite function but are valuable becauseof their emptiness,tends to
overemphasizeone aspect.
Vol. 56]
1939
J
GILBERT,
TheArianLung
andAir-•acSystem
METnOD for
61
CASTING
Sincethe author was especiallyinterestedin the relative positionsof the
sacsand their accessory
diverticula,the mostsatisfactoryapproachto the
problemwasby meansof casts. Severaltypesof injectionmasses
wereconsideredincluding Fol's metagelatin vehicle, celloidin, gelatin, paraffine,
Woods Alloy and Darcet's metal. Finally it was resolvedto use Woods
Alloy. This fusiblealloy is made up of bismuth,lead, tin and cadmium,
hasa specific•ravity of 9.5 and a meltingpoint at 70ø C.
Rather than go through the long formalin-hardeningprocessof Miiller
and injecting individual sacs,it was decidedto inject directly into the
tracheaof a pigeonfreshlykilled with ether. About 600 gramsof Woods
Alloy weremeltedin a beakerplacedin boilingwater. The meltedmetal was
then transferredinto the chamberof the syringewhich washeatedfurther.
Simultaneouslythe pigeonwas heateda few minutesin a water bath at a
temperatureof approximately65ø C. The bird was then removedfrom the
water bath and the tracheaquicklyexposedand slit for the receptionof the
syringecanula. The posteriorend of eachabdominalsacwaspuncturedso
that air in the lungsand sacsmight escapeand be replacedby WoodsAlloy.
The injectiontime lastedforty-five seconds.During this processthe bird
was held with the left hand while the syringewas manipulatedwith the
right. A glovewasusedto insulatethe right hand. The WoodsAlloy remainedfluid approximatelya minute and a half. This gave time to massageand turn the bird in variouspositionsso that the metal might be uniformly distributedthroughoutthe system. The metal was allowedto set
for half an hour beforethe castsweredissectedout. In the caseof the lung
and smaller diverticula where dissectionwas difficult, artificial gastric
juiceproveda usefulagentin digestingaway neighboringtissue.
The anterior and posteriorintermediatesacscast well consistently. To
obtain the remainingsacsit was necessaryto place the bird in various
positionswhile injectingthe metal and then to hold the bird head downward, closingthe trachea to prevent back flow. The castof the interclao
vicular sacand diverticulumsternalewas obtainedby allowingthe bird to
rest on its ventral surface. The best lung detail was obtainedwhen the
bird rested on its dorsal surface. The abdominal sacs were the most difficult
to cast. This wasprobablydue to the fact that they werefarthestfrom the
point of injectionand the metal beganto coolbeforereachingtheir orifices
from the mesobronchi.Thus it was necessaryto place the posteriorand
middleportionsof the bird in a hot bath and inject whilethe longaxisof the
bird was vertical. The subscapulare,
axillare, and suprahumeralediverticula were obtainedby puncturingthe pneumatizedhumerus.
62
GILBERT,
TheArianLung
andAir-Sac
System
[Auk
[Jan.
DISCUSSION
The castsobtainedagreerather closelywith thoseof Mfiller (1908) who
usedwax as an injection mass. The advantageof Woods Alloy over wax
lies in the fact that the former is more permanentand lesslikely to be
secondarilydistorted. By injectingdirectlyinto a warm, freshlykilled bird
the long formalin-hardeningprocessof Mfiller and the alcohol-distension
processof Locy and Larsell are eliminated. Becauseof the pressurewith
whichthe metalwasforcedinto the sacs,the completecastsobtainedprobably representthe sacsat their maximumdistension.By regulatingthe
amountof metalinjectedand the positionof the bird duringthe injection
it is possible
to castonlya desiredpart of the system(seePlate4). Duplicate
and unsatisfactorycastsmay be me]tedand the metal injectedinto another
bird. Castsof the lungand air sacshaveprovedusefulas teachingdemonstrationsand it is hopedwill be of servicein •nakinga cmnparative•norphologiealstudy of this remarkablearian system.
BIBLIOGRAPHY
BEDDARD,F. E.
1898. The structure and classificationof birds. Longmans, Green & Co., New
York, pp. xx + 548.
CAMPANA
1875. Physiologie de la respiration chez les oiseaux. Anatomie de l'appareil
pneumatique-pulmonaire,de faux diaphragmes, des sereuseset de Fintestin chezle poulet. Massonet Cie., Paris.
HARVEY, W.
1651. Exercitatio 3. Exercitationes de generatione animalium.
H•x•Y,
T.
1882. On the respiratory.organsof Apleryx. Proc. Zool. Soc. London for 1882,
pp. 560-571.
JUILLET,M. A.
1911. Recherehesanatomiques,embryologiques,histologiqueset comparatives
sur le poumon des oiseaux. Arch. de Zool. Experiment. et G•n., 9: 207-371.
LocY, W. A., •D LARSELL,0.
1916. The embryologyof the bird's lung (Part I). Amer. Journ. Anat., 19:
447-504.
1916a. The embryologyof the bird'slm•g (Part II).
Amer. Journ. Anat., 20: 1-44.
MOSER,FANNY
1902. Beltrage zur vergleichendenEntwicklungsgeschichteder Wirbeltierlunge.
Arch. f. Mikros. Anat., 60: 587-688, pl. 30-33.
MCLLER, B.
1908. The air-sacsof the pigeon. SmithsonianMisc. Coll., 50: 365-414.
NEWTON,A.
1896. A dictionaryof birds. Adam and CharlesBlack, London, 1088 pp.
0PPEL,A.
1905. Atmungsapparat. 0ppel, Lehrbuch der vergleichendenmikroskopischen
Anatomie der Wirbeltiere, 6: 312.
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1939J
GILBERT,
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System
63
PYCRAFT•W. P.
1910. A historyof birds. Methuen & Co., London,xxx + 458 pp.
RATItKE,l-I.
1828. Ueberdie EntwicklungderAtemwerkzeugebei denVSgelnund Saugetieren.
Nova Acta Acad. Leop.-Carol., 14: 159.
Ross, MARY J.
1899. Special structural features in the air-sacs of birds. Trans. Amer. Micr.
Soc., 20: 29-40.
SCHULZE,F. E.
1871. Die Lungen. Sticker, Handbuch der Lehre yon den GewebendesMenschen
u. der Tiere.
1911. •ber die LuftsackederVSgel. Verhandl.d. viii Internat.Zool.-Kong.
zu
Graz, Aug. 1910, pp. 446-482.
SELENKA•
E.
1866. Beltrag zur Entwickelungsgeschichte
der Luffsachedes Huhn.
Zeitsehr.
f. wiss. Zo51., 16: 178-182.
T•o•soN, J. A.
1923. The biologyof birds. Macmillan Co., New York, 436 pp.
WETMORE,A.
1921. Study of body temperaturesof birds. SmithsonianMisc. Coll., 72: (12)
1-52.
ZUMSTEIN,J.
1900. •er
den Bronchialbaum
der Saugerund VSgel. Sitzungsber.
Ges.z.
BefSrd. d. Ges. Naturwiss., 39-48.
DESCRIPTION OF PLATE 4
Upper left: Ventral view of partial cast, approximately two-thirds natural size.
Note: trachea (a); singleinterclavicularsac (b); left anterior intermediatesac (c);
left posterior intermediate sac (d) with accessorydiverticulum (e).
Upper right: Dorsal view of partial cast, approximatelytwo-thirds natural size.
Note: right cervicalsac (f); right subscapulardiverticulum(g); right lung (h).
Lower left: Dorsal view of nearly completecast, approximatelytwo-thirdsnatural
size. Note: right cervicalsac (f); left suprahumeraldiverticulum (i); right anterior
intermediate sac (c); right posterior intermediate sac (d); right anterior femoral
diverticulum (j); right posteriorfemoral diverticulum (k); right and left abdominal
sacs(l and m). Observeasymmetry of abdominalsacs.
Lower right: Right lateral view of samecast, approximatelytwo-thirdsnatural
size. Note: right anterior intermediate sac (c); right posterior intermediate sac
(d); right abdominal sac (/); left abdominalsac (m).
Department
of Zoology
CornellUniversity
Ithaca, New York