Paper - The embryology of the bird's lung 2 (1916)

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Locy WA. and Larsell O. The embryology of the bird's lung. Based on observations of the domestic fowl. Part II. (1916) Amer. J Anat. 20(1): 1-44.

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This historic 1915 paper by Locy and Larsell describes chicken lung development.

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The embryology of the bird's lung. Based on observations of the domestic fowl. Part II.

William A. Locy And Olof Larsell

Twenty-Two Figures

Part I of this paper appeared in the American Journal of Anatomy, vol. 19, no. 3, May, 1916.

Part III

3. The Air-Sacs And The Recurrent Bronchi

Morphologically considered, the air-sacs and recurrent bronchi are parts of the bronchial tree, but on account of their importance in the avian lung and their unusual interest they are separately considered in this section. This plan also promotes clearness of description, since, at best, the bronchial tree is very complex. The recurrent bronchi, in particular, should receive special notice, because they have been recently recognized and are of capital importance in the physiological anatomy of the lungs.

The name 'recurrent bronchi' has been given to certain bronchial tubes that grow from the air-sacs into the lungs of birds to connect with the other air passages. In this sense they are 'recurrent.' They are outgrowths from the air-sacs, rather than extensions of the bronchial tree from within the lung, and the air-sacs and recurrent bronchi are so intimately related in their development that the two structures should be considered together. In the course of development they unite with twigs of the bronchial tree and thus establish complete circuits with the air passages within the lungs. In the adult lung the air passes from the air-sacs through these recurrent bronchi, entering the lung by a returning current, and, in this sense, the air circuit through these bronchi is a recurrent one.

The credit for the recognition of the morphological arrangement as well as for the part which recurrent bronchi play in the respiration of birds should be divided between Schulze ('09 and '10) and Juillet ('12) who, working independently, and without knowledge of each others observations, grasped the essential features of these very important and characteristic structures of the avian lung. Although they were figured by earlier observers (Campana, '75, Fischer, '05), Schulze was the first to observe carefully their arrangement and relation to the air-sacs and to the other bronchi in a number of different birds, and to appreciate their physiological role, while Juillet added some morphological facts and made observations on their development.

Review of the extensive literature on the air-sacs seems to us unnecessary, since the bulk of it relates to their position, size and anatomical relationships in the adult. In this respect the papers of Campana, '75, Bruno Muller, '07, and Schulze. '11, are especially good. As regards their development, except for the paper of Bertilli, little has been added to the embryology of the airsacs since Selenka's paper of 1866 in which he described and figured their development in the chick.

The recurrent bronchi, however, have come into notice more recently and a brief account of the published observations on these structures should be given.

Campana ('75) in his extensive memoir dealing with the respiratory apparatus of birds and confined chiefly to a description of the adult structures, described the air-sacs and bronchial tree. He also made a careful analysis of the orifices connecting lung and air-sacs. Examination of his figures shows that some of the recurrent bronchi also stand out quite distinctly, but Campana considered them as the result of a reconstitution into a single trunk of several tertiary bronchi, without recognizing their true nature. He apparently considered them as merely a part of the network of air passages with no special significance attached to them.

On the other hand Campana used the term 'Bronche recurrente' in an entirely different connection, applying it to the curvilinear branch of the first entobranchus. This statement should be made to prevent confusion.

Guido Fischer ('05) likewise figures the recurrent bronchi of several of the air-sacs. The only reference he makes to these features of his (M^lloidiu corrosion pi-cparations, however, is in a note of exphmation of one of his figures in which he calls attention to a bronchial trunk larger than the others in the network of air-tubes which extends to the dorsal surface of the lung on its lateral side. This bronchial trunk, he says, 'directs itself toward' the abdominal air-sac, but since it is the nature of recurrent bronchi to grow inward from the air-sacs, the language employed by Fischer shows that he had a wrong conception of these important structures.

F. E. Schulze in 1909, '10 and '11 recognized these bronchi as coming from the air-sacs and designated them both 'Riichljiufigen Bronchen' and 'Bronchi recurrentes sue Saccobronchi.' With sketches he describes their origin from basal pockets on the four posterior air-sacs, variations in the number of their branches as well as the nature of their connections with parabronchi. His comparative observations embraced a variety of birds including the chick, duck, goose, pigeon, Rhea, ostrich, Cassowary, etc. In the Cassowary he noted that recurrent bronchi are lacking on the abdominal air-sac. Schulze also points out that the recurrent bronchi carry air from the air-sacs into the lung parenchyma and play an important part in respiration.

Juillet ('12) made an extensive study of the recurrent bronchi, and since he was unacquainted with the observations of Schulze he claims rank as the discoverer of the true anatomical relations of these structures and of the part they play in the respiration of birds. In all this however he was preceded by Schulze, and to a limited extent he engaged in the study of the embryology of the recurrent bronchi, which was not touched upon by Schulze.

He found recurrent bronchi in all the twenty-four species of birds which he examined. By a study of sections he traced some stages of their development in the embryonic lungs of the chick, and although he does not give an extended account of their developmental history, he arrived at a true conception of their origin and of their nature.

No more important advance in the knowledge of the avian lung has been made since William Harvey, in 1651, discovered the perforations of the bronchi into the air-sacs and found them sufficiently conspicuous in the ostrich to admit the points of my fingers."

It will be advantageous to describe the development of airsacs and recurrent bronchi by stages beginning with the seventh day.

The seventh day stage. There are five air-sacs in the lung of the adult fowl, and as will be shown later, one of these (the interclavicular) is the result of the fusion of four moieties, two from each lung, that arise independently. The names emploj^ed in the following descriptions are: cervical, interclavicular, anterior intermediate, posterior intermediate, and abdominal air-sacs. All the air-sacs, except the interclavicular of the adult, are paired. The cervical and interclavicular arise anteriorly, the other three upon the ventral and caudal surface of the lung.

The youngest embryo in which any of the air-sacs appear as projections beyond the lung wall are of about six days six hours incubation. As shown in figure 30, the abdominal air-sac of this stage projects as an extension from the lung proper. The primordium of this sac is the slightly expanded distal portion of the mesobronchus lying beyond the bend of the central lung tube.

In the same embryo may be seen the first indication of the cervical air-sac in the form of a bud projecting from the distal extremity of the first entobronchus. In its later develoi)ment the entobronchus becomes much branched, and the orifice of the air-sac is not terminal, as in the embryo . but on the body of the cranial branch of the entobronchus.

The anterior intermediate air-sac, with the mesial moiety of the interclavicular united to it, is also foreshadowed in this specimen as a bud of the third entobronchus. The third entobronchus shows at this stage. The beginning of an unequal bifurcation which shortly (figs. 34 and 37) becomes well differentiated. The more caudad, and longer, branch of the bifurcation develops into the foliate division of the entobronchus, and the forward projecting bud becomes eventually differentiated into the anterior intermediate air-sac and the mesial moiety of the interclavicular sac. To avoid confusion, one should constantly keep in mind that the intercla^-icular air-sac arises from two moieties on each side, and in subsequent references we should follow with care the development of a mesial and of a lateral moiety from different sources.

The ninth day stage. In the interval between the seventh and the ninth day the entire bronchial tree grows rapidly and the air-sacs enlarge.

Early on the ninth day of incubation carefully prepared air injections show important advances. The primordia of all five airsacs now project beyond the lung surface.

The cervical sac (fig. 36, is the forward prolongation of the cranial lobe of the first entobronchus and is little changed from the former stage.

In the meantime the first entobronchus has divided into several branches and from one of them (the transverse branch) may now be seen the beginning of the lateral moiety {Lat. inoi.) of the interclavicular sac. At this stage it is small and does not project beyond the lung wall. As shown in subsequent development this lateral moiety fuses with the mesial moiety to form a part of the interclavicular sac of the adult.

The mesial moiety is well developed at this stage. It arises on an anterior branch of the third entobronchus. This branch bifurcates early on the seventh day of development (not figured) . The smaller, and more cephalad, division becomes the mesial moiety of the interclavicular air-sac, the larger, and more caudad, division the anterior intermediate air-sac. As shown in figure 37, the mesial moiety, although very slender on the ninth day, is nevertheless sufficiently elongated to project beyond the lung wall.

Exceptionally the mesial moiety arises on a branch of the second entobronchus, in which case the third entobronchus gives origin only to the anterior intermediate sac. This condition is illustrated in figure 38 which represents a slightly earlier stage than the one sketched in figure 37.

When the development follows the usual rule the mesial moiety of the interclavicular sac is an offshoot of the anterior intermediate air-sac and the two are connected with the third entobronchus by a single orifice (the interclavicular canal).

By unequal growth the anterior intermediate air-sac (fig. 37) has increased relatively much faster than the mesial moiety of the interclavicular and forms, at this stage, a prominent landmark on the ventro-mesial part of the lung. It remains until the eleventh day of incubation the largest of the embryonic air-sacs.

Extending forward from its ventral anterior part may be seen three small papilla-like buds { connected with the sac by a short stem. These buds are the beginnings of the recurrent bronchi of the anterior intermediate air-sac. They make their first appearance (not figured) as a single bud during the latter part of the seventh day of incubation, and by division of the distal end of this bud the three papillae are formed. The proximal end remains as the stem and probably forms the basal pocket of Schulze.

The posterior intermediate air-sac (fig. 36, also makes its first appearance as a projection beyong the lung wall on the ninth day. It is the distal continuation of the third laterobronchus, and at this stage is but slightly distended and shows no indication of recurrent bronchi.

The abdominal air-sac, is on the ninth day of incubation greatly elongated. From its anterior end and point of union with the mesobronchus a pouch is developed which represents the beginning of recurrent bronchi of this sac. The distal end of the sac is but slightly more inflated than it was on the seventh day, but about two-thirds of it now project beyond the lung proper.

From the position of the pouch of the recurrent bronchi one would infer that the anterior limit of the abdominal air-sac of the embryo is more cephalad than is usually recognized. This also changes our idea of the position of the morphological tip of the mesobronchus.

The tenth day stage. From the beginning of the ninth day of incubation to the close of the tenth there is a steady growth of the various air-sacs and of their recurrent bronchi. It is not necessary to follow in detail the various steps between the two stages, since a description of the conditions found in the later stage will sufficiently indicate the changes through which the various structures have passed.

In an embryo of 9| days incubation (figs. 39 and 40) the cervical sac shows only an increase in size proportioned to the general growth of the king.

The lateral moiety of the interclavicular sac (fig. 40, now shows a well defined extension outside the lung wall. The subsequent history of this sac indicates that some of the intrapulmonary part of the transverse branch of the first entobronchus, from which the sac arises, must be considered as a part of the air-sac primordium. The line of separation betwen the entobronchus and the lateral moiety is where the more dorsal buds of recurrent bronchi arise. Two groups of recurrent bronchi belonging to this division of the interclavicular have appeared. The bud which represents the more ventral group of these bronchi extends caudally and ventrally and is as yet undivided. The more dorsal group is represented by an already bifurcated bud projecting caudally and somewhat mesially. These buds develop into the only recurrent bronchi arising from the interclavicular air-sac and it is to be noted that they arise only on its lateral moiety.

The mesial moiety of this stage, a part of which is shown in figure 40, is scarcely changed from the condition described in the eight day embryo, except that it has increased in size.

The anterior intermediate air-sac { at the close of the tenth day of incubation has enlarged considerably, as compared with the preceding stage. The recurrent bronchi have not greatly changed, but the stem thereof has elongated to some extent.

The posterior intermediate sac now projects beyond the lung, and its distal end forms a flask-like swelling. The proximal part remains still constricted and lies within the lung. From this part two buds are seen projecting dorsad and cephalad. The more anterior of these buds is already divided at its tip. These branches indicate the beginnings of the recurrent bronchi of the posterior intermediate air-sac.

The abdominal sac (figs. 39 and 40) has expanded greatly since the eighth day stage, and now lies almost entirely outside the lung. Its recurrent bronchi, of which there are two sets, have also made an obvious growth. The bud (fig. 39) previously described has divided into two main branches each of which has in turn bifurcated, as represented in the figure.

A second group of recurrent bronchi, also belonging to the abdominal sac, begins early in the tenth day of incubation. The bud for this group starts at a point just dorsal to the base of the first-formed group. At the close of the tenth day this outgrowth (fig. 39) has bifurcated so that there is an anterior and a lateral limb. The anterior limb curves gently upward. The lateral branch makes a more sudden turn posteriorly.

Fig. 47 Ventral view of the uninjected luilgs of a ten and one-ha f day embryo. Shows the air-sacs and their recurrent bronchi. The relations of the mesial and lateral moieties of the interclavicular air-sac are well exhibited. Rec.Br., recurrent bronchi, other reference letters as under figure 34.

The eleventh day stage. The eleventh day stage is of some especial interest since it corresponds with Selenka's figure (78) in which two moieties of the interclavicular sac are shown on the left hand of the figure (right lung). The air sacs are all clearly outlined at this stage and the recurrent bronchi have started.

The air-sacs as shown in figures 47 and 48 are relatively much larger than in the earlier stages.

Fig. 48 Lateral view of the left lung of the .same specimen. Showing the early condition of the recurrent bronchi of the four air-sacs possessing them. The mesial moiety of the interclavicular sac is hidden from view.

The cervical, the least modified of all the air-sacs, exhibits an expansion of the distal end, but no recurrent bronchi are developed from it.

The lateral moiety (fig. 47, of the interclavicular sac now projects well beyond the lung surface. The beginnings of the recurrent bronchi of this moiety (first seen in the tenth day stage) have elongated and undergone division. They are not symmetrically developed, those of the right lung showing more branches. Schulze has pointed out that, after the union of the parts to form a single median sac, there are, commonly, recurrent bronchi only on one side.

The mesial moiety { of the interclavicular sac is forked at its extremity into two lobe-like branches, the more mesial of which extends towards the median plane and comes nearly into contact with the corresponding branch from the opposite lung. The laterally extending branch, passes ventral to the extra pulmonary bronchus, and partly engirdles the bronchus on the left hand of the figure.

The anterior intermediate air-sac { has increased in size and its recurrent bronchi are much further developed. They occupy the antero-lateral border very close to those of the lateral moiety of the interclavicular sac.

Figure 47 shows also the connection between the mesial moiety of the interclavicular, and the anterior intermediate — both arising on a common canal (interclavicular canal) that opens into the third entobronchus (entobronchus not shown) .

The posterior intermediate and abdominal air-sacs lie at the caudal extremity of the lung and have obviously increased in size. In figure 47, only the proximal ends of the recurrent bronchi have been sketched since these show on the surface. They exhibit the same relationships as in the tenth day stages.

Figure 48, which is a dorso-lateral view of the same specimen shows to greater advantage the recurrent bronchi from the lateral moiety and the anterior intermediate air-sac at ten and onehalf days. The specimen in this position also shows the recurrent bronchi from the posterior intermediate and abdominal sacs. The enlargement at the base of the recurrent bronchi well exhibited in the posterior intermediate jjrobably corresponds to the basal pocket of Schulze.

Although the general appearance of the air-sacs on the tenth day of development (figs. 36 and 37) have been described, it will be advantageous for comparison to insert at this point a separate sketch of the anterior intermediate air-sac and the mesial moiety of the interclavicular sac. Figure 49 represents these air-sacs as removed from the left lung of an embryo of nine and one-half days incubation. (A) represents a view upon that surface of the anterior intermediate air-sac which is in contact with the lung. It is notable for showing the primordia of recurrent bronchi budding from the anterior lateral border of the air-sac. By comparison with figure 47 it will be observed that the recurrent bronchi of this sac lie close to those from the lateral moiety of the interclavicular sac.

Figure 49 shows further the mesial moiety of the interclavicular sac spinging from a common canal (the interclavicular canal) into which the anterior intermediate sac also opens. The interclavicular in turn opens into the third entobronchus. No recurrent bronchi arise from the mesial moiety. (B) shows a view upon the cephalad surface of the anterior intermediate air-sac and brings into prominence the forked extremity of the mesial moiety of the interclavicular air-sac, and, also shows the common origin from the third entobronchus of the mesial moiety and the anterior intermediate sac.

The twelve and fifteen day stages. The subsequent history of the air-sacs presents little difficulties except as regards the formation of the azygous condition of the interclavicular sac of the adult from the union of four parts which arise separately in the embryo. The changes in this air-sac are so unusual that they will be described more in detail.

The condition of the air-sacs at the close of the twelfth day of incubation is represented in figure 50. This is the camera outline of a dissection and in finishing is made only slightly diagrammatic. The external aspects of lungs and air-sacs are represented but the recurrent bronchi have not been sketched. By comparison with figure 47 (the eleventh day stage) it will be seen that the medially directed forks of the mesial moieties of the interclavicular sac have expanded and approach each other more closely in the interbronchial region. The cranially directed prongs have also lengthened and extend forward nearly parallel to the trachea.

In this figure the connection between the mesial moiety of the interclavicular and the anterior intermediate air-sac is clearly shown as well as the single orifice by which they open into the lung.

The lateral moiety of the interclavicular is relatively larger than in earlier stages but otherwise shows no marked change.

Between the twelfth and fifteenth days' occur relatively rapid expansions of the moieties of the interclavicular sac. The mesial moieties have fused with each other along the median line

Fig. 49 xAiiterior intermediate air-sac of the left lung of an embryo, nine and one-half days incubation. (A) View upon the surface that is in contact with the lung. Notable for showing the primordia of the recurrent bronchi springing from the anterior intermediate air-sac The mesial moiety of the interclavicular airsac is also shown. Ent. 3, opening into the third entobronchus; Bd., buds of recurrent bronchi;, mesial moiety of the anterior intermediate air-sac. (B) the same as seen from the cephalic end. Illustrates the connection between the anterior intermed ate and the mesial moiety of the interclavicular air-sacs, and also the forked extremity of the mesial moietv.

between the two lungs. They have apparently also united with the greatly expanded lateral moieties of the interclavicular (fig. 51). The dividing membranes remain for several days subsequent to the fusion of these different parts. The wall between the mesial moieties does not disappear until the first day after hatching. The septum between the mesial and lateral moieties is less persistent and, so far as dissections indicate, breaks down during the eighteenth day. In attempting to designate the time at which particular morphological changes occur one must, as previously indicated, take into account that individual variation is verj^ common in embryonic development.

The lateral moieties (fig. 51) have greatly expanded so as to unite in the median line. At this period they are the most prominent part of the interclavicular sac. The stalks connecting this portion_of the interclavicular with the first entobronchus are clearly indicated but the recurrent bronchi have not been shown. At the extreme antero-lateral margin of this division of the sac there is a narrow neck opening into the axillary sac.

Fig. 50 Ventral view of the lungs and air-sacs of a twelve day embryo.

The method of formation of the single interclavicular sac of the adult is now clearly foreshadowed. The four parts from which it is formed (two moieties from each lung) are in contact but still separated by partition walls.

The sixteenth day stage. The recurrent bronchi are now sufficiently advanced to observe the main features of their distribution. Figure 52 represents a partly diagrammatic camera tracing of a dorso-lateral view of the lung and shows the relations of the recurrent bronchi of the two posterior air-sacs at the close of the fifteenth day of incubation. The recurrent bronchi are represented black and the other air passages in stipple.

The distal tips of the longest recurrents of the abdominal airsac have anastomosed with the latero-ventral parabronchi of the first entobronchus. The more dorsal branches unite with parabronchi of laterobronchi. It is worthy of notice that the main stems of the first and second groups of recurrent bronchi of the abdominal sac have united so that the second group appears to be a branch of the first. By reference to figures 39 and 40 it will be seen that the two groups were originally separate. By limiting into a single trunk there is a single orifice (do.) opening from the abdominal sac into the recurrent bronchi.

Fig. 51 Latero-ventral view of the lungs and air-sacs of a fifteen day embryo. Figures 48, 49 and 50 should be compared to show the progressive development of the air-sacs and the way in which the four moieties of the interclavicular become united.

The recurrent bronchi of the posterior intermediate air-sac do not extend so far forward as do the branches of the preceding group. They occupy the extreme ventral part of the lung. Their anastomoses (not sketched) are principally with parabronchi of the first and second laterobronchus.

The recurrent bronchi of the two other air-sacs anastomose during the sixteenth day with parabronchi in parts of the lung adjacent to them. The distal ends of the recurrents from the interclavicular anastomose chiefly with the more ventral parabronchi of the first entobronchus and the recurrents of the anterior intermediate sac unite with parabronchi of the lateroventral part of the lung. It results that the anterior intermediate sac comes into communication with the air circuits in the latero-ventral lung region and the interclavicular sac comes into communication with passages in the anterior part of the lung.

As already pointed out, the anastomosing twigs are at first very slender, but, by the eighteenth day of incubation have increased in diameter so as to be practically the same size as the branches which they connect. The recurrent bronchi have by the eighteenth day of development assumed the relations to other parts of the bronchial tree which they bear in the adult lung.

Transition to the adult. In showing how the adult condition is reached it will be advantageous to summarize the principal changes subsequent to the eleventh day after which period the sacs grow more rapidly.

The abdominal sacs expand so as to fill the abdominal cavity, and partly surround the viscera therein contained. About the fourteenth day the walls of these sacs begin to fuse with the peritoneum and this fusion is apparently completed sometime before the eighteenth day of development. The left abdominal sac is somewhat larger than is the right.

The history of the posterior intermediate sacs after the eleventh day is closely parallel to that of the abdominals and does not require detailed description.

The same general course is followed by the anterior intermediate sacs. Their walls fuse with the lining of the thoracic cavity.

The cervical and interclavicular sacs attain their most rapid growth after the twelfth day of development. The cervical sacs grow forward toward the neck of the chick and between the fifteenth and nineteenth days of incubation their walls fuse to some degree with the pleura. They give rise to several subdivisions in the cervical and axillary regions.

The later stages of the interclavicular sacs require a more extended description than the others because of marked differences in their formation.

Returning to figure 47, the representation of the condition in the ten and one-half day embryo, we note again that the mesial moiety is bifurcated at its distal extremity. The more mesial lobe thus produced expands in such a manner that its walls come into contact with the walls of the corresponding lobe of the interclavicular sac of the opposite lung. This phase is reached on the fifteenth day of incubation (fig. 51). By the nineteenth day fusion of the walls has taken place, but there appears to be no breaking down of the septum thus formed. This appears also to be the case with the fused walls of the more anterior portion of the sac. This condition was demonstrated both by dissections and by Wood's metal casts of the adult lungs and air-sacs.

On the sixteenth day of development portions of the mesial moiety of both sides grow ventrally over the bronchus, and come into contact with the lateral moiety of the interclavicular sac. The membranous walls subsequently begin to fuse, and on the eighteenth day union is approximately completed. The single septum thus formed disappears sometime between the nineteenth day and the end of the first day after hatching, so that the two hitherto independent moieties coalesce to form one sac (fig. 53).

Thus the single large interclavicular sac of the adult is the result of the union of two moieties on each side which arise from different entobronchi. As diagrammatically illustrated in figure 53, the union of the sacs and the disappearance of the septum is completed by the close of the first day after hatching.

So far as we are aware a similar history of the formation of the interclavicular sac has not been given. It has been known since the time of Sappey ('47) that the single interclavicular sac of the adult was produced b}^ the union of two parts, but the formation of two moieties on each side from independent sources and the details of their union had not, we beheve, been anticipated.

Fig. 52 Diagram of the lateral surface of the right lung of a fifteen day embryo, to show the recurrent bronchi of the abdominal and of the posterior intermediate air-sacs. The outlines of the recurrent bronchi (in black) so far as represented were traced with the aid of the camera lucida from an air injected preparation. Dotted portions diagrammatic. O.abd., orifice of the abdominal sac; O.P.Int., orifice of the posterior intermediate; .4/(., anastomosis of recurrent bronchi. Other reference letters as before.

We turn now from the air-sacs to the recurrent bronchi, the embryonic history of which has been outlined from their earliest appearance to the time when they have established their union with other branches of the bronchial circuits.

Since the orifices of the recurrent bronchi are usually close to the direct opening into the air-sacs, attention should first be called to Campana's (75) analysis of orifices of the air-sacs: He divides them into two groups, the monobronchial and the polybronchial, according to the number of openings which they exhibit. The polybronchial orifices are further separated into two categories, the simple and the mixed polybronchials, the simple polybronchial being composed of several openings of one grade (parabronchi) , and the mixed polybronchial embracing openings of two grades, or, as in the case of the interclavicular and the anterior intermediate, uniting two neighboring sacs. Juillet accepts Campana's terminology but substitutes a clear basis of distinction for his confused account of polybronchials. This distinction consists in recognizing direct and recurrent orifices as the components of the polybronchials. A monobronchial orifice must necessarily be direct, but a polybronchial group may be composed of both direct and recurrent orifices (mixed polybronchial or of recurrent orifices only (simple polybronchial).

According to this analysis, which is in harmony with the developmental history, the cervical sac has a direct monobronchial orifice only, since it does not possess recurrent bronchi. A number of branches of the first entobronchus ramify posteriorly into the lung from a point nearly opposite the direct orifice of the cervical sac. These possibly serve the same purpose as the recurrent bronchi of the other air sacs, but do not appear to be developed from the sac itself as are the tubes which have been called recurrent bronchi.

The interclavicular air-sac is connected with the lung by two groups of orifices. The more mesial orifice, which is of the monobronchial direct type, opens into a short tube, the interclavicular canal, which also receives the direct orifice of the anterior intermediate sac. This short tube in turn communicates with the third entobronchus.

The more lateral group of interclavicular orifices is mixed polybronchial, having both a direct and several recurrent orifices. The direct orifice is the opening of the ventral tip of the lateral branch of the first entobronchus, from which as already described the lateral moiety of this sac has its origin. The recurrent orifices are three or four in number, and are the proximal openings of the recurrent bronchi. Reference to figure 47 will show that on the eleventh day of incubation there were but two recurrent openings connected with the sac. The change to the adult condition is brought about by the extension of the proximal ends of the original recurrent bronchial buds.

Juillet insists that there is no direct connection of the interclavicular with the first entobroncus, and accordingly, classifies this lateral group of orifices as simple polybronchial. We conclude, however, that the group is a mixed polybronchial and will return to the question under our general considerations.

The anterior intermediate air-sac also has two groups of orifices. The monobronchial direct orifice (figs. 47, 54) has already been mentioned in connection with the corresponding orifice of the interclavicular air sac. The other and more ventral group is of the polybronchial recurrent type. The number of orifices varies, but is usuall five or six.

The posterior intermediate sac communicates with the lung by a polybronchial group of orifices made up of both direct and recurrent tubes (polybronchial mixed). There is one direct orifice (figs. 53, 54), which is the opening of the third laterobronchus from which this sac has its origin. The recurrent orifices (figs. 53) represent the lungs of a one-day chick, but the relation of the orifices is the same as in the adult lung), three or four in number, as the openings of the recurrent bronchi and have a history very similar to that already described in connection with the two preceding sacs. The anterior ends of the posterior intermediate recurrent bronchi have for the most part anastomosed with the first and second laterobronchi.

The orifices of the abdominal air-sac are also of two kinds, direct and recurrent, which are so arranged as to form a mixed polybronchial group. The direct orifice (figs. 53 and 54) is the opening of the mesobronchus into the sac. The recurrent orifices arising as previously described are four or five in number. Schulze has shown that variations as to number exist in different birds being six to nine and sometimes reduced to one.

Figure 45 shows the surface aspects in the adult of the recurrent bronchi of the abdominal and posterior intermediate air-sacs to the bronchial tree and the way in which their stems connect with the air-sacs represented. In this metallic cast the abdominal air-sac was only partly injected so that the proximal end only is shown. It will be seen that the main recurrent bronchi of the abdominal air-sac extend more than one-third of the way

Fig. 53 Diagram of a ventral view of the lungs on the first day after hatching. The moieties of the interclavicular sac have united on each side and those of the right and left lung have come into contact, being separated only by a temporary partition wall. Shows also the nature of the orifices into the air-sacs. Cervical sac not represented.

toward the ventral anterior border of the lung before branching to any marked extend. The rami into which these recurrent bronchi finally break up anastomose with the numerous airpassages in the lateral facet of the lung.

Summary. Summarizing our observations we conclude that: 1. The recurrent bronchi are offshoots from the air-sacs leading into the lung parenchyraa, and the air-sacs in turn, except the abdominal (from the mesobronchus) , are the expanded terminal portions of secondary branches of the bronchial tree. Thus the recurrent bronchi sustain the same relation to the airsacs that the parabronchi do to the respective secondary branches from which they have their origin.

2. By means of the recurrent bronchi and their anastomoses with other branches of the bronchial circuits the air-sacs are brought into communication with all parts of the lung. They have direct communication with bronchus and central lung tube through their 'direct orifices' and a recurrent communication through the recurrent bronchi.

Fig. 54 Diagram of the ventral aspect of the adult lung constructed from studies of the prepared lung and from Wood's metal casts. Shows the nature of the seven orifices into the air-sacs as described in the text. DO., direct orifices, Rf'c.O.. orifices of recurrent bronchi.

3. The unpaired interclavicular air-sac of the adult fowl is the result of fusion of four embryonic outgrowths : two moieties from each lung which first unite and then undergo fusion across the median line to form the single interclavicular air-sac.

4. The Developiment of the Pulmoxary Artery

In describing the external appearance of the embryonic lung the pulmonary artery and pulmonar}^ vein were noted as a part of the surface view. We shall now give a more detailed account of the method of origin of the puhnonary blood vessels and of the embryonic changes that they undergo.

The pulmonary artery is formed by the union of two parts, one of which, the proximal end, sprouts from the sixth aortic arch, and the other, the distal end, begins in the lung wall and grows towards the sprout from the aortic arch.

The vascularization of the walls of the lung precedes the formation of the pulmonary artery and the distal extremity is the first formed. Examination of sections of the fifty- two hour stage shows the presence of rounded vascular spaces in the mesenchjmia of the lung primordium. When first formed these vascular spaces are of small extent and can seldom be traced through more than two sections, but the examination of numerous specimens of this age shows that they are fairly constant in appearance and as to their position in the median and dorsal portions of the lung parenchyma. These represent the rudimentary condition of the vascular area of the lungs.

As development proceeds, the vascular spaces assume greater definiteness, and by extension come together, and fuse forming an incipient network of capillary-like canals. Between the seventy-fifth and the eighty-second hour, in particular, these spaces show with increasing definiteness, and by the eighty-second hour of development the longer vascular spaces can be traced through twelve or more sections. These are intermingled with other spaces of less extent, all occupying the area of the lung in which, at a little later period, the pulmonary artery is formed. In the early formed vascular spaces it is not obvious which are destined to give rise to the artery and which to the pulmonary vein. This account agrees in essential particulars with Evans' observations of the development of blood vessels from capillary spaces.

These vascular changes in the mesenchyma of the lung wall begin before the formation of the sixth aortic arch. In many of our injected specimens tlie pulmonary vein takes the injection before the artery as shown in figure 6, part I. This injected specimen gives a view of the ]:)ulmonary veins as seen from the ventral aspect of the lung. A single well defined blood vessel passes on the ventral surface of each lung; these two unite into a trunk vessel situated in the median plane, and this, in turn, passes to the left atrium of the heart. Anteriorly is situated another vein that runs along the median line of the laryngo-tracheal groove and also unites with the trunk vessel that leads into the left atrium. In this specimen the pulmonary artery was not seen.

Fig. 55 Diagram of the dorso-lateral aspect of the adult lung. Exhibits openings into the mesobronchus of the dorsobronchi {Dor.) as seen when their stems are severed.

Fig. 56 Diagram of the mesial face of the adult lung to show parabronchi connecting ento- and ectobronchi.

There is considerable individual variation in the time of formation of the blood vessels, so that the precise time and the degree of development is not identical in corresponding specimens. Some of this obser^-ed variation may be owing to imperfect injection. Nevertheless, the method of formation of the pulmonary artery is sufficiently definite to leave little room for doubt. By the beginning of the fifth day there is a stem vessel in the lung wall and a short spur from the ventral end of the sixth aortic arch. These are directed towards each other but they are separated by a very obvious interval, they constitute the proximal and distal ends of the future pulmonary artery.

Sections of the 96-hour stage (fig. 58) show on each side a short spur from the ventral part of the sixth arch. About twelve hours later (4| days) we find in surface views (fig. 57) an almost completed pulmonary artery. There is, however, satisfactory evidence in the injected specimens thi :h.e spur from the sixth arch is not the only growing point in ii.e formation of the artery. On the contrary, it meets a forward growing vessel from the lung, which has been formed through the medium of the vascular spaces already described, and which precede its appearance. Fourteen injected specimens of the middle of the fifth day (4| days) were dissected. All showed the complete outline of the pulmonary artery, but in every specimen it was noticeable that the pulmonary artery was not of the same calibre throughout its course. Both ends were well developed, but about midway between the two ends the diameter was reduced, so that it presented the appearance of a slender tread. This is well shown in figure 57 which represents the dissection of an injected specimen of four and one-half days development. The distal division of the artery, from the sixth arch, is shorter than the proximal division from the lung. The slender thread-like portions shows the region of junction between the two ends. It would appear, therefore, that the first rudiment of the pulmonary artery begins in the mesenchyma of the lung walls in the form of vascular spaces, which by extension and union form a network of connecting passages, and from these arise the distal end of the pulmonary artery. The proximal division arises slightly later, springing from

Fig. 57 Dissection of the lung territory of an embryo incubated four and one-half days. Shows the pulmonary artery not yet completed in its middle course. Drawn bv G. H. A. Rech.

the sixth aortic arch, and then growing to meet the distal division from the lungs. When their union is effected the pulmonary artery is established. Figures 12 and 13, part I, show the surface appearance at five and one-half days after union of the two parts of the pulmonary artery.

Marshall ('92) was, we believe, the first to maintain that the "pulmonary arteries appear in the walls of the lung about the middle of the third day before the two hinder pairs of aortic arches are formed. On the appearance of the fifth (sixth !) pair of aortic arches the pulmonary arteries become connected with their ventral ends."

The spur from the sixth aortic arch arises before the arch is completed and at its first appearance it is on the ventral part of the arch near the truncus arteriosis. The sixth arch, in common with the others, is formed by a dorsal moiety from the dorsal aorta (fig. 5) , and a ventral moiety from the truncus arteriosus.

Fig. 58 Cross section of an embryo of the 96-hour stage to rt of tlie jiiihiionarv artery arising from the sixth aortic arch.

The ventral moiety is the longer and as it grows the relati\'e position of the arterial spur changes. At the 4^ day stage the position of the pulmonaiy arteiy is nearer the truncus arteriosus than the dorsal aorta. On the second half of the sixth day (fig. 12) it emerges at about the middle point of the sixth arch. The change in position is continued until, in later stages (fig. 22) the base of the pulmonary artery is nearer the dorsal aorta.

While the figures just described convey a good idea of the appearance of the pulmonary artery from surface views, the study of injected specimens as transparencies gives an idea of the internal distribution of vascular loops. Such a specimen of five days nine hours incubation is represented in figure 59 . This is the stage at which the first entobroiichus {Ent. I ) is given off and the internal changes are to go on rapidly, accordingly, we may expect, a good development of blood vessels. The artery enters the lung substance and passes dorsally as well as nearly parallel to the lung tube. Loops of blood vessels pass from the dorsal side around the lung tube and unite with the vein below. These capillary loops are more abundant near the bud of the first entobronchus and the expanded portion of the lung tube.

At five days, twenty hours, the pulmonary artery is seen (fig. 60) running nearly parallel to the course of the extra-pulmonary bronchus and entering the lung dorsal to the bronchus. The pulmonary vein runs through the ventral region below the central lung tube.

As shown in figure 60 A, a sketch from the ventral aspect, and figure 60 B, from a lateral view, the artery branches and divides into capillary networks around the entobronchi, and, more caudally, around the embryonic vestibulum from which the ectobronchi are soon to arise. The capillary network of the dorsal side, having surrounded the lung tube and its outgrowths, passes ventrally, and comes into communication with the capillary network of the pulmonary vein.

In the course of a few hours the branching of vessels within the lungs has obviously increased. Figure 61 A is the sketch of the left lung and 61 B of the right lung of an embryo incubated five days, twenty-two hours. In the left lung are represented the chief branches of the pulmonary vein and in the right lung both veins, arteries and capillaries are sketched, but the capillary network has been simplified. The pulmonary vein is split into two great divisions that form a fork over the bronchus (fig. 61 B, fig. 21). One arises from venules situated deep within the lung substance, dorsal to the bronchus, and is designated the internal branch, the other is the external branch. In examining figures 60 and 61 it is to be understood that the capillary network is more complex than shown in the sketches, at the same time, the network was sketched with the aid of a camera, and embraces those minute vessels that carried the injection and which could be readily made out.

Fig. 59 Transparency of the lung of an embryo of 5 days 9 hours incubation to illustrate capillary loops surrounding the meso])ronchus and connecting the pulmonary artery and the pulmonary vein.

Fig. 60 Lungs of an embryo incubated 5 days 20 hours to show the capillary network connecting pulmonary artery and vein. The four entobronchi have been established. The bronchus is occluded in its anterior portion. (A) dorsal aspect, (B) lateral aspect.

Fig;. 61 Transparency of the lungs of an embryo of 5 days 22 hours incubation. (A) illustrates the chief branches of the pulmonary vein of the left lung. (B) exhibits the pulmonary artery and the pulmonary vein of the right lung with parts of the capillary network connecting the two. Buds of ectobronohi are formed at this stage.

Fig. 62 Dissection of the lung territory of an embryo of 6| days incubation to show especially the capillary plexus connecting the pulmonary artery and the laryngo-tracheal vein. In other specimens a small vessel leaves the ventral wall of the pulmonary artery and breaks into a capillary network (figs. 12 and 14j . Shows also the connections of the pulmonary veins and the laryngo-tracheal veins with the trunk vessel leading into the left atrium of the heart.

Cross-sections of these stages were also studied under the microscope and in so far as the territory of distribution is concerned, bear out the observation on the injected specimens studied as transparencies.

The surface study of a dissected specimen of 6| days incubation (fig. 62) shows very well the connection between the pulmonary artery and the laryngo-tracheal vein. In part I, in a number of instances attention was called to a perpendicular branch (figs. 11, 12 and 14) emerging from the pulmonary artery upon its ventral border. Figure 62 shows that this short artery breaks into a network that is recombined into the vein running along the ventral border of the laryngo-tracheal region. This specimen was imperfectly injected so that the network of blood vessels on the anterior dorsal region of the lung did not show as in figure 14, but the connections of the arterial branch and of the laryngo-tracheal vein were well exhibited. The veins from the two sides join into a median vessel which, in turn, unites with the trunk vessel opening into the left atrium of the heart. The branches of the pulmonary vein also unite with this trunk.

On the eighth day of development, as indicated in part I (figs. 14 and 17), surface views of the injected lung show a capillary network occupying the antero-dorsal region of the lung, and, by the ten day stage the entire latero-dorsal surface is covered by a network of blood vessels. In addition to this there is a well defined denser network of capillaries upon the dorfeal surface. Figure 63 from a specimen of the ninth day, shows this denser area of capillaries from the dorsal aspect. In this figure the central portion of the dorsal region is occupied by a distinctly limited network of capillaries extending in the form of a longitudinal stripe from the cranial to the caudal part of the lung. This vascular development corresponds in position to the lane-like area (before mentioned) between the ends of the ento- and ectobronchi as they curve towards each other. It is a characteristic anatomical landmark of all later stages.

In this sketch an obhque view of the lateral face is exhibited and, on that surface, the capillary network is obviously more scattered than on the dorsal surface.

We shall now give attention to the transformations of the sixth aortic arch bj^ means of which the pulmonary artery becomes separated from the aorta so as to form an independent blood vessel coming from the right ventricle of the heart.

In the embryonic bird, after the sixth day, each pulmonary artery arises from one-half of the sixth arch. In the adult bud this has changed to the condition of right and left pulmonary arteries connected with a single tmnk issuing from the right ventricle. Not only has there been a complete separation of systemic and pulmonic circulation, but, also, the distal extremities of the sixth arch have atrophied. The way in which this is brought about may now be followed.

About the middle of the fifth day (4| day stage) the fourth, or systemic arch, the rudimentary fifth, and the sixth, or pulmonic arch are present. The fifth arch frequently fails to appear, and when it is present, it is extremely transitory. The disappearance of the rudimentary fifth leaves the fourth and sixth as the two posterior arches.

The left half of the fourth, or systemic, arch atrophies, the right half alone remaining, which becomes much enlarged.

In the meantime a septum develops that separates the right systemic from the base of the pulmonic, the systemic arch becoming connected with the left ventricle and the stem of the pulmonic with the right ventricle. When this has been accomplished the right and left halves of the sixth arch are still present and undiminished in size.

Figure 64 represents the condition at the close of the fourteenth day of incubation. The lung of the chick does not become functional as an organ of respiration until shortly before hatching. Accordingly, most of the blood from the right ventricle passes through both the left and the right divisions of the sixth arch to join the aorta with which these are connected. The pulmonary arteries springing from these divisions remain small (fig. 64). Near the heart the fourth and sixth arches are separated but the persistent right half of the fourth, and both right and left halves of the sixth arch, join the aorta. The fourth arch issues from the left ventricle, as the aortic arch, and the two halves of the sixth united into a oonunon ti'unk are connected witli the cavity of the right ventricle.

Fig. 63 Dorsal aspect of the lung of an embryo of the ninth day, showing the lane-like area of capillaries extending from the cranial to the caudal part of the lung.

Fig. 64 Sketch from an embryo at the close of the fourteenth day of incubation to show the way in which the persistent right half of the fourth aortic arch and the two halves of the sixth arch join the aorta. The pulmonary artery is small. Drawn bv G. H. A. Rech.

Ah hough the pulmonary arteries are relatively small, the right and left halves of the sixth arch are large, and, since they join the aorta, the principal function of the sixth arch at this time is in connection with the systemic rather than with the pulmonic circulation.

The pulmonary arteries remain relatively small up to the time of hatching, but those portions of the sixth arch lying behind them become constricted. This condition is represented on the nineteenth day of development in figure 65. At this time the pulmonary arteries are somewhat larger and the portions of the sixth arch behind them has undergone an obvious constriction. The parts of the sixth arch behind the pulmonary arteries are designated each ductus Botalli or ductus arteriosus. In the sketch the carotids and the pulmonics have been cut transversely so as to show in each case the cut ends of two vessels instead of single trunks into which they are imited nearer the heart.

The subsequent steps in the formation of the adult pulmonary arteries involve the disappearance of the ductus Botalli on each side. When respiration begins, the increase of blood flow^ through the lungs reacts on the growing tissue so that the pulmonary arteries become enlarged, and the ducti Botalli being deprived of blood rapidly diminish in size and soon become reduced to strands of connective tissue which usually disappear in the adult, although in some species of birds they are persistent but not functional.

The progress of affairs is represented in figure 66 sketched from a chick newly hatched. The pulmonary arteries have increased in size and the ducti Botalli are much reduced.

After hatching the ducti Botalli become occluded and reduced to slender cords of connective tissue. Figure ()7 represents the condition as seen from the right side, three days after hatching and figure 68 shows the heart and arteries of a young chick of the same age. In figure 68 the connections of the arterial trunks with the heart is exhibited. The puhnonary arteries are now hxrge and the ducti BotalU are atrophied.

Fig. 65 The arterial trunk.s on the nineteenth day of development. The sixth aortic arches are con.structed behind the ])uhnonarv arteries into the ducti Botalli. Drawn by G. H. A. Rech.

Fig. 66 Condition of the pulmonary artery and of the ductus Botalli of the newly hatched fowl. Drawn I)y G. H. A. Rech.

Fig. 67 The atrophied ductus Botalli and the enlarged pulmonary artery on each side, on the third day after liatching. Drawn by G. H. A. Rech.

Fig. 68 The heart and the arterial trunks on the third day after hatching. The ductus Botalli of each side is reduced to a slender cord and the pulmonary arteries have attained the diameter of the sixth arch of which they are continuations. Drawn by G. H. A. Rech.

The effect of the obhteration of the ducti BotaUi is that the blood from the right ventricle can no longer pass through the sixth arch to the aorta but is sent entirely through the pulmonary arteries to the lungs.


The morphology of the avian lung can be made clear only by observations of its development. It is through this channel alone that one becomes acquainted with the nature of the modifications of the bird's lung that place it in a class by itself. It can be safely said that the facts of morphology separate the avian lung from the lungs of all vertebrates, with the possible exception of the reptiles. The excellent papers of Milani ('94) and of Hesser ('05) on the embryology of the reptilian lung are classics, but the embryology of the air-sacs is insufficiently known. On account of the development of air-sacs, of recurrent bronchi and labyrinthine connections between all air passages, the avian lung exhibits a special architecture and upon our understanding of this architecture will depend our conception of its physiology. While we have described what we conceive to be its physiological anatomy, we have not engaged in experiments that entitle us to make any special comment on its physiology.

The steps in arriving at a conception of the bird's lung have been gradual and dependent upon increasing definiteness in the knowledge of its internal architecture. Since the observations of the early investigators have been a factor in molding this conception, and since ideas of lung anatomy have been so dominated by their results, they may be briefly summarized. Moreover, the sketches of Selenka ('66) are still used in text-books to illustrate the development of air-sacs (vide Lillie, Development of the Chick, '08) Hertwig-Kingsley, Manual of Zoology, Revised Edition, '12), accordingly a summary will not deal with obsolete matters.

The traditional view, that somehow the bird's king should be swung into line with the others, and ought to be compared part by part with the mammalian lung, persisted for a long time and created difficulties of interpretation. The idea that there are culs-de-sac on the ultimate twigs of the bronchioles, corresponding to the alveoli of the mammalian lung, has so often been tacitly assumed in the descriptions of the anatomy of the bird's lung that confusion has resulted. The conception, so fundamentally different from this, of labyrinthine passages, all intercomnmnicating, and forming bronchial circuits instead of a bronchial tree, has been a matter of gradual growth.

Inasmuch as the pioneer observers examined the bird's lung with great care, by transmitted as well as by reflected light, it is pertinent to inquire to what extent the structure of the bronchial tree was anticipated.

Rathke's ('28) figures of the embryonic lung of the chick show an attempt to represent the internal anatomy of the lung. In his figure 15 of the seven day stage, the main bronchus is shown with hernia-like growths (entobronchi) coming from it. In one of his five figures of the eleventh day (his fig. 16) he shows the air-sacs and a more profuse branching of the bronchial tree. In his figures 11 and 21 he sketches details of the terminal twigs which he illustrates as ending in grape-like clusters. These he compares directly with the alveoli of the sheep's lung of which he gives a similar picture.

Von Baer ('28) gives no picture of the embryonic lung but his descriptions show that his observations were carefully made. While Rathke's are tinctured with a subjective bias, Von Baer's are objective.

The next figures of importance for our review are those of Remak ('55). He was an excellent observer and his sketches are of high quahty. His illustrations show clearly two entobronchial buds on the fourth day of development (his fig. 78). This shows well the mesenchymic sheath and the endodermal tube. His pictures of the lung at 3^^ days (fig. 72), at the end of the fourth day (fig. 74), and on the fifth day (fig. 75), show two entobronchial buds. His sketch of the early sixth day (fig. 88) shows tln-ee sucli buds uiul of the seventh day (fi^- 71)) shows four. Tliese figures are evidently not drawn wdth the camera since altliough the niunber represented is correct, the buds are too widely separated and cover too much territory of the centi-al lung tube. The sketch of the condition on the eighth or ninth day (fig. 80) shows both ento- and ectobronchi as well as the expanded end of the mesobronchus. It should be said that Remak's figures represent the essential features of the anatomy of the embryonic lung. They are somewhat out of proportion and they show the great difficulty of study by transmitted light without the aid of some especial method of injection.

Selenka's studies ('6(3) of the development of the air-sacs of the chick added a number of points to the anatomy of the avian lung. His figure of the 3| day stage shows the occluded bronchus (fig. 2) . In the fifth day stage he illustrates for the first time, the beginning of the embryonic vestibulum (his fig. 3) . In his sketch of the sixth da}" stage he represents the bud of the first entobronchus, not quite in position, how^ever, in reference to the expansion of the lung tube, being in his figure posterior instead of anterior to the expanded part. His sketch of the condition on the seventh day (his fig. 5) shows seven or eight outgrowths (buds of ento- and ectobronchi) of the central lung tube.

His figure of the lungs and air-sacs of the eleven day embryo is very interesting and, as already stated, has been extensively copied in text-books. On the right lung is sketched (2') the sac that w^e have designated the lateral moiety of the interclavicular sac and w^hich he designates cellula infra laryngeus, on the left, not yet united" — stetz sich spater in die cellula axillaris fort." Although this figure needs attention, and some correction, it is for the methods at his command a good figure. This figure also show^s on the right lung the mesial moiety of the interclavicular sac, but it is represented on the wrong side of the bronchus. As shown in our figures 21 and 47 it arises on the mesial side and extends across the bronchus ventrally to the lateral side.

The sketches of Selenka and of Remak, made by talented observers show the limitations of observing the internal structures of the lung by transmitted light without the help of injections.

The reconstruction method has the advantage of giving relatively large models, but it is difficult and protracted. Injection with air, described under 'technique,' is simpler, it can be repeated indefinitely with the same specimen and gives clear pictures of the minuter details.

The researches of Sappey ('47) laid the foundation for those of Campana ('75) which, in particular, mark the next advance in our knowledge of the bronchial tree. These investigations were carried out on the adult lung and resulted in accurate figures and extended descriptions. The quahty of Campana's work has been spoken of before, but too great emphasis can not be laid on the thoroughness of his anatomical analysis. It is now fifty years in the past and on that account, coupled with the fact that his memoir is not easily obtainable, it is hkely to be slighted. The memoir is complete and critical for the adult stage embracing the intra- and extrapulmonary features, the bronchial tree, the air-sacs, their orifices and the bronchial circuits. Campana was apparently the first to fully grasp the idea of bronchial circuits. The earlier observers referred to, indicated the beginning of bronchial branches but their conception was apparently that of a true bronchial tree comparable to that of mammals. Schulze ('71), in giving a picture of the histology of the bird lung showing among other features the air-capillaries evidently interprets them more as alveoli than as a network of connecting passages.

Fischer ('05) studied the bronchial tree by injections and published many figures of wax casts. His descriptions are terse, more general than critical and are somewhat burdened with a new terminology.

It is through the investigations of Schulze (11) and Juillet ('12) that we arrive finally at our present conception of the architecture of the avian lung. Their discovery of the recurrent bronchi has been sufficiently commented upon in previous pages. Juillet's investigations introduced some innovations besides recurrent bronchi, as sketches of the embryonic tree of six and eight day stages. He was also the first to show the method of development of the recurrent bronchi, and after Schulze, to recognize their significance.

Some particulars in which our results differ from those of previous observers may now be mentioned.

Co77ipariso)i of enibryonic stages. On account of the method employed, of air injection, we were able to carry our studies of the embi-yonic bronchial tree to later stages of development than those previously sketched. One who compares our figures of the embr}' onic tree with those of Juillet will note several discrepancies. The development of the bronchial tree in his reconstruction of the six day stage (his fig. 4) is more advanced than in our sketch of five day twenty hours which is well along in the last half of the sixth day. His reconstruction of the bronchial tree of the eighth day (his fig. 5) is also in advance of our sketches of the same structure in the early part of the ninth day. There is substantial agreement as to the number of main branches but differences in detail including one of importance, viz., the relation of the transverse branch of the first entobronchus to the lateral moiety of the subbronchial sac.

It is also to be noted that Juillet omits the laterobronchi in his reconstruction of the eight day stage. His plastic reconstruction of that stage embraces, besides the mesobronchus, only entoand ecto-bronchi. In his text, as well as in his sketches, he gives little consideration to the laterobronchi, and sets to one side the dorsobronchi. He states clearly his reasons for so doing. Nevertheless, after observing them carefully in embryonic stages as well as in the metalic casts of the adult lung, we are inclined to attach considerable importance to the dorsobronchi, and also to the laterobronchi, on account of the part they play in helping form the network of the bronchial circuits. As Campana pointed out, the dorsobronchi (approximately twenty-five in number) form a fine network in the middle of the dorsal face of the lung that can be detected by surface studied of untreated specimens. The laterobronchi, besides giving rise to an air-sac, form many anastomoses through their branches in the ventral part of the lateral ahd caudal regions of the lungs and also with the recurrent bronchi of the two posterior air-sacs.

The interclavicular air-sac. It is on the question of the embryonic development of the interclavicular sac that our observations are more at variance with previous results than on any other point. The method of development of this sac is very remarkable. In late embryonic stage, as in the adult, it is an unpaired medial sac but it arises from four separate moieties, two from each lung. The lateral moiety springing from the transverse branch of the first entobronchus and the mesial moiety coming (with the exception noted above) from the third entobronchus.

The chief anticipation of the simultaneous existence of lateral and mesial moieties of this sac is found in Selenka's sketch of two separate sacs on the right lung (see reproduction of the sketch in figure 191 of Lilhe's development of the chick. He says that the sac which we have designated the mesial moiety later unites with the cellula axillaris. Only one moiety of the interclavicular (the lateral moiety) is sketched on the opposite side. As indicated above his sketch of the mesial moiety shows its origin on the wrong side of the bronchus.

On account of its position on the lung, the lateral moiety is the one that has usually been sketched in the published drawings of embryonic stages of the lung and the mesial moiety has commonly escaped notice. However, when the moieties have united, as in late embryonic stages and after hatching, the more obvious opening of the interclavicular, which is the mesial, has been correctly identified and that part of the sac that is derived from the lateral moieties has been regarded merely as an extension of the mesial moieties. Thus Juillet's diagram of the lung of the embryonic chick represents only the mesial moiety and this as expanded and bearing recurrent bronchi on its lateral border. It is only by following the embryonic development from the eleventh to the sixteenth days that the complex relations of this sac are cleared up.

Guido Fischer ('05) maintains that the lateral branch of the first entobronchus of the adult opens into the interclavicular sac. He gives a figure of a plastic cast to show this but does not name the bird in which it is found. While Campana does not mention it, his figure 11 is suggestive in showing the termination of the branch in question close to the lateral orifices of the interclavicular sac.

Juillet ('12) is very drastic in his criticism of several of Fischer's observations and of this one in particular he says: G. Fischer ('05) a donne des bronches diaphragmatiques une discrij)tion assez confuse et a laquelle il y'a plusieurs reproches a faire . . . . Le sac interclaviculaire s'ouvre d'apres lui sur ce ranieau" (lateral or transverse branch) bronchique: I'orifice qu'il signale ici est tres certainement I'orifice recurrent de ce sac dont il a nial saisi les rapports exacts," etc.

Howe\'^er defective Fischer's observations may be on other structural matters (as Juillet claims), on this point, in particular, our observations indicate that Fischer is probably correct. At SLuy rate, we \vd\e found the orifice in question in the embryo chick and also in the adult. In our preparations there are several that show both direct orifices, the lateral and the medial, of the interclavicular sac as in the Wood's metal cast of which figure 45 is a photograph. Moreover, the existence of a separate lateral moiety implies, at least in the embryo, a direct opening from that moiety into the lung. In this criticism Juillet overlooks the fact that the direct connection between the curvilinear branch of the first entobronchus and the interclavicular sac has been indicated by a number of observers, as Huxley ('82), Baer ('96), Lillie ('08), Schulze CIO). Accordingly, the claim of Fischer was neither novel or unique. A further claim of Fischer, as Juillet points out in the same paragraph, is that the curvilinear branch of the first entobronchus has also a direct opening into the anterior intermediate sac. On this point of the criticism our observations lead us to agree with Juillet that such an orifice is lacking.

Juillet's Schema (fig. X, p. 313), to show the relations of the air-sacs and their recurrent bronchi with the ventral face of the right lung of a chick embryo of the tenth day is faulty in showing the interclavicular sac with a wide lateral extension crossing the lung transversely and giving rise to recurrent bronchi. The interclavicular sac at this stage of development (and for several days thereafter) has separate lateral and mesial moieties as shown in figures 47 and 49. The recurrent bronchi of the interclavicular sac sprout from the lateral moiety, while, so far as we have been able to determine, the mesial moiety never has any.

Excepting the analysis of Campana and of Juillet, there is much confusion among authors regarding the orifices of the airsacs. In the chick we find seven groups of orifices, agreeing with Juillet except in regard to the nature of the lateral orifice of the interclavicular sac. This we find to be mixed polybronchial instead of simple polybronchial as claimed by Juillet. On the basis of our observations the seven groups of orifices are : one direct monobronchial orifice for the cervical sac; one medial direct monobronchial, and one, laterally placed, mixed polybronchial for the interclavicular sac, one direct monobronchial and one simple i^olybronchial for the anterior intermediate sac ; one mixed polybronchial for the posterior intermediate and one mixed polybronchial for the abdominal sac.

As Juillet ('12) has shown in admirable comparative studies, much variation exists as to numbers (6 to 9) and arrangement of orifices in the twenty-five species of birds which he studied. Since our observations are limited to the chick, the reader is referred to Juillet 's analysis of the different types of orifices (pp. 340-351) which can not be satisfactorily abbreviated.

As regards the method of growth and the type of branching within the lungs, we shall limit ourselves to the brief remarks — that the excellent observations of jMoser indicate the general method of growth and on the ciuestion of branching by monopodial or dichotomous formation, our observations incline us to adopt the view of an unequal dichotomy.

Recurrent hronchi. The recurrent bronchi are the most important recently recognized structures connected with the lungs of birds. As already indicated the credit for the recognition of their structure, development and physiological function is shared by Schulze ('11) and Juillet ('12). These new structures are of especial interest. There is no doubt that they spring from the air-sacs and grow into the lungs where they establish numerous connections with the bronchial branches. This gives a new view of air sacs: They are expanded parts of the bronchial circuits; branches from the main bronchus lead into them, but they are not terminal sacs, they are air reservoirs on the course of the bronchial circuits. Conduits de\'eloped from tliem turn back into the lung and join the network of air passages, so that, the air, httle changed, and warmed to body temperature, is carried back into the hmg for aeration of the blood. The lung, although relatively small, is highl}^ vascular and a very efficient organ of respiration. Rapid respiratory changes are favored by the structures described and by the very intimate relations between air capillaries and blood capillaries. Taken together they constitute a feltwork of vascular and air capillaries mingled together.

It is clear from Campana's text that he noticed the recurrent bronchi of the adult on the four air-sacs from which they have their origin. He makes comment upon them in each case. His reference to those of the abdominal sac shows that he thought of them as combinations of parabronchi. On page 54 of his memoir he says: "On voit a la face dorsale du poumon des grosses tertiaries, on pourrait presque dire des secondaires reconstituees par la reunion des tertiaries plus fines, aboutir sur les parois du septieme infundibulum (fig. 13, C) ou, ce qui revient au meme, s'ouvrir dans la termination des dernieres secondaires externes."

On the whole, Campana's observations afford a sort of prophetic anticipation of the full recognition of recurrent bronchi.

The discovery of the recurrent bronchi brings a new point of interest into the study of the lungs of Sauropsida, and it is much to be desired that extensive comparative studies may be entered into that will embrace a careful consideration of the air-sacs and their relations in reptiles. 2 The variations in chronology of chick embryos represented in tlie illustrations of the standard references is so great that an additional comment is appropriate. Comparison of the figures of Duval and of Keibel and Abraham shows variations sometimes exceeding twenty-four hours (cf. Duval, fig. 142, 140 hrs.; and Keibel and Abraham, fig. 27, 114| hrs.). While it would be a satisfaction to embryologists to have the chronology standardized, the essential point is a correct analysis of anatomical conditions and the sequence of events.

Literature Cited

In order to limit as far as practicable the bibliographical references to small compass, only those are listed that were of especial service in the preparation of the paper. The icadily accessihle pajiers of Flint, Fischer, Moser and Juillet contain more coniijrelicusive lists whicli makes unnecessary the repetition by title of' the other articles consulted, and referred to in our Comments on the Literature.

Campax.\ LS75 Physiologic de la respiration cliez les Oiseaux. Anatomie de

raj^pareil pneumatique i)ulmonaire, etc., chez le Poulct. Masson,

Paris. Fischer, Guido 190.5 \'ergleichend-aiiatomische Untersuchungen iiljer der

Bronchialljaum der Vcigel. Zoologica, lid. 1<).

Flint. J. M. 1906 The development of the lungs. Am. .Tour. Anat., vol. 6. HrxLKY. Thos. H. 1882 On the respiratory organs of Apteryx. Proceed. Zool. Soc. Lond.

JriLLKT, M. A. 1911 (aj Rapj)orts des sacs aeriens ct des bronches chez les

Oiseaux; (b) Observations comparatives sur les rapports du poumon et des sacs aeriens chez les oiseaux. C. 11. Acad. Sci. Paris, T. 152.

(c) Phases avancees du developpement du poumon chez e Poulet.

C\ R. Soc. Biol., T. 70. (d) Face ventrale du poumon des oiseaux et diaphragme. Ibid.. T. 71.

1912 Recherches Anatoiuiques, Embryologiques, Histologicjues et

Comparatives sur le Poumon des Oiseaux. Archives de Zool.

Experiment, et Gen. T. 9, pp. 207-371. Lakski.l, Olof 1914 The development of recurrent Ijionclii and of air-sacs of

the lung of the chick. Anat. Anz., Hd. 47. Miller. W. S. 1893 The structure of the lung. .Jour. Morph. vol. 8. Moser. Fanny 1902 Beitriige zur A'ergleichenden Entwicklungsgeschichte der

Wirl)eJtierlunge. Arcliiv. fiir Mikros. Anat. Bd. 60. Sapfey, p. C. 1847 Recherches sur rai)])ar(>il respiratoire des Oiseaux. Ger mer-Bailli<"Tc, Paris. ScHULZE F. E. 1872 The lungs in Strieker's Manual of Histology.

1908 Die Lungen der African Strausses. Sitzmigsber. d. Kgl. Preuss. Akad. Wiss.

1909 ('her die Functionen der Luftsa,cke bei den Vogeln. First mention of recuii-ent bronchi. SitzungslxM'. d. Kgl. Preuss. Akad. Wiss. 6 Mai.

1910 ("her die Bronclii saccales und den Mechanisms der Atmung l)ei den Vogeln. Ibid. 2 .Tuni.

1911 Uber die Luftsiicke der \'ogel. Verhandl. d. \TII Internat. Zool. -Kong, zu Graz. Aug. 1910.

Selexka, E. 1866 Beitrag Zur Entwickelungsgeschichte der Luftsiicke des

Huhns, Zeitsch. fiir wissenschft. Zool. Bd. F. 16. ZuMSTEiN, J. 1900 liber den Bronchialbauiii der Sanger und Vogel. Sitzungsber.

Ges. Z. Beford. d. Ges. Naturw iss. s. .39-48.

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