The Works of Francis Balfour 1-13
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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. I. Separate Memoirs (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. IV. Plates (1885) MacMillan and Co., London.
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Vol I. Separate Memoirs (1885)
XIII. On the Existence of a Head-Kidney in the Embryo Chick, and on certain points in the Development of the Müllerian Duct
By F. M. BALFOUR and A. SEDGWICK.
(With Plates 27 and 28.)
THE following paper is divided into three sections. The first of these records the existence of certain structures in the embryo chick, which eventually become in part the abdominal opening of the Miillerian duct, and which, we believe, correspond with the head-kidney, or " Vorniere " of German authors. The second deals with the growth and development of the Miillerian duct. With reference to this we have come to the conclusion that the Miillerian duct does not develop entirely independently of the Wolffian duct. The third section of our paper is of a more general character, and contains a discussion of the rectifications in the views of the homologies of the parts of the excretory system in Aves, necessitated by the results of our investigations.
We have, as far as possible, avoided entering into the extended literature of the excretory system, since this has been very fully given in three general papers which have recently appeared by Semper 2 , Fiirbinger 3 , and by one of us 4 .
All recent observers, including Braun 6 for Reptilia, and Egli 8 for Mammalia, have stated that the Miillerian duct develops as a groove in the peritoneal epithelium, which is continued backward as a primitively solid rod in the space between the Wolffian duct and peritoneal epithelium.
1 From the Quarterly Journal of Microscopical Science, Vol. xix. 1879. 2 "Das Urogenital-System der Plagiostomen," Arbeiten a. d. zool.-zoot. Institut. Wurzburg. 3 " Zur vergl. Anat. u. Entwick. d. Excretionsorgane d. Vertebraten," Morphologisches Jahrbuch, Vol. IV. 4 " On the Origin and History of the Urinogenital Organs of Vertebrates," Journal of Anat. and Phys., Vol. X. [This Edition No. vn.]
8 Arbeiten a. d. zool.-zoot. Institut. Wurzburg, Vol. IV.
8 Beitr. zur Anat. u. Entwick. </. Geschlechtsorgane, Inaug. Diss., Zurich, 1876.
In our preliminary account we stated 1 , in accordance with the general view, that the Miillerian duct was formed as a groove, or elongated involution of the peritoneal epithelium adjoining the Wolffian duct. We have now reason to believe that this is not the case. In the earliest condition of the Mullerian duct which we have been able to observe, it consists of three successive open involutions of the peritoneal epithelium, connected together by more or less well-defined ridge-like thickenings of the epithelium. We believe, on grounds hereafter to be stated, that the whole of this formation is equivalent to the head-kidney of the Ichthyopsida. The head-kidney, as we shall continue to call it, takes its origin from the layer of thickened epithelium situated near the dorsal angle of the body-cavity, close to the Wolffian duct, which has been known since the publication of Waldeyer's important researches as the germinal epithelium. The anterior of the three open involutions or grooves is situated some little distance behind the front end of the Wolffian duct. It is simply a shallow groove in the thickest part of the germinal epithelium, and forms a corresponding projection into the adjacent stroma. In front the projection is separated by a considerable interval from the Wolffian duct ; but near its hindermost part it almost comes into contact with the Wolffian duct. The groove extends in all for about five of our sections, and then terminates by its walls becoming gradually continued into a slight ridge-like thickening of the germinal epithelium. The groove arises as a simple depression in a linear area of thickened germinal epithelium. The linear area is, however, continued very considerably further forward than the groove, and sometimes exhibits a slight central depression, which might be regarded as a forward continuation of the groove. The passage from the groove to the ridge may best be conceived by supposing the groove to be suddenly filled up, so as to form a solid ridge pointing inwards towards the Wolffian duct.
1 Proceedings of Royal Society, 1878.
The ridge succeeding the first groove is continued for about six sections, and is considerably more prominent at its posterior extremity than in front. It is replaced by groove number two, which appears as if formed by the reverse process to that by which the ridge arose, viz., by a hollowing out of the ridge on the side towards the body-cavity. The wall of the second groove is, after a few sections, continued into a second ridge or thickening of the germinal epithelium, which, however, is so faintly marked as to be hardly visible in its middle part. In its turn this ridge is replaced by the third and last groove. This vanishes after one or two sections, and behind the point of its disappearance we have failed to find any further traces of the head-kidney. The whole formation extends through about twenty-four of our sections and one and a half segments (muscleplates).
We have represented (Plate 27, Series A, Nos. I 10) a fairly complete series of sections through part of the head-kidney of an embryo slightly older than that last described, containing the second and third grooves and accessory parts. The connection between the grooves and the ridges is very well illustrated in Nos. 3, 4, and 5 : of this series. In No. 3 we have a prominent ridge, in the interior of which there appears in No. 4 a groove, which becomes gradually wider in Nos. 5 and 6. Both the grooves and ridges are better marked in this than in the younger stage but the chief difference between the two stages consists in the third groove no longer forming the hindermost limit of the head-kidney. Instead of this, the last groove (No. 7) terminates by the upper part of its walls becoming constricted off as a separate rod, which appears at first to contain a lumen continuous with the open groove. This rod (Nos. 7, 8, 9, 10) situated between the germinal epithelium and Wolffian duct is continued backward for some sections. It finally terminates by a pointed extremity, composed of not more than two cells abreast (Nos. 8 10).
Our third stage, sections of which are represented in series B (Plate 27), is considerably advanced beyond that last described. The most important change which has been effected concerns the ridges connecting the successive grooves. A lumen has appeared in each of these, which seems to open at both ends into the adjacent grooves. At the same time the cells, which previously constituted the ridge, have become (except where they are continuous with the walls of the grooves) partially constricted off from the germinal epithelium. The ridges, in fact, now form ducts situated in the stroma of the ovarian ridge, in the space between the Wolffian duct and the germinal epithelium. The duct continuous with the last groove is somewhat longer than before. In a general way, the head-kidney may now be described as a duct opening into the body-cavity by three groove-like apertures, and continuous behind with the rudiment of the true Miillerian duct. Although the general constitution of the head-kidney at this stage is fairly simple, there are a few features in our sections which we do not fully understand, and a few points about the organ which deserve a rather fuller description than we have given in this general sketch.
The anterior groove (Nos. I 3, series B, PI. 27) is at first somewhat separated from the Wolffian duct, but approaches close to it in No. 3. In Nos. 2 and 3 there appears a rod-like body on the outer side of the walls of the groove. In No. 2 this body is disconnected with the walls of the groove, and even appears as if formed by a second invagination of the germinal epithelium. In No. 3 this body becomes partially continuous with the walls of the groove, and finally in No. 4 it becomes completely continuous with the walls of the groove, and its lumen communicates freely with the groove 1 .
The last trace of this body is seen on the upper wall of the groove in No. 5. We believe that the body (r x ) represents the ridge between the first and second grooves of the earlier stage; so that in passing from No. 3 to No. 5 we pass from the first to the second groove. The meaning of the features of the body r l in No. 2 we do not fully understand, but cannot regard them as purely accidental, since we have met with more or less similar features in other series of sections. The second groove becomes gradually narrower, and finally is continued into the second ridge (No. 8). The ridge contains a lumen, and is only connected with the germinal epithelium by a narrow wall of cells. A narrow passage from the body-cavity leads into that wall for a short distance in No. 8, but it is probably merely the hinder end of the groove of No. 7. The third groove appears in No. 11, and opens into the lumen of the second ridge (r 2 ) in No. 12. In No. 13 the groove is closed, and there is present in its place a duct (r B ) connected with the germinal epithelium by a wall of cells. This duct is the further development of the third ridge of the last stage ; its lumen opens into the body-cavity through the third and last groove (gr^). In the next section this duct (r a ) is entirely separated from the germinal epithelium, and it may be traced backwards through several sections until it terminates by a solid point, very much as in the last stage.
1 A deep focus of the rather thick section represented in No. 3 shewed the body much more nearly in the position it occupies in No. 4.
In the figures of this series (B) there may be noticed on the outer side of the Miillerian duct a fold of the germinal epithelium (x) forming a second groove. It is especially conspicuous in the first six sections of the series. This fold sometimes becomes much deeper, and then forms a groove, the upper end of which is close to the grooves of the head-kidney. It is very often much deeper than these are, and without careful study might easily be mistaken for one of these grooves. Fig. C, taken from a series slightly younger than B, shews this groove (x) in its most exaggerated form.
The stage we have just described is that of the fullest development of the head-kidney. In it, as in all the previous stages, there appear to be only three main openings into the body-cavity ; but we have met in some of our sections with indications of the possible presence of one or two extra rudimentary grooves.
In an embryo not very much older than the one last described the atrophy of the head-kidney is nearly completed, and there is present but a single groove opening into the bodycavity.
In series D (PL 28) are represented a number of sections from an embryo at this stage. Nos. I and 2 are sections through the hind end of the single groove now present. Its walls are widely separated from the Wolffian duct in front, but approach close to it at the hinder termination of the groove (No. 2). The features of the single groove present at this stage agree closely with those of the anterior groove of the previous stages. The groove is continued into a duct the Miillerian duct (as it may now be called, but in a previous stage the hollow ridge connecting the first and second grooves of the head -kidney) which, after becoming nearly separated from the germinal epithelium, is again connected to it by a mass of cells at two points (Nos. 5, 6, and 8). The germinal epithelium is slightly grooved and is much reduced in thickness at these points of contact (gr z and gr a \ and we believe that they are the remnants of the posterior grooves of the head-kidney present at an earlier stage.
The Miillerian duct has by this stage grown much further backwards, but the peculiarities of this part of it are treated in a subsequent section.
We consider that, taking into account the rudiments we have just described, as well as the fact that the features of the single groove at this stage correspond with those of the anterior groove, at an earlier stage, we are fully justified in concluding that the permanent abdominal opening of the Miillerian duct corresponds with the anterior of our three grooves.
Although we have, on account of their indefiniteness, avoided giving the ages of the chicks in which the successive changes of the head-kidney may be observed, we may, perhaps, state that all the changes we have described are usually completed between the Qoth and i2oth hour of incubation.
The Glomerulus of the Head-Kidney.
In connection with the head-kidney in Amphibians there is present, as is well known, a peculiar vascular body usually described as the glomerulus of the head-kidney. We have found in the chick a body so completely answering to this glomerulus that we have hardly any hesitation in identifying it as such.
In the chick the glomerulus is paired, and consists of a vascular outgrowth or ridge projecting into the body-cavity on each side at the root of the mesentery. It extends from the anterior end of the Wolffian body to the point where the foremost opening of the head-kidney commences. We have found it at a period slightly earlier than that of the first development of the head-kidney. It is represented in figs. E and F, PI. 28 gl, and is seen to form a somewhat irregular projection into the bodycavity, covered by a continuation of the peritoneal epithelium, and attached by a narrow stalk to the insertion of the embryonic mesentery (me).
In the interior of this body is seen a stroma with numerous vascular channels and blood corpuscles, and a vascular connection is apparently becoming established, if it is not so already, between the glomerulus and the aorta. We have reason to think that the corpuscles and vascular channels in the glomerulus are developed in situ. The stalk connecting the glomerulus with the attachment of the mesentery varies in thickness in different sections, but we believe that the glomerulus is continued unbroken throughout the very considerable region through which it extends. This point is, however, difficult to. .make sure of owing to the facility with which the glomerulus breaks away.
At the stage we are describing, no true Malpighian bodies are present in the part of the Wolffian body on the same level with the anterior end of the glomerulus, but the Wolffian body merely consists of the Wolffian duct. At the level of the posterior part of the glomerulus this is no longer the case, but here a regular series of primary Malpighian bodies is present (using the term "primary" to denote the Malpighian bodies developed directly out of part of the primary segmental tubes), and the glomerulus of the head-kidney may frequently be seen in the same section as a Malpighian body. In most sections the two bodies appear quite disconnected, but in those sections in which the glomernlns of the Malpighian body comes into view it is seen to be derived from the same formation as the glomerulus of the head-kidney (PI. 28, fig. F). It would seem, in fact, that the vascular tissue of the glomerulus of the head-kidney grows into the concavity of the Malpighian bodies. Owing to the stage we are now describing, in which we have found the glomerulus most fully developed, being prior to that in which the head-kidney appears, it is not possible to determine with certainty the position of the glomerulus in relation to the headkidney. After the development of the head-kidney it is" found, however, as we have already stated, that the glomerulus terminates at a point just in front of the anterior opening of the head-kidney. It is less developed than before, but is still present up to the period of the atrophy of the head-kidney. It does not apparently alter in constitution, and we have not thought it worth while giving any further representations of it during the later stages of its existence.
-Summary of the development of the head-kidney and glomertilus. The first rudiment of the head-kidney arises as three successive grooves in the thickened germinal epithelium, connected by ridges, and situated some way behind the front end of the Wolffian duct. In the next stage the three ridges connecting the grooves have become more marked, and in each of them a lumen has appeared, opening at both extremities into the adjoining grooves. Still later the ridges become more or less completely detached from the peritoneal epithelium, and the whole head-kidney then consists of a slightly convoluted duct, with, at the least, three peritoneal openings, which is posteriorly continued into the Miillerian duct. Still later the headkidney atrophies, its two posterior openings vanishing, and its anterior opening remaining as the permanent opening of the Miillerian duct. The glomerulus arises as a vascular prominence at the root of the mesentery, slightly prior in point of time to the head-kidney, and slightly more forward than it in position. We have not traced its atrophy.
We stated in our preliminary paper that the peculiar structures we had interpreted as the head-kidney had completely escaped the attention of previous observers, though we called attention to a well-known figure of Waldeyer's (copied in the Elements of Embryology, fig. 5 1 )- ^ n this figure a connection between the germinal epithelium and the Mulleriari duct is drawn, which is probably part of the head-kidney, and may be compared with our figures (Series B, No. 8, and Series D, No. 4). Since we made the above statement, Dr Gasser has called our attention to a passage in his valuable memoir on " The Development of the Allan tois 1 ," in which certain structures are described which are, perhaps, identical with our head-kidney. The following is a translation of the passage :
"In the upper region of Muller's duct I have often observed small canals, especially in the later stages of development, which appear as a kind of doubling of the duct; and run for a short distance close to Miiller's duct and in the same direction, opening, however, into the body-cavity posterior to the main duct. Further, one may often observe diverticula from the extreme anterior end of the oviduct of the bird, which form blind pouches and give one the impression of being receptacula seminis. Both these appearances can quite well be accounted for on the supposition that an abnormal communication is effected between the germinal epithelium and Miiller's duct at unusual places; or else that an attempt at such a communication is made, resulting, however, only in the formation of a diverticulum of the wall of the oviduct."
1 Beitrdge zur Entwickelungsgeschichte d. Allantois der Miiller'schen Gange u. des Afters. Frankfurt, 1874.
The statement that these accessory canals are late in developing, prevents us from feeling quite confident that they really correspond with our head-kidney.
Before passing on to the other parts of this paper it is necessary to say a few words in justification of the comparison we have made between the modified abdominal extremity of the Mullerian duct in the chick and the head-kidney of the Ichthyopsida.
For the fullest statement of what is known with reference to the anatomy and development of the head-kidney in the lower types we may refer to Spengel and Furbringer 1 . We propose ourselves merely giving a sufficient account of the head-kidney in Amphibia (which appears to be the type in which the headkidney can be most advantageously compared with that in the bird) to bring out the grounds for our determination of the homologies.
The development of the head-kidney in Amphibia has been fully elucidated by the researches of W. Miiller 2 , Gotte 8 , and FUrbringer*, while to the latter we are indebted for a knowledge of the development of the Mullerian duct in Amphibians. The first part of the urino-genital system to develop is the segmental duct ( Vornieregang of Furbringer), which is formed by a groovelike invagination of the peritoneal epithelium. It becomes constricted into a duct first of all in the middle, but soon in the posterior part also. It then forms a duct, ending in front by a groove in free communication with the body-cavity, and terminating blindly behind. The open groove in front at first deepens, and then becomes partially constricted into a duct, which elongates and becomes convoluted, but remains in communication with the body-cavity by from two to four (according to the species) separate openings. The manner in which the primitive single opening is related to the secondary openings is not fully understood. By these changes there is formed out of the primitive groove an anterior glandular body, communicating with the body-cavity by several apertures, and a posterior duct, which carries off the secretion of the gland, and which, though blind at first, eventually opens into the cloaca. In addition to these parts there is also formed on each side of the mesentery, opposite the peritoneal openings, a very vascular projection into this part of the body-cavity, which is known as the glomerulus of the head-kidney, and which very closely resembles in structure and position the body to which we have assigned the same name in the chick.
1 Loc. cit.
2 Jenaische Zeitschrift', Vol. IX. 1875.
3 Entwickelungsgeschichte d. Unke.
4 Loc. cit.
The primitive segmental duct is at first only the duct for the head-kidney, but on the formation of the posterior parts of the kidney (Wolffian body, &c.) it becomes the duct for these also.
After the Wolffian bodies have attained to a considerable development, the head-kidney undergoes atrophy, and its peritoneal openings become successively closed from before backwards. At this period the formation of the Miillerian duct takes place. It is a solid constriction of the ventral or lateral wall of the segmental duct, which subsequently becomes hollow, and acquires an opening into the body-cavity quite independent of the openings of the head-kidney.
The similarity in development and structure between the head-kidney in Amphibia and the body we have identified as such in Aves, is to our minds too striking to be denied. Both consist of two .parts (i) a somewhat convoluted longitudinal canal, with a certain number of peritoneal openings; (2) a vascular prominence at the root of the mesentery, which forms a glomerulus. As to the identity in position of the two organs we hope to deal with that more fully in speaking of the general
628 EXISTENCE OF A HEAD-KIDNEY
structure of the excretory system, but may say that one of us 1 has already, on other grounds, attempted to shew that the abdominal opening of the MUllerian duct in the bird is the homologue of the abdominal opening of the segmental duct in Amphibia, Elasmobranchii, &c., and that we believe that this homology will be admitted by most anatomists. If this homology is admitted, the identity in position of this organ in Aves and Amphibia necessarily follows. The most striking difference between Aves and Amphibia in relation to these structures is the fact that in Aves the anterior pore of the head-kidney remains as the permanent opening of the Mullerian duct, while in Amphibia, the pores of the head-kidney atrophy, and an entirely fresh abdominal opening is formed for the Mullerian duct.
The Growth of the Mullerian Duct.
Although a great variety of views have been expressed by different observers on the growth of the Mullerian duct, it is now fairly generally admitted that it grows in the space between a portion of the thickened germinal epithelium and the Wolffian duct, but quite independently of both of them. Both Braun and Egli, who have specially directed their attention to this point, have for Reptilia and Mammalia fully confirmed the views of previous observers. We were, nevertheless, induced, partly -on account of the a priori difficulties of this view, and partly by certain peculiar appearances which we observed, to undertake the re-examination of this point, and have- found ourselves unable altogether to accept the general account. We propose first describing, in as matter-of-fact a way as possible, the actual observations we have made, and then stating what conclusions we think may be drawn from these observations.
We have found it necessary to distinguish three stages in the growth of the Mullerian duct. Our first stage embraces the
1 Balfour, "Origin and History of Urinogenital Organs of Vertebrates," Journal of Anat. and Phys. Vol. X., and Monograph on Elasmobranch Fishes. [This edition Nos. vii. and x.]
IN THE EMBRYO CHICK. 629
period prior to the disappearance of the head-kidney. At this stage the structure we have already spoken of as the rudiment of the Mullerian duct consists of a solid rod of cells, continuous with the third groove of the head-kidney. It extends through a very few sections, and terminates by a fine point of about two cells, wedged in between the Wolffian duct and germinal epithelium (described above, Nos. 7 10, series A, Plate 27).
In an embryo slightly older than the above, such as that from which series B was taken, but still belonging to our first stage, a definite lumen appears in the anterior part of the Mullerian duct, which vanishes after a few sections, "The duct terminates in a point which lies in a concavity of the wall of the Wolffian duct (Plate 27, Nos. I and 2, series G). The limits of the Wolffian wall and the pointed termination of the Mullerian duct are in many instances quite distinct ; but the outline of the Wolffian duct appears to be carried round the Mullerian duct, and in some instances the terminal point of the Mullerian duct seems almost to form an integral part of the wall of the Wolffian duct.
The second of our stages corresponds with that in which the atrophy of the head-kidney is nearly complete (series D and H, Plate 28).
The Miillerian duct has by this stage made a very marked progress in its growth towards the cloaca, and, in contradistinction to the earlier stage, a lumen is now continued close up to the terminal point of the duct. In the two or three sections before it ends it appears as a distinct oval mass of cells (No. 10, series D, and No. i, series H), without a lumen, lying between and touching the external wall of the Wolffian duct on the one hand, and the germinal epithelium on the other. It may either lie on the ventral side of the Wolffian duct (series D), or on the outer side (series H), but in either case is opposite the maximum thickening of that part of the germinal epithelium which always accompanies the Mullerian duct in its backward growth.
In the last section in which any trace of the Mullerian duct can be made out (series D, No. 1 1, and series H, No. 2), it has no longer an oval, well-defined contour, but appears to have completely fused with the wall of the Wolffian duct, which is accordingly very thick, and occupies the space which in the previous
630 EXISTENCE OF A HEAD-KIDNEY
section was filled by its own wall and the Miillerian duct. In the following section the thickening in the wall of the Wolffian duct has disappeared (Plate 28, series H, No. 3), and every trace of the Miillerian duct has vanished from view. The Wolffian duct is on one side in contact with the germinal epithelium.
The stage during which the condition above described lasts is not of long duration, but is soon succeeded by our third stage, in which a fresh mode of termination of the Miillerian duct is found. (Plate 28, series I.) This last stage remains up to about the close of the sixth day, beyond which our investigations do not extend.
A typical series of sections through the terminal part of the Mullerian duct at this stage presents the following features:
A few sections before its termination the Miillerian duct appears as a well-defined oval duct lying in contact with the wall of the Wolffian duct on the one hand and the germinal epithelium on the other (series I, No. i). Gradually, however, as we pass backwards, the Miillerian duct dilates ; the external wall of the Wolffian duct adjoining it becomes greatly thickened and pushed in in its middle part, so as almost to touch the opposite wall of the duct, and so form a bay in which the Miillerian duct lies (Plate 28, series I, Nos. 2 and 3). As soon as the Miillerian duct has come to lie in this bay its walls lose their previous distinctness of outline, and the cells composing them assume a curious vacuolated appearance. No well-defined line of separation can any longer be traced between the walls of the Wolffian duct and those of the Miillerian, but between the two is a narrow clear space traversed by an irregular network of fibres, in some of the meshes of which nuclei are present.
The Miillerian duct may be traced in this condition for a considerable number of sections, the peculiar features above described becoming more and more marked as its termination is approached. It continues to dilate and attains a maximum size in the section or so before it disappears. A lumen may be observed in it up to its very end, but is usually irregular in outline and frequently traversed by strands of protoplasm. The Mullerian duct finally terminates quite suddenly (Plate 28, series I, No. 4), and in the section immediately behind its termination the Wolffian duct assumes its normal appearance, and the part of
IN THE EMBRYO CHICK. 63!
its outer wall on the level of the Mullerian duct comes into contact with the germinal epithelium (Plate 28, series I, No. 5).
We have traced the growing point of the Miillerian duct with the above features till not far from the cloaca, but we have not followed the last phases of its growth and its final opening into the cloaca.
In some of our embryos we have noticed certain rather peculiar structures, an example of which is represented at y in fig. K, taken from an embryo of 123 hours, in which all traces of the head-kidney had disappeared. It consists of a cord of cells, connecting the Wolffian duct and the hind end of the abdominal opening of the Miillerian duct. At the least one similar cord was met with in the same embryo, situated just behind the abdominal opening of the Miillerian duct. We have found similar structures in other embryos of about the same age, though never so well marked as in the embryo from which fig. K is taken. We have quite failed to make out the meaning, if any, of them.
Our interpretation of the appearances we have described in connection with the growth of the Miillerian duct can be stated in a very few words. Our second stage, where the solid point of the Miillerian duct terminates by fusing with the walls of the Wolffian duct, we interpret as meaning that the Miillerian is growing backwards as a solid rod of cells, split off from the outer wall of the Wolffian duct; in the same manner, in fact, as in Amphibia and Elasmobranchii. The condition of the terminal part of the Miillerian duct during our third stage cannot, we think, be interpreted in the same way, but the peculiarities of the cells of both Mullerian and Wolffian ducts, and the indistinctness of the outlines between them, appear to indicate that the Mullerian duct grows by cells passing from the Wolffian duct to it. In fact, although in a certain sense the growth of the two ducts is independent, yet the actual cells which assist in the growth of the Mullerian duct are, we believe, derived from the walls of the Wolffian duct.
632 EXISTENCE OF A HEAD-KIDNEY
The excretory system of a typical Vertebrate consists of the following parts:
1. A head-kidney with the characters already described, rj
2. A duct for the head-kidney the segmental duct.
3. A posterior kidney (Wolffian body, permanent kidney, &c. The nature and relation, of these parts we leave out of consideration, as they have no bearing upon our present investiga-r tions). The primitive duct for the Wolffian body is the segmental duct.
4. The segmental duct may become split into (a) a dorsal or inner duct, which serves as ureter (in the widest sense of the word); and (#) a ventral or outer duct, which has an opening into the body-cavity, and serves as the generative duct for the female, or for both sexes.
These parts exhibit considerable variations both in their structure and development, into some of which it is necessary for us to enter.
The head-kidney 1 attains to its highest development in the Marsipobranchii (Myxine, Bdellostoma). It consists of a, longitudinal canal, from the ventral side of which numerous tubules ' pass. These tubules, after considerable subdivision, open by a large number of apertures into the pericardial cavity. From the longitudinal canal a few dorsal diverticula, provided with glomeruli, are given off. In the young the longitudinal canal is continued into the segmental duct ; but this connection becomes
1 I am inclined to give up the view I formerly expressed with reference to the head-kidney and segmental duct, viz. " that they were to be regarded as the most anterior segmental tube, the peritoneal opening of which had become divided, and which had become prolonged backwards so as to serve as the duct for the posterior segmental tubes," and provisionally to accept the Gegenbaur-Fiirbringer view which has been fully worked out and ably argued for by Fiirbringer (loc. cit. p. 96). According to this view the head-kidney and its duct are to be looked on as the primitive and unsegmented part of the excretory system, more or less similar to the excretory system of many Trematodes and unsegmented Vermes. The segmental tubes I regard as a truly segmental part of the excretory system acquired subsequently. F. M. B.
IN THE EMBRYO CHICK. 633
lost in the adult. The head-kidney remains, however, through life. In Teleostei and Ganoidei (?) the head-kidney is generally believed to remain through life, as the dilated cephalic portion of the kidneys when such is present. In Petr.omyzon and Amphibia the head-kidney atrophies. In Elasmobranchii the headkidney, so far as is known, is absent.
The development of the segmental duct and head-kidney (when present) is still more important for our purpose than their adult structure.
In Myxine the development of these structures is not known. In Amphibia and Teleostei it takes place upon the same type, viz. by the conversion of a groove-like invagination of the peri^ toneal epithelium into a canal open in front. The head-kidney is developed from the anterior end of this canal, the opening of which remains in Teleostei single and closes early in embryonic life, but becomes in Amphibia divided into two, three, or four openings. In Elasmobranchii the development is very different.
" The first trace of the urinary system makes its appearance as a knob springing from the intermediate cell-mass opposite the fifth proto-vertebra. This knob is the rudiment of the abdominal opening of the segmental duct, and from it there grows backwards to the level of the anus a solid column of cells, which constitutes the rudiment of the segmental duct itself. The knob projects towards the epiblast, and the column connected with it lies between the mesoblast and epiblast. The knob and column do not long remain solid, but the former acquires an opening into the body-cavity continuous with a lumen, which makes its appearance in the latter."
The difference in the development of the segmental duct in the two types (Amphibia and Elasmobranchii) is very important. In the one case a continuous groove of the peritoneal epithelium becomes constricted into a canal, in the other a solid knob of cells is continued into a rod, at first solid, which grows backwards without any apparent relation to the peritoneal epithelium 1 .
1 In a note on p. 50 of his memoir Fiirbringer criticises my description of the mode of growth of the segmental duct. The following is a free translation of what he says : " In Balfour's, as in other descriptions, an account is given of a backward
634 EXISTENCE OF A HEAD-KIDNEY
The abdominal aperture of the segmental duct in Elasmobranchii, in that it becomes the permanent abdominal opening of the oviduct, corresponds physiologically rather with the abdominal opening of the Miillerian duct than with that of the segmental duct of Amphibia, which, after becoming divided up to form the pores of the head-kidney, undergoes atrophy. Morphologically, however, it appears to correspond with the opening of the segmental duct in Amphibia. We shall allude to this point more than once again, and give our grounds for the above view on p. 640.
The development of the segmental duct in .Elasmobranchii as a solid rod is, we hope to shew, of special importance for the elucidation of the excretory system of Aves.
The development of these parts of Petromyzon is not fully known, but from W. Muller's account (Jenaische Zeitschrift, 1875) it would seem that an anterior invagination of the peritoneal epithelium is continued backwards as a duct (segmental duct), and that the anterior opening subsequently becomes divided up into the various apertures of the head-kidney. If this account is correct, Petromyzon presents a type intermediate between Amphibia and Elasmobranchii. In certain types, viz. Marsipobranchii and Teleostei, the segmental duct becomes the duct for the posterior kidney (segmental tubes), but otherwise undergoes no further differentiation. In the majority of types,
growth, which easily leads to the supposition of a structure formed anteriorly forcing its way through the tissues behind. This is, however, not the case, since, to my knowledge, no author has ever detected a sharp boundary between the growing point of the segmental duct (or Miillerian duct) and the surrounding tissues." He goes on to say that " the growth in these cases really takes place by a differentiation of tissue along a line in the region of the peritoneal cavity." Although I fully admit that it would be far easier to homologise the development of the segmental duct in Amphibia and Elasmobranchii according to this view, I must nevertheless vindicate the accuracy of my original account. I have looked over my specimens again, since the appearance of Dr Furbringer's paper, and can find no evidence of the end of the duct becoming continuous with the adjoining mesoblastic tissues. In the section, before its disappearance, the segmental duct may, so far as I can make out, be seen as a very small but distinct rod, which is much more closely connected with the epiblast than with any other layer. From Gasser's observations on the Wolman duct in the bird, I am led to conclude that it behaves in the same way as the segmental duct in the Elasmobranchii. I will not deny that it is possible that the growth of the duct takes place by wandering cells, but on this point I have no evidence, and must therefore leave the question an open one. F. M. B.
IN THE EMBRYO CHICK. 635
however, the case is different. In Amphibia 1 , as has already been mentioned, a solid rod of cells is split off from its ventral wall, which afterwards becomes hollow, acquires an opening into the body-cavity, and forms the Mullerian duct.
In Elasmobranchii the segmental duct undergoes a more or less similar division. " It becomes longitudinally split into two complete ducts in the female, and one complete duct and parts of a second in the male. The resulting ducts are (i) the Wolffian duct dorsally, which remains continuous with the excretory tubules of the kidney, and ventrally (2) the oviduct or Mullerian duct in the female, and the rudiments of this duct in the male. In the female the formation of these ducts takes place by a nearly solid rod of cells, being gradually split off from the ventral side of all but the foremost part of the original segmental duct, with the short undivided anterior part of which duct it is continuous in front. Into it a very small portion of the lumen of the original segmental duct is perhaps continued. The remainder of the segmental duct (after the loss of its anterior section and the part split off from its ventral side) forms the Wolffian duct. The process of formation of the ducts in the male chiefly differs from that in the female, in the fact of the anterior undivided part of the segmental duct, which forms the front end of the Mullerian duct, being shorter, and in the column of cells with which it is continuous being from the first incomplete."
It will be seen from the above that the Mullerian duct con'sists of two distinct parts an anterior part with the abdominal opening, and a posterior part split off from the segmental duct. This double constitution of the Mullerian duct is of great importance for a proper understanding of what takes place in the Bird.
The Mullerian duct appears therefore to develop in nearly the same manner in the Amphibian and Elasmobranch type, as a solid or nearly solid rod split off from the ventral wall of the segmental duct. But there is one important difference concerning the abdominal opening of the duct. In Amphibia this is a new formation, but in Elasmobranchii it is the original opening of the segmental duct. Although we admit that in a large
1 Fiirbringer, loc. cit.
636 EXISTENCE OF A HEAD-KIDNEY
number of points, including the presence of a head-kidney, the urinq-genital organs of Amphibia are formed on a lower type than those of the Elasmobranchii, yet it appears to us that this does not hold good for the development of the Mullerian duct.
The above description will, we trust, be sufficient to render clear our views upon the development of the excretory system in Aves.
In the bird the excretory system consists of the following parts (using the ordinary nomenclature) which are developed in the order below.
I. Wolffian duct. 2. Wolffian body. 3. Head-kidney. 4. Mullerian duct. 5. Permanent kidney and ureter.
About 2 and 5 we shall have nothing to say in the sequel.
We have already in the early part of the paper given an account of the head-kidney and Mullerian duct, but it will be necessary for us to say a few words about the development of the Wolffian duct (so called). Without entering into the somewhat extended literature on the subject, we may state that we consider that the recent paper of Dr Gasser 1 supplies us with the best extant account of the development of the Wolffian duct.
The first trace of it, which he finds, is visible in an embryo with eight proto-vertebrae as a slight projection from the intermediate cell mass towards the epiblast in the region of the three hindermost proto-vertebrae. In the next stage, with eleven proto-vertebrae, the solid rudiment of the duct extends from the fifth to the eleventh proto- vertebra, from the eighth to the eleventh proto-vertebra it lies between the epiblast and mesoblast, and is quite distinct from both, and Dr Gasser distinctly states that in its growth backwards from the eighth protovertebra the Wolffian duct never comes into continuity with the adjacent layers.
In the region of the fifth proto-vertebra, where the duct was originally continuous with the mesoblast, it has now become free, but is still attached in the region of the sixth and to the eighth proto-vertebra. In an embryo with fourteen proto-vertebrae the duct extends from the fourth to the fourteenth protovertebra, and is now free between epiblast and mesoblast for its whole extent. It is still for the most part solid though perhaps
1 Arc h. fur Mic. Anat. Vol. XIV.
IN THE EMBRYO CHICK. 637
a small lumen is present in its middle part. In the succeeding stages the lumen of the duct gradually extends backwards and forwards, the duct itself also passes inwards till it acquires its final position close' to the peritoneal epithelium ; at the same time its hind end elongates till it comes into connection with the cloacal section of the hind-gut. It should be noted that the duct in its backward growth does not appear to come into continuity with the subjacent mesoblast, but behaves in this respect exactly as does the segmental duct in Elasmobranchii (vide note on p. 634).
The question which we propose to ourselves is the following : What are the homologies of the parts of the Avian urinogenital system above enumerated ? The Wolffian duct appears to us morphologically to correspond in part to the segmental duct 1 , or what Furbringer would call the duct of the head-kidney. This may seem a paradox, since in birds it never comes into relation with the head-kidney. Nevertheless we consider that this homology is morphologically established, for the following reasons :
(1) That the Wolffian duct gives rise (vide supra, p. 631) to the Mullerian duct as well as to the duct of the Wolffian body. In this respect it behaves precisely as does the segmental duct of Elasmobranchii and Amphibia. That it serves as the duct for the Wolffian body, before the Mullerian duct originates from it, is also in accordance with what takes place in other types.
(2) That it develops in a strikingly similar manner to the segmental duct of Elasmobranchii.
We stated expressly that the Wolffian duct corresponded only in part to the segmental duct. It does not, in fact, in our opinion, correspond to the whole segmental duct, but to the segmental duct minus the anterior abdominal opening in Elasmobranchii, which becomes the head-kidney in other types. In fact, we suppose that the segmental duct and head-kidney, which
1 The views here expressed about the Wolffian duct are nearly though not exactly those which one of us previously put forward (" Urinogenital Organs of Vertebrates," &c., pp. 45 46) [This edition, pp. 164, 165], and with which Furbringer appears exactly to agree. Possibly Dr Furbringer would alter his view on this point were he to accept the facts we believe ourselves to have discovered. Semper's view also differs from ours, in that he believes the Wolffian duct to correspond in its entirety with the segmental duct.
638 EXISTENCE OF A HEAD-KIDNEY
in the Ichthyopsida develop as a single formation, develop in the Bird as two distinct structures one of these known as the Wolffian duct, and the other the head*kidney. If our view about the head-kidney is accepted the above position will hardly require to be disputed, but we may point out that the only feature in which the Wolffian duct of the Bird differs in development from the segmental duct of Elasmobranchii is in the absence of the knob, which forms the commencement of the segmental duct, and in which the abdominal opening is formed; so that the comparison of the development of the duct in the two types confirms the view arrived at from other considerations.
The head-kidney and Mullerian duct in the Bird must be considered together. The parts which they eventually give rise to after the atrophy of the head-kidney have almost universally been regarded as equivalent to the Mullerian duct of the Ichthyopsida. By Braun 1 , however, who from his researches on the Lizard satisfied himself of the entire independence of the Mullerian and Wolffian ducts in the Amniota, the Mullerian duct of these forms is regarded as a completely new structure with no genetic relations to the Mullerian duct of the Ichthyopsida. Semper 2 , on the other hand, though he accepts the homology of the Mullerian duct iri the Ichthyopsida and Amniota, is of opinion that the anterior part of the Mullerian duct in the Amniota is really derived from the Wolffian duct, though he apparently admits the independent growth of the posterior part of the Mullerian duct. We have been led by our observations, as well as by our theoretical deductions, to adopt a view exactly the reverse of that of Professor Semper. We believe that the anterior part of the Mullerian duct of Aves, which is at first the head-kidney, and subsequently becomes the abdominal opening of the duct, is developed from the peritoneal epithelium independently of all other parts of the excretory system ; but that the posterior part of the duct is more or less completely derived from the walls of the Wolffian duct. This view is clearly in accordance with our account of the facts of development in Aves, and it fits in very well with the development of the Mullerian
1 " Urogenital-System d. Reptilien," Arb. aits d. zool,-zoot. Inst. Wurzburg, Vol. IV.
1 Lof. fit.
IN THE EMBRYO CHICK. 639
duct in Elasmobranchii. We have already pointed out that in Elasmobranchii the Miillerian duct is formed of two factors (i) of the whole anterior extremity of the segmental duct, including its abdominal opening ; (2) of a rod split off from the ventral side of the segmental duct. In Birds the anterior part (corresponding to factor No. i) of the Miillerian duct has a different origin from the remainder ; so that if the development of the posterior part of the duct (factor No. 2) were to proceed in the same manner in Birds and Elasmobranchii, it ought to be formed at the expense of the Wolffian (i.e. segmental) duct, though in connection anteriorly with the head-kidney. And this is what actually appears to take place.
So far the homologies of the avian excretory system are fairly clear; but there are still some points which have to be dealt with in connection with the permanent opening of the Miillerian duct, and the relatively posterior position of the headkidney. With reference to the first of these points the facts of the case are the following :
In Amphibia the permanent opening of the Mullerian duct is formed as an independent opening after the atrophy of the head-kidney.
In Elasmobranchii the original opening of the segmental duct forms the permanent opening of the Mullerian duct and no head-kidney appears to be formed.
In Birds the anterior of the three openings of the head-kidney remains as the permanent opening of the Miillerian duct.
With reference to the difficulties involved in there being apparently three different modes in which the permanent opening of the Mullerian duct is formed, we would suggest the following considerations:
The history of the development of the excretory system teaches us that primitively the segmental duct must have served as efferent duct both for the generative products and kidney secretion (just as the Wolffian duct still does for the testicular products and secretion of the Wolffian body in Elasmobranchii and Amphibia) ; and further, that at first the generative products entered the segmental duct from the abdominal cavity by one or more of the abdominal openings of the kidney (almost certainly of the head-kidney). That the generative products did
640 EXISTENCE OF A HEAD-KIDNEY
not enter the segmental duct at first by an opening specially developed for them appears to us to follow from Dohrn's principle of the transmutation of function (Functionswec/isel). As a consequence (by a process of natural selection) of the segmental duct having both a generative and a urinary function, a further differentiation took place, by which that duct became split into two a ventral Miillerian duct and dorsal Wolffian duct.
The Miillerian duct without doubt was continuous with the head-kidney, and so with the abdominal opening or openings of the head-kidney which served as generative pores. At first the segmental duct was probably split longitudinally into two equal portions, but the generative function of the Miillerian duct gradually impressed itself more and more upon the embryonic development, so that, in the course of time, the Miillerian duct developed less and less at the expense of the Wolffian duct. This process appears partly to have taken place in Elasmobranchii, and still more in Amphibia ; the Amphibia offering in this respect a less primitive condition than Elasmobranchii ; while in Aves it has been carried even further. The abdominal opening no doubt also became specialised. At first it is quite possible that more than one abdominal pore may have served for the generative products ; one of which, no doubt, eventually came to function alone. In Amphibia the specialisation of the opening appears to have gone so far that it no longer has any relation to the head-kidney, and even develops after the atrophy of the head-kidney. In Elasmobranchii, on the other hand, the functional opening appears at a period when we should expect the head-kidney to develop. This state is very possibly the result of a differentiation (along a different line to that in Amphibia) by which the head-kidney gradually ceased to become developed, but by which the primitive opening (which in the development of the head-kidney used to be divided into several pores leading into the body-cavity) remained undivided and served as the abdominal aperture of the Miillerian duct. Aves, finally, appear to have become differentiated along a third line ; since in their ancestors the anterior pore of the head-kidney appears to have become specialised as the permanent opening of the Miillerian duct.
With reference to the posterior position of the head-kidney
IN THE EMBRYO CHICK. 641
in Aves we have only to remark, that a change in position of the head-kidney might easily take place after it acquired an independent development. The fact that it is slightly behind the glomerulus would seem to indicate, on the one hand, that it has already ceased to be of any functional importance ; and, on the other, that the shifting has been due to its having a connection with the Mullerian duct.
We have made a few observations on the development of the Miillerian duct in Lacerta muralis, which have unfortunately led us to no decided conclusions. In a fairly young stage in the development of the , Mullerian duct (the youngest we have met with), no trace of a head-kidney could be observed, but the character of the abdominal opening of the Miillerian duct was very similar to that figured by Braun 1 . As to the backward growth of the Mullerian duct, we can only state that the solid point of the duct in the young stages is in contact with the wall of the Wolffian duct, and the relation between the two is rather like that figured by Fiirbringer (PI. I, figs. 14 15) in Amphibia.
DESCRIPTION OF PLATES 27 AND 28.
COMPLETE LIST of REFERENCE LETTERS.
ao. Aorta, cv. Cardinal vein. gl. Glomerulus. gr r First groove of headkidney, gr^. Second groove of head-kidney. gr 3 . Third groove of head-kidney. ge. Germinal epithelium, mrb. Malpighian body. me. Mesentery, m d. Miillerian duct. r r First ridge of head-kidney, r 3 . Second ridge of head-kidney. r s . Third ridge of head-kidney. W d. Wolffian duct. x. Fold in germinal epithelium.
SERIES A. Sections through the head-kidney at our second stage. Zeiss 2, ocul. 3 (reduced one-third). The second and third grooves are represented with the ridge connecting them, and the- rod of cells running backwards for a short distance.
No. i. Section'through the second groove.
No. i. Section through the ridge connecting the second and third grooves. No. 3. Section passing through the same ridge at a point nearer the third groove. Nos. 4, 5,6. Sections through the third groove.
No. 7. Section through the point where the third groove passes into the solid rod of cells.
1 Loc. cit.
642 EXISTENCE OF HEAD-KIDNEY IN EMBRYO-CHICK.
No. 8. Section through the rod when quite separated from the germinal epithelium.
No. 9. Section very near the termination of the rod.
No. 10. Last section in which any trace of the rod is seen.
SERIES B. Sections passing through the head-kidney at our third stage. Zeiss C, ocul. 2. Our figures are representations of the following sections of the series, section i being the first which passes through the anterior groove of the head-kidney.
No. i SECTION
8. 10. n.
No. 8 ............... SECTION 13.
10 ............... 16.
The Miillerian duct extends through eleven more sections. The first groove (gr. ) extends to No. 3. The second groove (^r 2 .) extends from No. 4 to No. 7. The third groove (gr y ) extends from No. 11 to No. 13. The first ridge (r^.) extends from No. 2 to No. 5. The second ridge (r 2 .) extends from No. 8 to No. u.
The third ridge (r y ) extends from No. 13 backwards through twelve sections, when it terminates by a pointed extremity.
FIG. C. Section through the ridge connecting the second and third grooves of the head-kidney of an embryo slightly younger than that from which Series B was taken. Zeiss C, ocul. 3 (reduced one-third).
The fold of the germinal epithelium, which gives rise to a deep groove (x.) external to the head-kidney is well marked.
SERIES G. Sections through the rod of cells constituting the termination of the Mullerian duct at a stage in which the head-kidney is still present. Zeiss C, ocul. 2.
SERIES D. Sections chosen at intervals from a complete series traversing the peritoneal opening of the Mullerian duct, the remnant of the head-kidney, and the termination of the Mullerian duct. Zeiss C, ocul. 3 (reduced one-third).
Nos. i and 2. Sections through the persistent anterior opening of the headkidney (abdominal opening of Mullerian duct). The approach of the Wolffian duct to the groove may be seen by a comparison of these two figures. In the sections in front of these (not figured) the two are much more widely separated than in No. t.
No. 3. Section through the Mullerian duct, just posterior to the persistent opening.
Nos. 4 and 5. Remains of the ridges, which at an earlier stage connected the first and second grooves, are seen passing from the Mullerian duct to the peritoneal epithelium.
No. 6. Rudiment of the second groove (gr z .) of the head-kidney.
Between 6 and 7 is a considerable interval.
No. 7. All traces of this groove (gr y ) have vanished, and the Miillerian duct is quite disconnected from the epithelium.
DESCRIPTION OF PLATES 2J AND 28. 643
No. 8. Rudiment of the third groove (gr y ).
No. 9. Miillerian duct quite free in the space between the peritoneal epithelium and the Wolfflan duct, in which condition it extends until near its termination.
Between Nos. 9 and lo is an interval of eight sections.
No. 10. The penultimate section, in which the Miillerian duct is seen. A lumen cannot be clearly made out.
No. ii. The last section in which any trace of the Miillerian duct is visible. No line of demarcation can be seen separating the solid end of the Miillerian duct from the ventral wall of the Wolffian duct.
FIGS. E. and F. Sections through the glomerulus of the head-kidney from an embryo prior to the appearance of the head-kidney. Zeiss B, ocul. 2. A comparison of the two figures shows the variation in the thickness of the stalk of the glomerulus. E. Section anterior to the foremost Malpighian body. F. Section through both the glomerulus of the head-kidney and that of a Malpighian body. The two are seen to be connected.
SERIES H. Consecutive sections through the hind end of the Miillerian duct, from an embryo in which the head-kidney Was only represented by a rudiment. (The embryo was, perhaps, very slightly older than that from which Series D was taken.) Zeiss C, ocul. 3 (reduced oneMhird).
No. i. Miillerian duct is without a lumen, and quite distinct from- the Wolffian wall.
No. 2. The solid end of the Miillerian duct is no longer distinct from the internal wall of the Wolffian duct.
No. 3. All trace of the Miillerian duct has vanished.
SERIES i. Sections through the hinder end of the Miillerian duct from an embryo of about the middle of the sixth day. Zeiss C, ocul. 2 (reduced one-third).
No. i. The Miillerian duct is distinct and small.
No. 2. Is posterior by twelve sections to No. I. The Miillerian duct is dilated, and its cells are vaCuolated.
No. 3. Penultimate section, in which the Miillerian duct is visible ; it is separated by three sections from No. 2.
No. 4. Last section in which any trace of the Miillerian duct is visible ; the lumen, which was visible in the previous section, is now absent.
No. 5. No trace of Miillerian duct. Nos. 3, 4, and 5 are consecutive sections.
FIG. K. Section through the hind end of the abdominal opening of the Miillerian duct of a chick of 123 hours. Zeiss C, ocul. 2 (reduced one-third). It illustrates the peculiar cord connecting the Miillerian and Wolffian ducts.