Paper - The development of the cloaca in birds (1922)

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Boyden EA. The development of the cloaca in birds, with special reference to the origin of the bursa of Fabricius, the formation of a urodaeal sinus, and the regular occurrence of a cloacal fenestra. (1922) Amer. J Anat. 30: 163.

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The Development of the Cloaca In Birds, with Special Reference to the Origin of the Bursa Of Fabricius, the Formation of a Urodaeal Sinus, and the Regular Occurrence of a Cloacae Fenestra

Edward A. Boyden

Department of Anatomy, Harvard Medical School

Forty-One Figures

The cloaca of the domestic fowl has been an object of interest to anatomists since early in the seventeenth century. It was discovered by Hieronymus Fabricius while investigating the urogenital apparatus of birds in connection with his pioneer study of the chick embryo. In his posthumous treatise, entitled De Formatione Ovi et PulU," Patavii, 1621, he describes as follows a blind sac lying behind the uterus of the fowl, but emptying into the cloaca close to its external orifice:

A third thing to be noted in the anus is a duplex vesicle,* which in its deepest part rises up to the os pubis, and is seen clearly and further back as soon as the uterus, already described, offers itself to view. Since the vesicle is pervious to the extent that a passage opens below from the anus to the uterus itself and from the uterus into the vesicle, as it were superiorly, the vesicle being closed at the other end, we have come to the belief that this is the place into which the cock injects his semen, and forces it in so that it is kept there.

1 The meaning of duplex in this passage is doubtful. The organ itself is never double. But in two species, a nestling raven (Osawa, '11) and the jay (Jolly, '15), it has been reported as bilobate. Osawa suggests that perhaps Fabricius may have had such a case before him when writing his description, but apparently Fabricius dealt only with the fowl, a species in which a bilobed condition has never been reported. The bursa is, however, two-walled, consisting of a mucous membrane and a muscular layer; and the recognized use of duplex to mean stout or thick, as applied to garments, may have been in the mind of Fabricius when he used this term. Unfortunately, its form is not recognizable in the woodcut in which he intended to show it.

This idea of a receptaciihim seminis was discussed at length by his student Harvey, and by de Graaf, the latter publishing the first picture of the bursa. Both denied the function ascribed to it by its discoverer on the ground that it was equally well developed in both sexes. Beginning with the middle of the nineteenth century, it was subjected to microscopic examination and thereafter repeatedly studied, one group of investigators (Leydig and his successors) holding that it was purely a lymphoid organ; another group (Stieda and his school) maintaining, on embryological grounds, that it was primarily a glandular organ. Following Kolliker's description vof the epithelial origin of the thjnnus, in 1879, these views were partially reconciled, but gave rise to a new discussion as to whether the epithelial primordium is replaced by invading tissue or whether it is itself transformed into a reticulurn containing lymphocytes. Most authors since Wenckebach ('88) have held that the epithelium undergoes transformation without invasion. Recently Jolly ('15), in an elaborate summary of five years' work on the histogenesis, haematopoietic activity, and involution of the bursa of Fabricius, has advanced the theory that "the bursa represents an ancestral glandular organ, a cloacal caecum undergoing regression, which has become invaded by lymphocytes like other retrograding diverticula (the vermiform process of mammals and the intestinal caeca of birds), but in which, in view of a new function, a particular adaptation has taken place between the (persisting) epithelial tissue and the (invading) mesodermal, lymphoid tissue." In recognition of this sjonbiotic relation. Jolly would define both thymus and bursa as lympho-epithelial organs. Up to the present time, however, one must acknowledge that all attempts to analyze the function of the bursa or to find its counterpart in the hind-gut of other vertebrates have met with only partial success.

Modern investigation of the cloaca may be said to have begun with the embryological studies of Gasser ('73-'80) and of Wenckebach ('88), who reestablished the view of Bornhaupt ('67) regarding the entoclermal origin of the bursa. Since then only one paper has added any substantial increment to our knowledge of the general development of the avian cloaca, that of Pomayer ('02), in the Fleischmann series, dealing especially with the development of the phallus.

The present study originated with the discovery of a temporary foramen in the dorsal wall of the cloaca, produced by the disintegration of a definitely localized patch of epithelium and its subsequent removal by phagocytes, following which the contents of the cloaca are left in contact with the mesenchyma for a period of nearly twenty-four hours of incubation. This curious phenomenon was observed in over thirty embryos of the Harvard Collection, and its failure to occur has not been recorded in anv embryos incubated approximately three days, the period at which the fenestra reaches its maximum size. My attention was first attracted to it by the presence of large numbers of embryonic phagocytes^ similar to those found in the vestigial gill-filaments of chick embryos of corresponding age (Boyden, '18). Further study then demonstrated that this peculiar foramen was constant in its mode of development and invariably occurs, not only in chick embryos where it was first found, but in duck and pheasant embryos as well. It is of special interest not merely because it furnishes the only instance in the differentiation of a hollow organ, so far as I am aware, in which a gap occurs in the epithelial wall as a normal and constant feature of development, but also because it enables us, by virtue of the landmarks it establishes, to determine for the first time the exact point of origin of the bursa of Fabricius.

'^ These cells were first described as degeneration cysts, but they were subsequently seen in the underlying tissues into which they had been extruded from the epithelium, and were then recognized as embryonic phagocytes. It is a debated question whether these should be classed with the wandering cells of later embryonic stages and thus derived from the mesenchyma in general (the macrophages, clasmatocytes, etc., of numerous authors), or should be considered to have arisen in situ as reactions of the local mesenchyma, or even of the epithelium itself, to the presence of dead protein. This problem will be discussed in another paper in connection with the appearance of phagocytes in the anal plate at so early a period as forty-eight hours of incubation.

In following the origin and fate of this particular foramen, to which I have applied the name cloacal fenestra, it became necessary to review the entire chain of events in the development of the cloaca from the formation of the primitive streak to the period of histological differentiation, and to supplement a quantitative study of chick embryos with observations on other species, notably duck, pheasant, gull, and tern embryos. As a result of this study a number of other interesting facts have come to light. Those relating to the early development of the hind-gut and tail have been reserved for a subsequent publication.

Development of the Cloacal Fenestra

In describing the origin of this foramen it will be necessary to refer occasionally to a peculiar tissue in the sacrocaudal region of young chick, pheasant, and duck embryos, which up to this time has not been observed in other birds or vertebrates. I refer to an indifferent cell-mass in the proximal end of the tail which persists long after the adjacent region has been differentiated — as late as the beginning of the fourth day of incubation in chick embryos. As seen in figure 5 {ps. v.), this inert mass lies within the angle formed by the cloaca and the caudal intestine, to both of which structures it is fused in a sagittal plane. Laterally it passes over into the mesenchyma of the tail, but rather abruptly, so that its limits can be approximately defined and the whole mass modeled in relation to surrounding structures, as displayed in figure 13. Beginning at the proximal end of the tail, this tissue is seen to be directly fused with the wall of the cloaca in the territory included between the anal plate and the junction of the caudal intestine with the cloaca (this being the wall of the cloaca which will later give rise to the bursa of Fabricius). Dorsally, this tissue is fused with the ventral border of the caudal intestine, and so intimately that the latter never has a chance to differentiate into an epithelium before it is resorbed. Ventrally, it fuses with the ectoderm bordering the anal sinus, while caudally it merges with the tail-bud mass — a fusion of three germ-layers extending across the tip of the tail. Thus the core of the tail is composed of an indifferent cell-mass, the whole of which can now be defined as representing a persistence of the primitive streak in the form of a primitive-knot mass.^ From the cloaca to the tip of the tail it forms a deeply staining homogeneous mass differentiating above and below into epithelial structures and on the sides into the mesenchyma of the tail. The portion occupying the distal end of the tail is an active tissue giving rise to the medullary tube, caudal intestine, notochord, and other caudal tissues. The proximal half, on the other hand, is degenerating. Some of it may contribute to the mesenchyma of the tail, but most of it, as indicated by the presence of innumerable phagocytes gorged with pycnotic nuclei, is undergoing resorption. This latter portion, representing an excess tissue, is absent from saurians and mammals, the caudal intestine in these forms lying close to the inner curvature of the tail. In this respect the cloaca of the tern (fig. 1) resembles that of lizards and snakes more than it does that of the gallinaceous birds.

GRAPHIC RECONSTRUCTIONS ILLUSTRATING INITIAL STAGES IN THE FORMATION OP THE CLOACAL FENESTRA

(Dotted lines and arabic numerals refer to somites; dash lines, to cavities of the cloaca; crosses, to the primitive-streak mass; periods, to scattered phagocytes; cross-hatching, to concentrated areas of disintegration on left side of embryo.)

Fig. 1 Tern embryo (Sterna hirundo) H.E.C. 2167: 5.5 mm. X 42. all., allantois; an. -pi., cloacal membrane; c. i., caudal intestine; reel., rectum;!^. D., wolffian duct.

Fig. 2 Duck embryo (Anas domestica) H.E.C. 2193: 3 days, 21 hours. X 42. t. p., terminal portion of W. D.; y and z, primary and secondary foci of disintegration (z restricted to right side of embryo in this stage).

Fig. 3 Turtle embryo (Chrysemys marginata) H.E.C. 1067: 6 mm. X 42. after R. F. Shaner. an. s., primordium of anal sacs (cf. div. c. of chick embryo in plate 3) ; x, point of rupture of caudal intestine.

Fig. 4 Duck embryo (Anas domestica) H.E.C. 2194: 3 days, 21 hours. X 42. ps. v., ventral half of primitive-streak remnant; x, occluded segment of caudal intestine.

Fig. 5 Chick embryo (Callus domesticus) H.E.C. 2071: 3 days, 18 hours. X 42. (Compare with model of same embryo, fig. 13.) m, marginal sulcus separating thin-walled roof from thick-walled sides of cloaca.

A second process which must be considered in relation to the formation of the cloacal fenestra is the disintegration of the caudal intestine. ■* In all reptiles and mammals that I have examined and in one species of bird embryos (Sterna hirundo, the common tern) the caudal intestine undergoes reduction in the following manner. It appears to be pulled out, as if by the elongation of the tail, so that it tapers uniformly from the newly formed dilated portion at the tip of the tail to a slender tube at the oldest portion — the region adjacent to the cloaca. As the latter por ^ The details of the process by means of which the primitive streak is segregated in the tail of the embryo will be described in a subsequent paper. At this time it is sufficient to state that the area described above is derived from that portion of the primitive streak which is included between the rhomboidal sinus and the anal plate of a fifteen-somite embryo. In consequence of the folding of the blastoderm, and of the accompanying overgrowth of the tail, the dorsal portion of the primitive streak, lying under the ectoderm, is folded into the outer curvature which forms the tip of the tail and thus becomes the tail-bud mass. The ventral half, lying above the entoderm, and therefore on the inner curvature of the fold, is tucked under the tail and compressed into the angle between the anal plate and the caudal intestine.

This term of Koelliker's seems more appropriate than 'post-anal gut' introduced by Balfour, since the gut-tract of the tail is an outgrowth of an area which originally lies anterior to the anal plate. As applied to mammals, the term is still less appropriate, as the caudal intestine disappears long before the anus is formed.

tion becomes more slender the lumen becomes occluded and the solid strand thus formed soon after ruptures (fig. 3, x). At least some of the cells disintegrate and are removed by phagocytes, but pycnotic nuclei are inconspicuous here as compared with the abundance of necrotic cells to be found in the degenerating caudal intestine of the chick. This process, which begins at the cloacal end of the gut, progresses slowly in a craniocaudal direction until the entire caudal intestine disappears. In duck, pheasant, and chick embryos, however, the reduction of the caudal intestine is greatly complicated by the disintegrating process going on in the primitive-streak mass, as referred to above, and by the disintegration of the adjacent cloacal wall, the latter process resulting in the formation of the cloacal fenestra.

The developmental history of this foramen, which is thus intimately associated with the removal of the caudal intestine, is divided into two phases, a period of active disintegration, beginning at about the 41-somite stage (chick embryo, 2 days, 18 hours), and lasting approximately twelve hours, and a period of closure, beginning somehere near the 50-somite stage (7-mm. embryos, of approximately 3 1/3 days), and ending in embryos of about 9 mm., incubated 3 days and 18 hours. Expressed in terms of embryonic growth, the first trace of the process appears just before the wolffian ducts fuse to the cloaca. The final stage in closure occurs about the time the ultimate somite is formed (I have found as many as fifty-three) ; that is, before the resorption of caudal somites begins.

The initial phase, as illustrated by the first text plate (figs. 1 to 5), is based upon two embryos. In consequence of the great rapidity with which the degenerative process is initiated, a far greater number of specimens of the same age than were available would have had to have been sectioned in order to have provided more than the two stages referred to. For there is not the slightest indication of the process in an embryo only one somite younger than the one shown in figure 5, where the entire area of the cloacal wall which is to be denuded has already begun to degenerate.

The first indication of impending disintegration appears in a duck embryo of forty-five somites (fig. 2). Two paired foci of degeneration {y and z) are here disclosed in the cloacal wall, one near the junction of the caudal intestine and cloaca, the other just anterior to the orifice of the wolffian duct. It is probable that area y is the first to develop as it is present on both sides of the cloaca, while area z is present only on the left side. This specimen, if corroborated by more examples, would seem to indicate that the degenerative process, which later involves the caudal intestine, begins in the wall of the cloaca near its junction with that structure. •

In the next stage (fig. 4, of a duck embryo two somites older), the two areas on each side have grown together, presenting a continuous line of degeneration. In addition the lumen of the caudal intestine has become occluded (fig. 4, x), in the region which corresponds to the point of rupture in other vertebrates. This observation is important as indicating the independent origin of the two processes^ — the resorption of the caudal intestine and the formation of a cloacal fenestra — and shows that in the duck, at least, the caudal intestine becomes detached slightly in advance of the production of the fenestra. In this specimen, what remains of the undifferentiated primitive streak (ps. v.) is appended to the caudal intestine. In the embryo shown in figure 2, which is younger in other respects, all the primitive streak has been removed, its former presence being indicated only by the roughened and irregular ventral margin of the caudal intestine.

The third stage, illustrated by a chick embryo of forty-one somites (fig. 5), shows an extension of the area of degeneration both caudal and cephalad,^ and the appearance within this area

^ The cephalic extension contains only scattered phagocytes (represented by periods in the figure) and does not usually become denuded of epithelium, although the fenestra has been observed to extend that far in a few cases. If the cut end of the rectum in figure 5 be examined, it will be noticed that the periods are limited to a zone of the cloacal wall which is thinner than the adjacent zones. This area, together with the dorsal wall of the caudal intestine with which it is continue us and homonymous, represents a persistence of the primitive condition of the hind-gut which, like the roof of the f oregut, is always thin-walled when first of discontinuous holes where complete resorption of the epithelium has taken place (fig. 13, from a wax model of the same embryo). The perforated walls of the cloaca at this period thus simulate in appearance a fenestrated membrane. Almost immediately, however, the holes run together, forming a continuous rift along the cloaca and caudal intestine. In this manner the dorsal wall of the cloaca becomes detached from the sides and thus isolated as a trough-shaped structure, is slowly resorbed. Its histological appearance will be described later in the paper.

An invasion of the caudal intestine also occurs from another region in chick embryos and, to a lesser extent, in ducks. This is an extension of the degeneration process going on in the primitive-streak mass (fig. 5, ps. v.) into the ventral wall of the caudal intestine, and involves only that part of the intestine which is adjacent to the primitive streak. Thus, in the undifferentiated epithelium of the inner curvature of the caudal intestine are found phagocytes (again represented by periods, fig. 5) which are coextensive and continuous with the primitive-streak mass, which is itself undergoing rapid phagocytosis. The occurrence of these has nothing to do with the invasion of the caudal intestine from the cloacal end, except that the two processes cooperate in destroying that end of the gut.

The resorption of the caudal intestine in birds can now be summarized as follows. In chick embryos the flanks of the caudal intestine are invaded by a degenerative process originating in the cloaca, which removes the epithelium before the cavity of the anal gut can be occluded. In duck embryos the two processes take place nearly simultaneously, the cloacal invasion slightly preceding the occlusion of the caudal intestine. Finally, in terns, the cloacal fenestra is not present at all, and the caudal intestine undergoes reduction by the method already described as common to most amniotes.

formed. The side walls are the first to thicken. As development proceeds, the latter are brought closely together, buckling the flat, thin-walled area into a steeppitched roof. But for some time there is an abrupt transition between thickand thin-walled portions, and it is along this thin area, and its continuation into the cloaca, that resorption of epithelium first appears.

The final stage in the formation of the fenestra, ending the period of disintegration, is shown in figures 14 and 15, of an 8-mni. embryo of forty-eight somites (3 days and 6 hours) . The entire roof of the cloaca, between the wolffian ducts and the anal side of the caudal intestine, has been denuded of epithelium, leaving a considerable gap bounded only by mesenchyma (dash line, fig. 14). The connection of the cloaca with the caudal intestine has been lost, and the latter, together with the primitive-streak mass, is now rapidly disintegrating at the ruptured ends. As a rule, degeneration does not spread any farther cephalad than recorded in figure 5. But occasionally it extends much farther, and is probably instrumental in producing irregularities in the dorsal wall, which will be discussed later, in the section dealing with accessory diverticula.

The cytological changes involved in the formation of the fenestra include the necrosis of the epithelial cells, their removal by phagocytes, and the reaction of the surrounding mesenchyma to the denuded area. As seen in ordinary serial sections, the first step in the disintegration of the flanks of the cloaca is a slight oedema of the epithelium which causes the cells to spread apart. As these become necrotic, the cytoplasm becomes finely granular and then vesicular and the nuclei pycnotic. At this stage the epithelium presents a confused histological picture due to the simultaneous degeneration of so many cells. But almost immediately the cells in regions y and z (fig. 2) are resorbed, leaving a gap in the wall covered only by mesenchyma. At first the mesenchymal cells appear to congregate about the region, as if to plug up the opening, and this continues as long as there is an abundance of necrotic tissue. During the stage when the wall is a fenestrated membrane the mesenchyma may even invade the cavity. This is especially true of the caudal intestine which is eventually replaced by mesenchyma which has grown in through rifts in the sides and filled the cavity before the walls have been completely removed.

The most favorable time for observing the cytological changes is after the gap has been formed on each flank of the cloaca, but before the roof of the cloaca thus isolated has itself been removed.

The degenerating epithelial cells bordering the gap may then be studied in less crowded condition. Such a picture is presented in figure 19^an obliquely frontal section passing through the fenestrated area at right angles to the back lines of the cloaca; that is, in a plane cutting the allantoic duct lengthwise. In this figure the following features should be noted : the isolated roof of the cloaca, rows of necrotic epithelial cells on either flank, the concentration of mesenchyma about the gap on either side, and the rounded margins of the epithelium conspicuous by their failure to regenerate. In the epithelium bordering the gap are occasional pycnotic nuclei, and here and there a phagocyte, indicating a slow resorption in contrast to the sudden removal characteristic of initial stages. When the degenerative process slows down and finally comes to an end, a single large foramen is left in the dorsal wall of the cloaca extending from behind the level of the wolffian duct to the site of the caudal intestine, having a lenticular shape when viewed from below^ (fig. 15). As seen in microscopic section (fig. 20) the epithelium of the roof of the cloaca has been entirely removed, leaving in its place a line of mesenchymal cells which have flattened out into a surface layer as if under compression by the fluid in the cavity, in a manner recalling the formation of the false epithelium which lines the joint cavities.

Even before degeneration stops, however, the process of closure sets in. This consists of a fusion of the epithelial margins of the gap beginning at the caudal angle of the aperture, so that in the space of another twelve hours, only a slender cleft remains at the anterior end of what was once a big fenestra (fig. 23, fen.). This process of closure seems to be aided if not caused by a progressive approximation of the sides of the cloaca, beginning at the anal plate, which results in the fusion of opposite walls and the formation of a urodaeal membrane. Figure 21, of a crosssection of the fenestra in the last stage of closure, shows that even to the end of closure no regeneration of the cloacal lips has taken place, but that rather the free margins of the walls have been pushed down into the mesenchymal cavity, as if by lateral compression exerted upon the side of the cloaca. By the middle of the fourth day of incubation all signs of the cloacal fenestra have disappeared, and its site cannot be accurately located except in such general terms as lying between the accessory bursa and the urodaeal sinus.

In concluding this chapter one may say that the most conspicuous feature of the entire process is the rapidity with which it takes place^ — both the sudden appearance of a gap and the rapid closure of it — all occurring within a period of twenty-four hours. Although the evidence presented would lead one to infer that the disintegration of the cloacal wall precedes the reduction of the caudal intestine, and is thereby independent of it, and calls for a separate explanation, it is still possible that the cloacal fenestra represents a modification or extension of the process by which the caudal intestine is reduced in other vertebrates. Any attempt, however, to explain the significance of this foramen in the domestic fowl, duck, and pheasant, must take into account, an equally peculiar feature, likewise found only in birds with a fenestra, namely, the undue persistence of the primitive streak in the proximal end of the tail. It is well known that the tail in modern birds, and of fowls in particular, is shorter than in the Archaeornithes. It is conceivable that the degenerating primitive-streak mass in the tail of the chick embryo represents a persistence of material once utilized in tail-building but now superfluous. It would also seem, from a comparison of the cloacas in the first text plate, that the persistence of this indifferent tissue has delayed the differentiation of the caudal intestine and perhaps of the whole tail itself. For figure 5 represents a chick embryo in which the ventral wall of the caudal intestine has not been differentiated into an epithelium, but is still continuous with the primitive streak throughout its length. Yet that chick is older in other respects than the tern embryo of "figure 1, as evidenced by the lesser number of somites in the chick, and by its greater maturity of form. If it be granted that the development of the caudal intestine in the chick has been retarded by the persistence of the primitive-streak mass, it is not inconceivable that the development of the corresponding region in the adjacent cloacal wall has likewise been interfered with, and that when reduction of the caudal intestine does occur, both of these areas are subjected to a retrograde process more rapid and extensive than obtains in other vertebrates.

Development of the Urogenital Apparatus

Anomalies arising in connection with the wolffian ducts

About the time that the primary excretory ducts reach the level of the cloaca in their downgrowth from the pronephros, an eruption of diverticula appears on each flank of the cloaca opposite the distal portion of the dti'pts. Since these outpocketings of the cloaca seem to develop in response to the presence of the wolffian ducts, and later fuse with them, I have named them complemental diverticula. A surface view of this stage, such as is shown in figure 13 of a 41-somite chick. embryo (62 hours), reveals the presence of two groups of diverticula — a circlet of five or six small ones opposite the terminal portion of the duct, and a single larger one farther up on the shaft, as broad as the whole field of smaller ones. In this embryo the duct of the left side has not fused with the cloaca, although fusion on the right side has taken place. In a 40-somite embryo neither duct, has fused. My observations would therefore differ somewhat in detail from the statement of Lillie that the wolffian duct reaches the cloaca (with which it unites) about the 31-som. stage" and that at about the sixtieth hour the ends of the ducts (described in the preceding sentence as solid) fuse with broad lateral diverticula of the cloaca, and the lumen extends backwards until the duct becomes viable (?) all the way into the cloaca (at about 72 hours, 35 somite stage)." For a frontal section (fig. 6) of the cloaca shown in figure 13, at the place where the left wolffian duct makes the nearest approach, shows that the duct has not yet fused with the cloaca, that its terminal portion is patent, and that the mesial wall of the duct is thinning out in anticipation of fusion. The section through the left side happens to pass through three diverticula, the broad one (a) , and two smaller ones (b and c, members of the terminal circlet of diverticula). The arrow indicates that the duct in sections higher up would reach as far as the point c. In subsequent stages the mesial wall of the duct would fuse with the cloacal diverticula forming a continuous plate (figs. 8 and 9, x) from a to c. In some cases the plate ruptures first through the distal diverticulum (see arrow in fig. 8) ; in others at first through the proximal one (fig. 9). But in all chicks of older stages that I have examined, the plate is resorbed, leaving a single large opening from a to c. It is probable that phagocytes aid in this resorption, as I have found them within the thin plate as soon as the duct has joined the cloaca. As development proceeds, the lateral walls of the cloaca beginning with the anal plate gradually come together, forming a solid membrane comparable to the urethral plate of mammals, so that finally the opening of the wolffian duct becomes restricted to the middle of the cloaca at the level a of figure 6 (cf . figs. 14 and 16). Not all of the complemental diverticula, however, fuse with the ducts. Some of them, no doubt, are soon suppressed. Others of them persist for a longer or shorter time, growing out as accessory diverticula (figs. 11, 22, 24, and 32, div.).

TEXT PLATE ILLUSTRATING ANOMALIES OF THE WOLFFIAN DUCT

Fig. 6 Chick, H.E.C. 2071 (section 661) : 2 days, 18 hours. X 77. a, proximal complemental diverticulum; h and c, distal complemental diverticulum; arrow indicates extent of wolffian duct in other sections. Note thinning out of mesial wall of duct in preparation for fusion with cloaca.

Fig. 7 Duck, H.E.C. 2194 (section 680): 3 days, 21 hours. X 77. mes., mesenchyma interposed between distal and proximal attachments of duct.

Fig. 8 Chick, H.E.C. 2073: 2 days, 21 hours. X 77. x, plate formed by fusion of mesial wall of W. D. with complemental diverticula of cloaca; arrow shows where plate has been ruptured, through distal diverticulum.

Fig. 9 Chick, H.E.C. 2072 : 2 days, 22 hours. X 77. Arrow shows where plate has been ruptured through proximal diverticulum.

Fig. 10 Model of duck embryo, H.E.C. 2197: 4 days, 8 hours. X 40. all., allantois; an. pi., cloacal membrane; c. i., caudal intestine; cy., epithelial cysts of unknown origin;/e»., fenestra; t. -p., terminal portion of W. D.; wr."", primordium of ureter; W. D., wolffian duct.

Fig. 11 Model of duck embryo, H.E.C. 2195: 4 days, 8 hours. X 40. div., aberrant complemental diverticulum.

The most interesting anomalies occur in duck embryos, and are due to the excessive length of the wolffian duct, which normally grows down to the very end of the cloaca (fig. 7). In one case observed, only the proximal portion of the duct had fused with the cloaca, the terminal portion growing out as an aberrant diverticulum (fig. 10, t.p., left). In other cases both terminal and proximal portions fuse, but not continuously, so that an area of mesenchyma is left between the two attachments (fig. 7, mes.). If, then, the basal end,s of the ducts begin to grow, a ring-shaped (fig. 10, t.p., right) or a U-shaped (fig. 11, t.p., left) attachment of the ducts is formed, opening into the cloaca at two points, representing the original points of fusion. A similar anomaly has been found in a chick embryo (H.E.C. 99), and it would seem almost certain that a larger number of specimens would show many indications of aberrance resulting from the fusion of the wolffian duct to the complemental diverticula. The further changes in the form of the wolffian ducts and their incorporation into the wall of the cloaca will be considered in the next chapter.

Formation of the urodaeal sinus

In discussing the origin of urinary bladders Felix defines four main types: 1) mesodermal bladders, arising from the fusion or dilation of the caudal ends of the wolffian duct; 2 and 3) dorsal and ventral cloacogenic bladders, outgrowths or dilations of the dorsal and ventral w^alls of the cloaca, respectively, and, 4) allantoidogenic bladders formed by the retention of the proximal end of the allantois. The first type in its pure form is realized only in selachians, the second type only in amphibians, both groups being devoid of an allantois. The bladders of all other vertebrates, according to Felix, are of mixed origin. When we examine birds, it appears that they are the only class among amniotes without one or more bladders, yet curiously enough, reptiles, from which birds have descended, constitute the class with the greatest number and diversity of bladders. Thus, according to Felix, lizards derive their bladders from three sources, dorsocloacogenic, allantoidogenic and mesodermal; and in turtles the bladder is formed from dorsocloacogenic, ventrocloacogenic, allantoidogenic, and mesodermal origins (Keibel and Mall, II, p. 869). It would be strange, then, if the bird did not exhibit some traces of bladder formation in its ontogeny, and such, in fact, may be found. The most conspicuous of these is the intra-embryonic expansion of the allantois shown in figure 39. It is almost identical at this stage with the primordium which develops into the ventral bladder in most reptiles. But it is completely resorbed in adult birds.

The other structure in bird embryos which recalls the reptilian bladders (this time those of dorsocloacogenic and mesodermal origin) is the urodaeal sinus, a name which I have applied to the cavity of the urodaeum at its maximum extent (figs. 40 and 41 mod.). Minot in 1900 called attention to the peculiar relations of this cavity as follows: "From the closure of the intestinal opening by the entoderm (occluded rectum), and of the anal opening by the anal plate (meaning urodaeal membrane), there is left a clear passage from the wolffian duct across (to) the opening of the allantois." And he quotes the suggestion offered by G. H. Parker that "the physiological purpose of this arrangement is to secure the transmission of the excretion from the embryonic kidney to the allantois, and to prevent the escape of the excretion, either into the intestine or into the amniotic cavity, where it might prove injurious to the embryo." That the urodaeal sinus is a mechanism inherited directly from reptiles was revealed two years later by the comparative studies of Fleischmann and his students on the cloaca and phallus of lizards, snakes, turtles, birds, and mammals. He notes that in the Sauropsida the urodaeum is divided into two poriions, a distended oral portion always in relation to the wolffian ducts, and an elongated caudal portion which forms an open passageway (even in young embryos) to the anus. The shutting off of the urodaeal sinus from below in birds is due to the fact that the second half of the urodaeum never elongates, but remains short and impervious through the formation of a urodaeal membrane.

While the posterior portion of the urodaeum becomes elongated and subject to great modification in various reptiles, the anterior chamber (urodaeal Kammer of Unterhossel) is always associated with bladder formation. It becomes chiefly dilated in a dorsolateral direction, so that the entire cavity and associated mesodermal ducts assume the appeance of a dorsal bladder (cf . Fleischmann, Taf. VIII, figs. 1, 2 and 4). This striking feature appears temporarily in bird embryos as the urodaeal sinus, and is as convincing a repetition of reptilian ancestry as the allantoic bladder previously referred to in figure 39. But since it was studied chiefly in older embryos, and then largely by means of sagittal sections, its extent and composition was not fully appreciated even by Fleischmann.

As seen in figures 40 and 41 , the urodaeal sinus (urod.) is a greatly inflated segment of the cloaca, placed athwart the main axis of the hind-gut, between the occluded rectum and the urodaeal membrane. Its lumen from front to back is reduced to the size of a fissure, but is greatly expanded laterally and dorsoventrally, extending from the woMan duct of one side to that of the other and from the dorsal side of the cloaca to the allantois. Although existing as a single structure at this stage, it has been formed by the confluence of three originally separate elements. The first of these to appear is the median diverticulum designated as diverticulum c in the reconstructions shown in plate 3. It arises as early as the beginuing of the fourth day and maintains its identity as a distinct and conspicuous feature of the cloaca as late as the seventh day, at which time it is incorporated in the urodaeal sinus. This structure has been figured in descriptions of the avian cloaca as far back, at least, as the work of Bomhaupt ('67) . But I question whether its existence as a separate rounded diverticulum has ever been appreciated. Pomayer, in the Fleischmann series, labeled it "Urogenitaltasche" in a sagittal section of a duck, giving it the same designation as the paired urogenital pockets of the snake, Tropidonotus, which are dilated outpocketings on the dorsal wall of the cloaca into which the wolffian ducts empty. A median diverticulum occurs in the same place (as diverticulum c) in the turtle embryos modeled by R. F. Shaner (fig. 3, an. s.), and has been interpreted by that author as the primordium from which the respiratory sacs (bursae anales) of turtles develop. In view of its position between the two wolffian ducts in both chicks and turtles, it seems not improbable that diverticulum c represents the dorsal outpocketing of the cloaca of reptiles from which the wolffian ducts have shifted in course of their migration to the allantois. The second and third components of the urodaeal sinus arise more or less together. As seen in figures 14 and 6, thewolffi.an ducts, when they first reach the level of the cloaca, fuse to the cloaca along a broad area extending from the caudal margin to near the allantois (a to c). The fusion at c approximates the primary position of the excretory ducts in lower vertebrates. In consequence, however, of the fusion of the two side walls of the cloaca, beginning with the anal plate, to form the urodaeal membrane, the outlet of the wolffian ducts at c and h in figure 6 is suppressed. The broad complemental diverticulum (fig. 6, a) thus becomes the main channel, and in course of development is enlarged into a wing-like expansion of the cloaca connecting the wolffian duct with the neck of the allantois (fig. 16). Meanwhile the segment of the wolffian duct between the orifice of the ureter and the cloaca begins to develop irregular enlargements sometimes suggesting diverticula (fig. 17), which eventually result in the widening of that segment. By the eighth day the distended ends of the woffian ducts have been taken up in the urodaeal sinus as far as the origin of the ureters, the latter ducts in this process rotating from the dorsal to the mesial border of the wolffian duct. From this period on, the original components lose their identity in the sinus. In the adult the depth of this cavity is greatly reduced, the whole forming a shallow transverse segment, the definitive urodaeum, the latter being separated from the coprodaeum by the urorectal fold of Retterer and from the proctodaeum by the uro-anal fold. The position of these folds in the embryo is evident as early as the beginning of the fourth day of incubation.

Another interesting feature of the urogenital apparatus which occurs at this time is the constriction of the metanephric pelvis at its lower third into a narrow isthmus (fig. 39). This was figured by Schreiner ('02), who noted its relation to the umbilical arteries. As is well known, the adult kidney of birds is constricted into three lobes. The cause of the upper constriction is yet to be determined; the lower constriction is accounted for by the mechanical obstruction offered by the umbilical arteries. The developing kidneys of the pig, as shown by Lewis and Papez, are similarly caught in the bifurcation of these vessels, but instead of becoming notched as in the bird, they escape by moving upward, sometimes, however, being brought so near together as to fuse from side to side, forming a 'horseshoe kidney.'

In closing this chapter I wish to call attention to the changes which have been taking place in the terminal segment of the intestine. In figures 35 and 40 its lumen is shown to be occluded for some distance, the solid tube thus formed joining the urodaeal sinus by a thin linear attachment. By the fifteenth day the cavity of the coprodaeum has been reestablished and considerably distended except at the solid linear attachment. This greatly dilated chamber at the end of the intestine (fig. 41, copr.) is unquestionably homologous with the lower end of the rectum of the human foetus, as figured by Johnson ('14).

This includes a rectal ampulla passing below into a plicated 'zona columnaris.' In the chick embryo it is bounded above by a single transverse plica and below by the urorectal fold already mentioned. Since this ampulla functions as a part of the cloaca in the adult bird, being the chamber in which both fecal matter and urine are retained, it seems better to keep the name coprodaeum, which Gadow applied to the most anterior of the three divisions of the cloaca.

DEVELOPMENT OF THE BURSA OF FABRICIUS AND ASSOCIATED DIVERTICULA

The primordium of the bursa is usually described as a swelling in the caudal wall of the cloaca, caused by the coalescence of vacuoles arising within the urodaeal membrane during the fifth and sixth days of incubation (figs. 31 and 18, bursa). While modeling earlier stages of the cloaca in relation to the development of the fenestra, I was much surprised to find that all chick embryos which had been incubated about four days showed a conspicuous diverticulum at the site of the caudal end of the cloacal fenestra, measured by its greatest extent (figs. 24 and 27, a; cf. figs. 16 and 18). The picture was further complicated by the occurrence, in several cases, of a second diverticulum (fig. 24, b), arising as an outpocketing of the cloaca at the site of the cephalic end of the fenestra. Furthermore, diverticulum a, while originally developing as an invagination of the cloaca, soon became solid, then vacuolated, in continuity with the vacuoles in the developing urodaeal membrane (fig. 28, a), and then, by fusion of vacuoles, appeared to develop into the bursa itself (fig. 30, bursa) . In view of these facts, it seemed not improbable that diverticulum a represented an earlier and more significant stage in the origin of the bursa than had hitherto been reported — a stage which had been overlooked because the cloaca had never been modeled during this period of its growth. This interpretation, if true, would be of importance as bringing the origin of the organ into line with other derivatives of the gut. For it would show that it originated as an invagination of the entodermal tube, thus removing one more difficulty in the interpretation of an organ which has been a bone of contention among anatomists since its discovery by Fabricius. The chief obstacle to this conclusion, however, arose from the examination of a single specimen pictured in figure 29. In this figure diverticulum a seemed farther removed from the anal plate than in other specimens, thereby leaving a vacuolated area between it and the anal plate (labeled bursa in the drawing) which might well develop into the bursa of figure 30, there recognized as the definitive bursa by the coalescence of the vacuoles. To solve this difficulty it became necessary to collect a series of graded embryos of other species of birds. Subsequent reconstruction of domestic duck and pheasant embryos left the matter still more confused, as in these forms the diverticula were present and similar to those in the chick, but less pronounced. Finally, an examination of tern embryos, birds some distance removed from the gallinaceous tribe, brought the desired results. In these forms, as can be seen in figure 36 to 38 and reconstructions of earlier stages, no diverticula are developed at all, and the bursa arises directly from the region adjoining the anal plate, as a thickening of epithelium in continuity with that plate and restricted to the territory lying between it and the site of the caudal intestine (fig. 1). A reexamination of chick embryos in the light of these facts has led to the following conclusions. The bursa of Fabricius in the chick begins soon after the rupture of the caudal intestine, as early as the beginning of the fifth day, as a proliferation of entodermal epithelium on the caudal border of the cloaca adjoining the anal plate (fig. 26, bursa), but it does not develop from the epithelial elements which originally belonged to the caudal intestine, as maintained by Stieda. As the two walls of the cloaca, beginning at the anal plate, progressively fuse to form the urodaeal membrane, vacuoles appear in the solid plate thus formed (figs. 27, 28, and 29, bursa). Those on the free border adjoining the anal plate coalesce and distend the cloaca, forming the definitive bursa of Fabricius (fig. 30, bursa). Previous to these events, however, a diverticulum may appear at each end of the area marking the site of the cloacal fenestra. The caudal diverticulum (a) is always present in chick embryos, where it is associated with the bursa of Fabricius (figs. 33 and 34). The other diverticulum (b), when present, becomes associated with the urodaeal sinus (fig. 32, div. c). Both of them are probably to be regarded as irregularities produced at either end of the fenestra by the removal of intervening epithelium. They are present only in those birds which exhibit a fenestra, and are most conspicuous in that species which has the largest fenestra — the domestic fowl. The regularity with which diverticulum a appears may be explained by the fact that the posterior end of the fenestra is always larger, and that diverticulum a, when first formed, arises from the prominence to which the primitive streak of earlier stages was attached (cf. figs. 21 and 23).

The later stages of development, which have been partly described by previous authors on the basis of sagittal sections, are shown in figures 34 and 39, 35 and 40, and 41. These models illustrate the development of the bursa up to the period of histological differentiation. The successive steps leading to this period are: 1) the continued outgrowth of the bursa and simultaneous enlargement of its cavity through further coalescence of vacuoles; 2) the projection of the anal sinus (proctodaeum) in a ventrodorsal direction across the flanks of the urodaeum on its way to connect with the bursa (cf. figs. 18 and 39); 3) the breaking through of the thin plate separating the cavity of the bursa from the proctodaeum (cf. figs. 34 and 35), and, lastly (fig. 41), the differentiation into three parts of the passage-way thus made continuous from anus to the end of the bursa. At this stage (eleventh day) this passage-way is still separated from the rest of the cloaca by the urodaeal membrane, which does not rupture until after the seventeenth day (Gasser). As seen in figure 41, the first of its three parts, the proctodaeum of ectodermal origin, has assumed the shape of a compressed chamber with broad flange-like expansions. By the fifteenth day ectodermal glands have begun to differentiate around its circumference. The second and third parts, of entodermal origin, have developed, respectively, into a short bursal stalk and a greatly expanded but plicated sac, the bursa itself (fig. 41). The cavity of the latter is subdivided by longitudinal plicae into eleven (or twelve) grooved chambers. A cross-section of the bursa during the fifteenth day (fig. 12) shows that in the interval between the eleventh and fifteenth days some of the primary plicae have cleft the central cavity deeper than others, so that the eleven primary cavities have become tributary to six or seven secondary channels, opening into the main cavity after the manner that minor and major calyces open into the pelvis of the kidney.

Fig. 12 Transverse section of a model of a 55-mm. chick embryo, H.E.C. 1968: 14 days and 5 hours. X 28. bl. v., blood vessel; cav., cavity of bursa; cor., cortex of follicle, derived from tunica propria; med., medulla of follicle, derived from epithelium; muse, muscularis; t. p., tunica propria.

Histogenesis begins with the appearance of the primary plicae and ends in the formation of spherical masses of lymphoid tissue (the 'follicles' of Stannius). Each follicle consists of a cortex and a medulla, the medullae or cores of the follicles (the Tollikelkeime' of Stieda) being the first to appear. These grow out into the tunica propria as solid buds of epithelium which soon become clothed peripherally with a cortical layer derived from the subjacent connective tissue (fig. 12, cor. and med.). In the course of development the follicles grow larger and larger until they meet, the resulting pressure molding them into a polyhedral shape. The walls of the bursa thus become greatly thickened, resembling somewhat in gross appearance the walls of the proventriculus (glandular stomach of birds) to which the bursa was compared in 1829 by Berthold. In the region next to the stalk, according to Schumacher ('03), the follicles are neither so thick nor so sharply limited, but look more like a diffuse infiltration of tunica propria with lymphocytes. To these finger-like processes, which in my model of the fourteen-day chick are restricted to the dorsal wall of the bursa where it joins the stalk, Schumacher has applied the term mucosal villi.

The nature of the epithelial transformation has received several interpretations. Wenckebach ('88) and Schumacher ('03) maintain that the entodermal epithelium constituting the medulla of each follicle is differentiated directly into lymphoid tissue, and that tliis process is followed by a differentiation of the mesenchymal cortex into a similar tissue, the border-line between the two layers becoming ill-defined in later stages. Retterer, in his latest paper ('13), extends the activity of the epithelium still further, stating that the cortex of the follicles of the bursa is likewise of epithelial origin." The most comprehensive account, however, is that of Jolly ('15), who based his conclusions not merely upon histogenesis, but also upon the involution of the organ (both natural and induced) and upon examination of tissues in vitro. Beginning with the eleventh day of incubation, he finds numerous amoeboid cells, formed directly from the mesenchymal network, accumulating in the vicinity of the epithelial buds. These they soon invade, the most active phase of penetration occurring between the fourteenth and eighteenth days. Although at first the epithelial cells give way to the new arrivals, by becoming detached from one another and in some cases by even degenerating, the majority of them, he maintains, enter upon a symbiotic relation with the invaders by means of which both cell strains continue to divide actively, the amoeboid cells giving rise to large numbers of small lymphocytes, the epithelial cells forming a reticular network within which the lymphocytes reside. Simultaneously the cortex becomes differentiated into a highly vascularized lymphoid tissue.

In involution the order of events is reversed; the lymphocytes in the medulla die and the epithelial cells close their ranks, tending to reconstitute themselves into a compact epithelial bud — a process which Jolly has compared to the production of Hassal's corpuscles in the thymus. As involution continues the follicles separate from the epithelium and become replaced by fibrous tissue, the whole process taking place progressively from apex to base of the bursa in such a way that a gradual but rapid diminution of volume and weight ensues. During the eighth month the bursa loses all possibility of functioning, and in the course of the next two months becomes reduced to a thin-walled cyst, still opening into the cloaca at its posterior end, but so completely fused to the aponeurosis of the rectum that it can be detected only by careful dissection. In this condition it may persist until old age. Only in the Ratitae, according to Forbes, does it remain as an undiminished organ throughout life where, by virtue of its broad opening into the proctodaeum, it becomes a repository for the urine. In these birds, according to Gadow, micturition and defecation are separate processes, whereas in most other birds the urine backs up into the coprodaeum and there mixes with the faeces until evacuated.

The following table, arranged from data submitted by Jolly, is introduced to summarize the growth and involution of the bursa in the fowl:

^ Length Weight

mm. grams

Hatching 5 0.05

1 month 10 0.50

2 months 15-18 0.50-1.0

3 months 20-25 1.5

4 months 30 3.0 (:f^^ of body)

4| months 2.51

5 months .97

6 months 0.22

7 months 10-20 0.26

12 months .' 0.12

The function of the bursa has never been satisfactorily explained. Jolly's description of the haematopoietic foci of the bursa, from which he derives not merely lymphocytes, but also red corpuscles and granular leucocytes, has added something to our knowledge of its activity, but, as he well recognized, this function is not peculiar to the bursa, but is an attribute common to the mesenchyma of certain other organs. He does, however, propose a specific function when he suggests that the bursa contributes substances to the organism which bear a causal relation to the inception of sexual maturity. He bases this theory on two facts: 1) that the maximum development of the bursa is attained at the time when spermatogenesis is just getting under way; 2) that involution of the bursa corresponds exactly with the appearance of sexual maturity, as measured by the sudden increase of testicular weight and the appearance of ripe spermatozoa. Before accepting this theory, however, one would like to know to what extent the precocious involution, which Jolly produced in the bursa by means of the x-ray, affected the differentiation of the testis. That some such line of experimentation as this would be profitable seems almost certain when we consider the history of such organs as the thymus. For it is far from inconceivable that the bursa may also be a glandular organ in process of transformation into an endocrine gland, if it has not already arrived at that estate.

The phylogenetic interpretation of the bursa is equally obscure. An extensive number of investigators distributed over three centuries have tried to solve this problem and during this period have proposed numerous hypotheses, all of which have been rejected (see Retterer, '13 b, for list). Forbes, after examining the bursae of over ninety species of birds and covering the literature, came to the conclusion that the bursa was a glandular outgrowth of birds sui generis. Wenckebach limited the problem by establishing the entodermal origin of the bursa, thus making obligatory the origin of homologous structures (with which it is to be compared) from the dorsal wall of the vertebrate cloaca. Its origin has been still further limited by this paper to the area between the cloacal end of the caudal intestine and the anal plate.

These limitations render untenable the hypothesis put forth by Stieda ('80) that the bursa develops from the epithehal elements which originally belong to the caudal intestine." Equally untenable is the modification of this theory, presented by Fleischmann ('02). ^ Recently Stieda's point of view has been revived again, this time by Jolly ('15), who has made it a basis for the theory that the bursa represents a recrudescence of the cloacal end of the ruptured caudal intestine.

The first anlage of the bursa," he writes in his conclusion," occupies exactly the situation of the post-anal intestine and it is orientated like it; it may be said, even, that the anlage blends with what remains of the post-anal intestine. One may consider that the bursa represents the remainder of the caudal intestine which rises up again posteriorly and, turned toward the head, undergoes a further development under the form of a true cloacal caecum, in the walls of which lymphoid tissue develops."

In refutation of this. theory, new evidence, presented in the first section of this paper, shows that the entire region of junction between caudal intestine and cloaca, together with the adjacent wall of the latter, has been removed by the process which forms the cloacal fenestra. There is, therefore, nothing left of this end of the caudal intestine which Jolly assumes to be present and which he describes as growing out, in an unusual direction, to form the bursa. Furthermore, even after the closure of the fenestra, the bursa does not arise at the site of the former caudal intestine, but on the anal side of it, beyond diverticulum a (figs. 25 to 33).

Another theory, presented during the last ten years, is that of Osawa ('11), who has revived the hypothesis of Martin St. Ange ('56) . He believes that the bursa is homologous with the prostate gland even though the latter is well developed in the male only. Osawa bases his conclusions on the ground that the "bursa occupies the place where the ureter and ductus deferens discharge themselves, and its follicles are laid out after the manner of glands." In refutation of this view, it may be stated that the point of origin of the group of glandular outgrowths that constitute the prostate gland is rather remote, embryologically, from that of the bursa; also that the prostate develops much later and is radically different in its histological nature. Physiologically it becomes functional with sexual maturity, at the time when, as Jolly has shown, the bursa degenerates.

In a foot-note to his paper (p. 58) Fleischmann suggests that "the caudal process of the primitive urodaeum of mammals, which now bears the perplexing name caudal intestine, is comparable morphogenetically with the bursa of Fabricius." This conjecture has recently called forth the following rejoinder from Keibel ('21): "The caudal intestine of birds has not the slightest thing to do with the bursa of Fabricius."

The only other vertebrate structures thus far proposed, which in any way meet the requirements of the homology, are the anal sacs (bursae anales) of turtles. Gadow, in the Cambridge Natural History Series, 1909, describes these organs in the adult as highly vascularized, thin-walled sacs which are incessantly filled and emptied with water through the vent, and act as important respiratory organs. Forbes, in. 1877, objected to the comparison of these sacs with the bursa of Fabricius on the ground that they were paired, lateral structures. Wenckebach also saw this objection, but considered that the anal sacs were the only diverticula which in any way could be compared in point of origin with the bursa, and, in view of the almost total ignorance regarding the embryology of the sacs, held that the objections to the comparison should not be conclusive. During the last year a graded series of models of the turtle cloaca have been made in this laboratory by R. F. Shaner as a part of an anatomical study of the 9.5-mm. Chrysemys embryo. As a result of this study he is of the opinion that the anal sacs arise from a single median diverticulum (fig. 3, an. s.). Through the courtesy of Doctor Shaner, I have had the pleasure of studying the models upon which his paper is based and concur in his opinion. Another feature which at first seemed to favor the comparison between the bursa and the anal sacs is the striking similarity of the process by means of which the outlet of each diverticulum is taken over by the proctodaeum. In each case lateral expansions of the proctodaeum (fig. 39) grow down across the flanks of the cloaca until they establish communication with either the bursa or the anal sacs. But the description of the saurian cloacas in the Fleischmann series seems to indicate that this invasion of some point of the urodaeum by the lateral proctadaeal invagination is not restricted to reptiles equipped with anal sacs, but occurs in most other reptiles. Another objection to this homology is based upon the fact that the anal sacs arise on the cephaUc rather than on the anal side of the caudal intestine. They are thus more nearly comparable to diverticulum c, which unquestionably represents the urodaeal Kammer or dorsal bladder of the saurian cloaca, than to the bursa of Fabricius.

In Unterhossel's account of the saurian cloaca another diverticulum is represented which, as a possible homologue of the bursa, seems much more promising. This is an invagination of the dorsal wall of the cloaca, defined by Unterhossel as lying at the junction of the urodaeum and the proctodaeum. It is figured in models of late embryonic stages of three different species, and would seem to be a modification of the same structures. The first is a vaulted portion of the roof of the urodaeum of the lizard Platydactylus guttatus (Taf. VIII, fig. 1, st). The second is a comb-shaped diverticulum occupying the same position in the cloaca of the snake Anguis fragilis (Taf. VIII, fig. 2, not labeled) . The third consists of a pair of dorsal diverticula lying behind the urodaeal chamber and described as outpocketings of the proctodaeum in the snake Tropidonotus natrix (Taf. VIII, fig. 4, s). But it will be remembered that the bursa for a long time was described as an outgrowth of the proctodaeum, and the author in this case admits the lack of younger stages. From an examination of the account of the saurian cloaca I am convinced that the key to the homology of the bursa of Fabricius lies in the study of the reptilian cloaca, and am optimistic enough to believe that such a careful study of the younger stages of the reptile cloaca as Fleischmann and his students have made of older stages will bring the desired results. The comparison which Schumaker has lately made with the tonsiloid tissue discovered by Keibel in the cloaca of the mammal Echidna does not seem to meet the problem. At best it can only be considered a vestige of a reptilian prototype, and to reptiles we must again direct our attention for interpretation of the bursa of Fabricius.

Summary

This paper represents a review of the development of the cloaca in bird embryos from the third to the fifteenth day of incubation. It is based on the study of a large number of chick embryos supplemented by observations on three other species of birds. The most striking feature to be recorded is the regular occurrence of a temporary fenestra in the wall of the cloaca, caused by the disintegration of a definitely localized area of epithelium and its subsequent removal by phagocytes, following which the contents of the cloaca are left in contact with the mesenchyma for a period of nearly twenty-four hours. It is of interest not merely because it furnishes the only instance in the differentiation of a hollow organ in which a gap occurs in the epithelial wall as a normal and constant feature of development, but also because it enables us, by virtue of the landmarks it establishes, to determine for the first time the exact point of origin of the bursa of Fabricius.

The second part of this paper deals with the formation of a temporary sinus, placed athwart the main axis of the cloaca, which sinus has been interpreted as a repetition of the dorsal bladder of reptiles. This section also deals with some interesting anomalies growing out of the attachment of the wolffian ducts to the cloaca.

A third feature of interest is the regular occurrence in chick embryos of an accessory bursal diverticulum {div. a), probably arising from the irregularities consequent upon the formation of the cloacal fenestra. By means of this diverticulum it has been possible to define the primordium of the bursa more accurately than has hitherto been done and therefore to offer new suggestions regarding its phylogenetic origin.

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Arch. f. Anat. u. Entwick., S. 297-319. Harvey, William 1651 De generatione animalium. Tr. Syd. Soc. 1847, p. 183.

London. Johnson, F. P. 1914 The development of the rectum in the human embryo.

Am. Jour. Anat., vol. 16, pp. 1-57. Jolly, T. 1915 La bourse de Fabricius et les organes lymphoepitheliaux.

Arch, d'anat. micr. T. 16, pp. 363-547. Keibel, Franz 1902 Zur Anatomie des Urogenitalkanals der Echidna aculeata var. typica. Anat. Anz., Bd. 22. S. -301.

1921 Der Schwanzdarm und die Bursa Fabricii bei Vogelembryonen. Anat. Anz., Bd. 54, S. 301-303. Lewis and Papez 1914 Anat. Rec, vol. 9, p. 105.

Leydig 1857 Lehrbuch der Histologie, S. 321. Frankfurt am Main. AIiNOT, C. S. 1900 On the solid stage of the large intestine in the chick. Bos.

Soc. Nat. Hist., vol. 4, pp. 153-164. OsAWA, Gakutaro 1911 L^eber die Bursa Fabricii der Vogel. Mitt, aus den

Med. Fak. der Kais. Jap. Univ. zu Tokyo, Bd. 9, S. 299-341. PoMAYER, Carl 1902 III. Die Vogel. In Fleischmann's Kloake und Phallus,

S. 78-116. Retterer, E. 1885 Contributions a I'etude du cloaque et de la bourse de Fabricius chez des oiseaux. Journ. de I'anat. et la phys., T. 21, p. 369. 1913 a Nouvelles recherches sur la bourse de Fabricius. C. R. de la Soc. de Biol., 25 Janvier, T. 74, p. 182.

1913 b Homologies de la bourse de Fabricius. C. R. de la Soc.de Biol., 22 fevrier, T. 74, no. 8, p. 382. Schreiner, K. E. 1902 Ueber die Entwickelung der Amniotenniere. Zeitschr.

f. wiss. Zool., Bd. 71, S. 66. Schumacher, Siegmtjnd 1903 Ueber die Entwicklung und den Bau der Bursa Fabricii. Sitzber. d. kais. Akad. d. Wiss. in Wien, Bd. 112, Abt. Ill, S.163. Stieda, Ludwig 1880 Ueber den Bau und die Entwickelung der Bursa Fabricii.

Zeitschr. f. wiss. Zool., Bd. 34, S. 296-309. Untbrhossel, Paul 1902 I. Die Eidechsen und Schlangen, S. 5-45. In

Fleischmann's Kloake und Phallus. Wenckebach, K. F. 1888 De Ontwikkeling en de Bouw der Bursa Fabricii. Proefschrift. Leiden. 1896 Die Follikel der Bursa Fabricii. Anat. Anz., Bd. 11, S. 159.

Plates

Plate 1

EXPLANATION OF FIGURES

Models illustrating the formation of a cloacal fenestra and the early development of the cloaca in chick embryos. All figures are drawn to the same scale (magnification, X 50). H. F. Aitken, del. (plates 1 and 4).

13 H. E. C. 2071 : 2 days, 18 hours (cf. with text fig. 5, a sagittal reconstruction of the same embryo). In passing across the picture from left to right at its upper level the organs are encountered in the following order: medullary tube, notochord, caudal intestine, primitive-streak mass, proctodaeum, allantois, rectum, dorsal aortae. This stage shows the persistence of a mass of primitivestreak tis.sue in the angle between the cloaca and caudal intestine; the mergence of four structures (medullary tube, notochord, caudal intestine, and anterior half of primitive-streak remnant) with the indifferent tail-bud mass; a circlet of five or six complemental diverticula around the unattached terminal portion of the W. D. ; a larger complemental diverticulum opposite its shaft; and the isolated foramina (in the back wall of the cloaca and adjacent portion of the caudal intestine) which mark the first step in the disintegration of the cloacal wall and the formation of a fenestra.

14 and 15 H.E.C. 1953: 3 days, 6 hours; 8 mm. (cf. with fig. 22, a sagittal reconstruction of the same embryo). At the left of figure 13 are the remnants of the caudal intestine and primitive streak, each detached from the cloaca by a process of disintegration. The dash line indicates that portion of the cavity of the cloaca which has been denuded of epithelium. It is bounded by mesenchyma only, and indicates the maximum extent of the cloacal fenestra, shown to better advantage from below in figure 15. At the cephalic end of the fenestra in both figures is an aberrant diverticulum probably derived from one of the complemental diverticula shown in figure 12.

16 H. E. C. 1942: 4 days, 3 hours; 10.5 mm. (cf. with fig. 27, a sagittal reconstruction of the same embryo). Note diverticula lettered a and c in fig. 26, together with accompanying legend.

17 H.E.C. 2097:4 days, 3 hours; 10.5 mm. (cf. with fig. 28, a sagittal reconstruction of the same embryo). Note accessory diverticulum lettered h in figure 27.

18 H.E.C. 1951: 5 days, 13 mm. (cf. with fig. 31, a sagittal reconstruction of the same embryo). Note the swelling (bursa of Fabricius) caused by coalescence of vacuoles at the bottom of the cloaca; the distended cavity of the urodaeum connecting allantois and excretory ducts; the flattened and occluded area between the urodaeum and bursa (urodaeal membrane) ; the down-growing proctodaeum astride the cloacal membrane, reaching out to connect with the bursa; the constriction in the metanephric pelvis marking the future division between the second and third lobes of the adult kidney (cf. with fig. 39).

Plate 2

EXPLANATION OP FIGURES

Projection-lantern drawings of microscopic sections through the cloacal fenestra of chick embryos, drawn to the same scale (magnification, X 340).

19 H.E.C. 512 (section 121) : 2 days, 20 hours? Obliquely-transverse section passing through cloaca at right angles to the long axis of the fenestra (of. with imaginary line connecting letters y and all. in text fig. 5). Note bilaterally symmetrical gaps in cloacal wall; the concentration of mesenchyma around the gaps; the isolated floor of the cloaca, with necrotic cells on margin; the phagocytes in the cavity and the pycnotic nuclei in the epithelium bordering the gap.

20 H.E.C. 2057 (section 736): 3 days, 4 hours; 6.8 mm. Section through fenestra during period of maximum e.xtent (cf. embryos shown in figs. 14, 15 and 22). Note complete resorption of disintegrating epithelium shown in preceding figure, the rounded epithelial margins which fail to regenerate, the flattening out of the mesenchyma bordering exposed cavity.

21 H.E.C. 2124 (section 749): 3 days, 18 hours; 8.5 mm. Last stage before closure showing section through fenestra reduced to small slit (same age as embryos shown in figs. 23 and 24). Note approximation of two side walls, the complete absence of regeneration along epithelial margins.

Plate 3

EXPLANATION OF FIGURES

Graphic reconstructions of the cloaca of bird embryos drawn to the same scale (magnification, X 35). Dash lines indicate cavity; dotted lines, vacuoles. This plate represents chiefly a quantitative study of chick embryos made to demonstrate the origin of the bursa of Fabricius together with the identity and significance of a series of diverticula occurring on the back wall of the cloaca between the anal plate and the rectum. Diverticulum a represents an accessory diverticulum, arising from the caudal angle of the cloacal fenestra, which regularly becomes appended to the bursa of Fabricius; h represents an accessory diverticulum, only occasionally present, which arises from the cephalic angle of the cloacal fenestra and which becomes associated with the urodaeal sinus; c represents a diverticulum which regularly forms the medial component of the urodaeal sinus.

22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38

Chick embryo, H.E.C. 1953. Chick embryo, H.E.C. 2120. Chick embryo, H.E.C. 2126. Chick embryo, H.E.C. 2058. Chick embryo, H.E.C. 2098. Chick embryo, H.E.C. 1942. Chick embryo, H.E.C. 2097. Chick embryo, H.E.C. 2100. Chick embryo, H.E.C. 1943. Chick embryo, H.E.C. 1951. Chick embryo, H.E.C. 2059. Chick embryo, H.E.C. 2074. Chick embryo, H.E.C. 2076.

Chick embryo, H.E.C. 1962.

Sterna hirundo (common tern) H.E.C. 2169.

Sterna hirundo (common tern) H.E.C. 2115.

3 days, 6 hours, 8.0 mm. 3 days, 18 hours, 9.2 mm.

3 days, 18 hours, 9.5 mm.

4 days, 4 hours, 11.0 mm. 4 days, 3 hours, 10.0 mm, 4 days, 3 hours, 10.5 mm. 4 days, 3 hours, 10.5 mm. 4 days, 22 hours, 13.0 mm.

4 days, 3 hours, 12.0 mm.

5 days, hours, 13.0 mm.

4 days, 23 hours, 14.0 mm.

5 days, 23 hours, 15.0 mm.

6 days, 7 hours, 17.3 mm. 8 days, 1 hours, 21.5 mm.

8.0 mm. 10.4 mm.

Sterna hirundo (common tern) H.E.C. 2173. 13.4 mm.

ABBREVIATIONS

all., allantois

an., anus

an. pi., cloacal membrane (anal plate)

huma, bursa cloacae (of Fabricius)

Cauda, inner curvature of tail

cau. A., caudal artery

c, %., caudal intestine

copr., coprodaeum (ampulla recti)

d., accessory rectal diverticulum

div., complementary diverticula

fen., cloacal fenestra

Mull., Miillerian duct

pelv., pelvis of kidney

phal., phallus

proct., proctodaeum

ps. v., ventral half of primitive streak

red., ampulla recti (coprodaeum)

umb. A., umbilical artery

ur., ureter

urod., urodaeum

ur. m., urodaeal membrane

W. D., Wolffian duct

198

Plate 4

EXPLANATION OP FIGURES

39 Model of chick embryo, H.E.C. 1945: 5 days, 15 hours; 15 mm. X 37. Showing especially the bladder-like enlargement of the allantois in the intraembryonic body cavity, the lateral invaginations of the proctodaeum to meet the bursa of Fabricius {prod.), and the constriction of the metanephric pelvis into two parts by the umbilical artery.

40 Model of chick embryo, H.E.C. 1962: 8 days, 1 hour; 21.5 mm. X 37. Note the occluded rectum, the prominent urodaeal sinus (urod.), and the elongating bursa.

41 Modelof chick embryo, H.E.C. 1967: 11 days; 31 mm. X 21. Note differentiation of bursa into stalk and plicated ghxnd, also division of cloaca into the three transverse parts characteristic of the adult: proctodaeum (ectodermal origin); urodaeum, cloaca proper, receiving urogenital ducts; and the coprodaeum, rectal amjiulla, with its 'zona columnaris.'

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