The Works of Francis Balfour 3-10

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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.

Cephalochorda | Urochorda | Elasmobranchii | Teleostei | Cyclostomata | Ganoidei | Amphibia | Aves | Reptilia | Mammalia | Comparison of the Formation of Germinal Layers and Early Stages in Vertebrate Development | Ancestral form of the Chordata | General Conclusions | Epidermis and Derivatives | The Nervous System | Organs of Vision | Auditory, Olfactory, and Lateral Line Sense Organs | Notochord, Vertebral Column, Ribs, and Sternum | The Skull | Pectoral and Pelvic Girdles and Limb Skeleton | Body Cavity, Vascular System and Glands | The Muscular System | Excretory Organs | Generative Organs and Genital Ducts | The Alimentary Canal and Appendages in Chordata
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This historic 1885 book edited by Foster and Sedgwick is the third of Francis Balfour's collected works published in four editions. Francis (Frank) Maitland Balfour, known as F. M. Balfour, (November 10, 1851 - July 19, 1882) was a British biologist who co-authored embryology textbooks.



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.
Modern Notes:

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)


Draft Version - Notice removed when completed.

Vol. III. A Treatise on Comparative Embryology 2 (1885)

CHAPTER X. MAMMALIA

THE classical researches of Bischoff on the embryology of several mammalian types, as well as those of other observers, have made us acquainted with the general form of the embryos of the Placentalia, and have shewn that, except in the earliest stages of development, there is a close agreement between them. More recently Hensen, Schafer, Kolliker, Van Beneden and Lieberkiihn have shed a large amount of light on the obscurer points of the earliest developmental periods, especially in the rabbit. For the early stages the rabbit necessarily serves as type; but there are grounds for thinking that not inconsiderable variations are likely to be met with in other species, and it is not at present easy to assign to some of the developmental features their true value. We have no knowledge of the early development of the Ornithodelphia or Marsupialia.

The ovum on leaving the ovary is received by the fimbriated extremity of the Fallopian tube, down which it slowly travels. It is still invested by the zona radiata, and in the rabbit an albuminous envelope is formed around it in its passage downwards. Impregnation takes place in the upper part of the Fallopian tube, and is shortly followed by the segmentation, which is remarkable amongst the Amniota for being complete.

Although this process (the details of which have been made known by the brilliant researches of Ed. van Beneden) has already been shortly dealt with as it occurs in the rabbit (Vol. II. p. 98) it will be convenient to describe it again with somewhat greater detail.

The ovum first divides into two nearly equal spheres, of which one is slightly larger and more transparent than the


MAMMALIA.


other. The larger sphere and its products will be spoken of as the epiblastic spheres, and the smaller one and its products as the hypoblastic spheres, in accordance with their different destinations.

Both the spheres are soon divided into two, and each of the four so formed into two again; and thus a stage with eight spheres ensues. At the moment of their first separation these spheres are spherical, and arranged in two layers, one of them formed of the four epiblastic spheres, and the other of the four hypoblastic. This position is not long retained, but one of the hypoblastic spheres passes to the centre; and the whole ovum again takes a spherical form.

In the next phase of segmentation each of the four epiblastic spheres divides into two, and the ovum thus becomes constituted of twelve spheres, eight epiblastic and four hypoblastic. The epiblastic spheres have now become markedly smaller than the hypoblastic.

The four hypoblastic spheres next divide, giving rise, together with the eight epiblastic spheres, to sixteen spheres in all; which are nearly uniform in size. Of the eight hypoblastic spheres four soon pass to the centre, while the eight superficial epiblastic spheres form a kind of cup partially enclosing the hypoblastic spheres. The epiblastic spheres now divide in their turn, giving rise to sixteen spheres which largely enclose the hypoblastic spheres. The segmentation of both epiblastic and hypoblastic spheres continues, and in the course of it the epiblastic spheres spread further and further over the hypoblastic, so that at the close of segmentation the hypoblastic spheres constitute a central solid mass almost entirely surrounded by the epiblastic spheres. In a small circular area however the hypoblastic spheres remain for some time exposed at the surface (fig. 1 34 A).

The whole process of segmentation is completed in the rabbit about seventy hours after impregnation. At its close the epiblast cells, as they may now be called, are clear, and have an irregularly cubical form ; while the hypoblast cells are polygonal and granular, and somewhat larger than the epiblast cells.

The opening in the epiblastic layer where the hypoblast cells are exposed on the surface may for convenience be called with


2l6


THE SEGMENTATION.


Van Beneden the blastoporc, though it is highly improbable that it in any way corresponds with the blastopore of other vertebrate

ova 1 .

R



FIG. 134. OPTICAL SECTIONS OF A RAKBIT'S OVUM AT TWO STAGES CLOSELY FOLLOWING UPON THE SEGMENTATION. (After E. van Beneden.)

ep. epiblast ; hy. primary hypoblast ; bp. Van Beneden's blastopore. The shading of the epiblast and hypoblast is diagrammatic.

After its segmentation the ovum passes into the uterus. The epiblast cells soon grow over the blastopore and thus form a complete superficial layer. A series of changes next take place which result in the formation of what has been called the blastodermic vescicle. To Ed. van Beneden we owe the fullest account of these changes ; to Hensen and Kolliker however we are also indebted for valuable observations, especially on the later stages in the development of this vesicle.

The succeeding changes commence with the appearance of a narrow cavity between the epiblast and hypoblast, which extends so as completely to separate these two layers except in the region adjoining the original site of the blastopore (fig. 134 B) a . The cavity so formed rapidly enlarges, and with it the ovum also ; which soon takes the form of a thin-walled vesicle with a large central cavity. This vesicle is the blastodermic

1 It is stated by Bischoff that shortly after impregnation, and before the commencement of the segmentation, the ova of the rabbit and guinea-pig are covered with cilia and exhibit the phenomenon of rotation. This has not been noticed by other observers.

  • Van Beneden regards it as probable that the blastopore is situated somewhat

excentrically in relation to the area of attachment of the hypoblastic mass to the epiblast.


MAMMALIA.


217


vesicle. The greater part of its walls are formed of a single row of flattened epiblast cells; while the hypoblast cells form a small lens -shaped mass attached to the inner side of the epiblast cells (fig- 135).

In the Vespertilionidee Van Beneden and Julin have shewn that the ovum undergoes at the close of segmentation changes of a more or less similar nature to those in the rabbit ; the blastopore would however appear to be wider, and to persist even after the cavity of the blastodermic vesicle has commenced to be developed.



FIG. 135. RABBIT'S OVUM BETWEEN 7090

HOURS AFTER IMPREGNATION. (After E. van

Beneden.)

bv. cavity of blastodermic vesicle (yolk-sack) ; ep. epiblast ; hy. primitive hypoblast ; Z/. mucous envelope (zona pellucida).


Although by this stage, which occurs in the rabbit between seventy and ninety hours after impregnation, the blastodermic vesicle has by no means attained its greatest dimensions, it has nevertheless grown from about 0x39 mm. the size of the ovum at the close of segmentation to about 0*28. It is enclosed by a membrane formed from the zona radiata and the mucous layer around it. The blastodermic vesicle continues to enlarge rapidly, and during the process the hypoblastic mass undergoes important changes. It spreads out on the inner side of the epiblast and at the same time loses its lens-like form and becomes flattened. The central part of it remains however thicker, and is constituted of two rows of cells, while the peripheral part, the outer boundary of which is irregular, is formed of an imperfect layer of amoeboid cells which continually spread further and further within the epiblast. The central thickening of the hypoblast forms an opaque circular spot on the blastoderm, which constitutes the commencement of the embryonic area.


2l8 FORMATION OF THE LAYERS.

The history of the stages immediately following, from about the commencement of the fifth day to the seventh day, when a primitive streak makes its appearance, is imperfectly understood, and has been interpreted very differently by Van Beneden (No. 171) on the one hand and by Kolliker (184), Rauber (187) and Lieberkiihn (186) on the other. I have myself in conjunction with my pupil, Mr Heape, also conducted some investigations on these stages, which have unfortunately not as yet led me to a completely satisfactory reconciliation of the opposing views.

Van Beneden states that about five days after impregnation the hypoblast cells in the embryonic area become divided into two distinct strata, an upper stratum of small cells adjoining the epiblast and a lower stratum of flattened cells which form the true hypoblast. At the edge of the embryonic area the hypoblast is continuous with a peripheral ring of the amoeboid cells of the earlier stage, which now form, except at the edge of the ring, a continuous layer of flattened cells in contact with the epiblast. During the sixth day the flattened epiblast cells are believed by Van Beneden to become columnar. The embryonic area gradually extends itself, and as it does so becomes oval. A central lighter portion next becomes apparent, which gradually spreads, till eventually the darker part of the embryonic area forms a crescent at the posterior part of the now somewhat pyriform embryonic area. The lighter part is formed of columnar epiblast and hypoblast only, while in the darker area a layer of the mesoblast, derived from the intermediate layer of the fifth day, is also found. In this darker area the primitive streak originates early on the seventh day.

Kolliker, following the lines originally laid down by Rauber, has arrived at very different results. He starts from the three-layered condition described by Van Beneden for the fifth day, but does not give any investigations of his own as to the origin of the middle layer. He holds the outer layer to be a provisional layer of protective cells, forming part of the wall of the original vesicle, the middle layer he regards as the true epiblast and the inner layer as the hypoblast.

During the sixth day he finds that the cells of the outer layer gradually cease to form a continuous layer and finally disappear ; while the cells of the middle layer become columnar, and form the columnar epiblast present in the embryonic area at the end of the sixth day. The mesoblast first takes its origin in the region and on the formation of the primitive streak.

The investigations of Heape and myself do not extend to the first formation of the intermediate layer found on the fifth day. We find on the sixth day in germinal vesicles of about 2-2 2'5 millimetres in diameter with embryonic areas of about '8 mm. that the embryonic area (fig. 136) is throughout composed of


MAMMALIA.


(1) A layer of flattened hypoblast cells ;

(2) A somewhat irregular layer of more columnar elements, in some places only a single row deep and in other places two or more rows deep.

(3) Flat elements on the surface, which do not, however, form a continuous layer, and are intimately attached to the columnar cells below.

Our results as to the structure of the blastoderm at this stage closely correspond therefore with those of Kolliker, but on one important point we have arrived at a different conclusion. Kolliker states that he has never found the flattened elements in the act of becoming columnar. We believe that we have in many instances been able to trace them in the act of undergoing this change, and have attempted to shew this in our figure.

Our next oldest embryonic areas were somewhat pyriform measuring about i '19 mm. in length and '85 in breadth. Of these we have several, some from a rabbit in which we also met with younger still nearly circular areas. All of them had a distinctly marked posterior opacity forming a commencing primitive streak, though decidedly less advanced than in the blastoderm represented in fig. 140. In the younger specimens the epiblast in front of the primitive streak was formed of a single row of columnar cells (fig. 138 A), no mesoblast was present and the hypoblast formed a layer of flattened cells. In the region immediately in front of the primitive streak, an irregular layer of mesoblast cells was interposed between the epiblast and hypoblast. In the anterior part of the primitive streak itself (fig. 138 B) there was a layer of mesoblast with a considerable lateral extension, while in the median line there was a distinct mesoblastic proliferation of epiblast cells. In the posterior sections the lateral extension of the mesoblast was less, but the mesoblast cells formed a thicker cord in the axial line.

Owing to the unsatisfactory character of our data the following attempt to fill in the history of the fifth and sixth days must be regarded as tentative 1 . At the commencement of the fifth day the central thickening, of what has been called above the primitive hypoblast, becomes divided into two layers: the lower of these is continuous with the peripheral hypoblast and is formed of flattened cells, while the upper one is formed of small rounded elements. The superficial epiblast again is formed of flattened cells.

During the fifth day remarkable changes take place in the epiblast of the embryonic area. It is probable that its con 1 The attempt made below to frame a consecutive history out of the contradictory data at my disposal is not entirely satisfactory. Should Kolliker's view turn out to be quite correct, the origin of the middle layer of the fifth day, which Kolliker believes to become the permanent epiblast, will have to be worked out again, in order to determine whether it really comes, as it is stated by Van Beneden to do, from the primitive hypoblast.


220


FORMATION OF THE LAYERS.


stituent cells increase in number and become one by one columnar; and that in the process they press against the layer of rounded elements below them, so that the two layers cease to be distinguishable, and the whole embryonic area acquires in section the characters represented in fig. I36 1 . Towards the end of the



FIG. 136. SECTION THROUGH THE NEARLY CIRCULAR EMBRYONIC AREA OF A RABBIT'S OVUM OF six DAYS, NINE HOURS AND '8 MM. IN DIAMETER.

The section shews the peculiar character of the upper layer with a certain number of superficial flattened cells ; and represents about half the breadth of the area.

sixth day the embryonic area becomes oval, but the changes which next take place are not understood. In the front part of the area only two layers of cells are found, (i) an hypoblast, and (2) an epiblast of columnar cells probably derived from the flattened epiblast cells of the earlier stages. In the posterior part of the blastoderm a middle layer is present (Van Beneden) in addition to the two other layers; and this layer probably originates from the middle layer which extended throughout the area at the beginning of the fifth day, and then became fused with the epiblast. The middle layer does not give rise to the whole of the eventual mesoblast, but only to part of it. From its origin it may be called the hypoblastic mesoblast, and it is probably equivalent to the hypoblastic mesoblast already described in the chick (pp. 154 and 155). The stage just described has only been met with by Van Beneden 2 .

A diagrammatic view of the whole blastodermic vesicle at about the beginning of the seventh day is given in fig. 137. The embryonic area is represented in white. The line ge in B shews the extension of the hypoblast round the inner side of the vesicle. The blastodermic vesicle is therefore formed of three areas, (i)

1 The section figured may perhaps hardly appear to justify this view; the examination of a larger number of sections is, however, more favourable to it, but it must be admitted that the interpretation is by no means thoroughly satisfactory.

Kolliker does not believe in the existence of this stage, having never met with it himself. It appears to me, however, more probable that Kolliker has failed to obtain it, than that Van Beneden has been guilty of such an extraordinary blunder as to have described a stage which has no existence.


MAMMALIA.


221


the embryonic area with three layers: this area is placed where the blastopore was originally situated. (2) The ring around the embryonic area where the walls of the vesicle are formed of epiblast and hypoblast. (3) The area beyond this again where the vesicle is formed of epiblast only 1 .


A.


B,



FlG. 137. VIEWS OF THE BLASTODERMIC VESICLE OF A RABBIT ON THE SEVENTH DAY WITHOUT THE ZONA. A. from above, B. from the side. (From Kolliker.)

ag. embryonic area ; ge. boundary of the hypoblast.

The changes which next take place begin with the formation of a primitive streak, homologous with, and in most respects similar to, the primitive streak in Birds. The formation of the streak is preceded by that of a clear spot near the middle of the blastoderm, forming the nodal point of Hensen. This spot subsequently constitutes the front end of the primitive streak.

The history of the primitive streak was first worked out in a satisfactory manner by Hensen (No. 182), from whom however I differ in admitting the existence of a certain part of the mesoblast before its appearance.

Early on the seventh day the embryonic area becomes pyriform, and at its posterior and narrower end a primitive streak makes its appearance, which is due to a proliferation of rounded cells from the epiblast. At the time when this proliferation

1 Schafer describes the blastodermic vesicle of the cat as being throughout in a bilaminar condition before the formation of a definite primitive streak or of the mesoblast.


222


THE PRIMITIVE STREAK.


commences the layer of hypoblastic mesoblast is present, especially just in front of, and at the sides of, the anterior part of the streak; but no mesoblast is found in the anterior part of the embryonic area. These features are shewn in fig. 138 A and B.

A.



FlG. 138. TWO SECTIONS THROUGH OVAL BLASTODERMS OF A RABBIT ON THE SEVENTH DAY. THE LENGTH OF THE AREA WAS ABOUT I '2 MM. AND ITS BREADTH ABOUT '86 MM.

A. Through the region of the blastoderm in front of the primitive streak; B. through the front part of the primitive streak ; ep. epiblast ; m. mesoblast ; hy. hypoblast ; /;-. primitive streak.

The mesoblast derived from the proliferation of the epiblast soon joins the mesoblast already present; though in many sections it



FlG. 139. TWO TRANSVERSE SECTIONS THROUGH THE EMBRYONIC AREA OF AN KMBRYO RABBIT OF SEVEN DAYS.

The embryo has nearly the structure represented in fig. 140.

A. is taken through the anterior part of the embryonic area. It represents about half the breadth of the area, and there is no trace of a medullary groove or of the mesoblast.

B. Is taken through the posterior part of the primitive streak.

ep. epiblast; hy. hypoblast.


MAMMALIA. 223


seems possible to trace a separation between the two parts (fig. 139 B) of the mesoblast.

During the seventh day the primitive streak becomes a more pronounced structure, the mesoblast in its neighbourhood increases in quantity, while an axial groove the primitive groove is formed on its upper surface. The mesoblastic layer in front of the primitive streak becomes thicker, and, in the twolayered region in front, the epiblast becomes several rows deep (fig. 139 A).

In the part of the embryonic area in front of the primitive streak there arise during the eighth day two folds bounding a shallow median groove, which meet in front, but diverge behind, and enclose between them the foremost end of the primitive streak (fig. 141). These folds are the medullary folds and they constitute the first definite traces of the embryo. The medullary plate bounded by them rapidly grows in length, the primitive streak always remaining at its hinder end. While the lateral epiblast is formed of several rows of cells, that of the me- FlG I40 EMBRYONIC

dullary plate is at first formed of but a AREA OF AN EIGHT DAYS '

, J J RABBIT. (After Kolliker.)

Single row (fig. 142, mg). The mesoblast, ^ embryonic area ;pr.

which appears to grow forward from the primitive streak. primitive streak, is stated to be at first a continuous sheet between the epiblast and hypoblast (Hensen). The evidence on this point does not however appear to me to be quite conclusive. In any case, as soon as ever the medullary groove is formed, the mesoblast becomes divided, exactly as in Lacerta and Elasmobranchii, into two independent lateral plates, which are not continuous across the middle line (fig. 142, me]. The hypoblast cells are flattened laterally, but become columnar beneath the medullary plate (fig. 142).

In tracing the changes which take place in the relations of the layers, in passing from the region of the embryo to that of the primitive streak, it will be convenient to follow the account given by Schafer for the guinea-pig (No. 190), which on this point is far fuller and more satisfactory than that of other ob


224


THE BLASTOPORE.


servers. In doing so I shall leave out of consideration the fact (fully dealt with later in this chapter) that the layers in the guinea-pig are inverted. Fig. 143 represents a series of sections through this part in the guinea-pig. The anterior section (D)



FIG. 141. EMBRYONIC AREA OF A SEVEN DAYS' EMBRYO RABBIT. (From Kolliker.)

o. place of future area vasculosa ; rf. medullary groove ; fir. primitive streak ; ag. embryonic area.



FIG. 142. TRANSVERSE SECTION THROUGH AN EMBRYO RABBIT OF EIGHT DAYS. ep. epiblast ; me. mesoblast ; hy. hypoblast ; mg. medullary groove.

passes through the medullary groove near its hinder end. The commencement of the primitive streak is marked by a slight prominence on the floor of the medullary groove between the two diverging medullary folds (fig. 143 C, ae). Where this prominence becomes first apparent the epiblast and hypoblast are united together. The mesoblast plates at the two sides remain


MAMMALIA.


225


in the meantime quite free. Slightly further back, but before the primitive groove is reached, the epiblast and hypoblast arc connected together by a cord of cells (fig. 143 B, /), which in the section next following becomes detached from the hypoblast and forms a solid keel projecting from the epiblast. In the following section the hitherto independent mcsoblast plates become united with this keel (fig. 143 A); and in the posterior sections, through the part of the primitive streak with the primitive groove, the epiblast and mesoblast continue to be united in the axial line, but the hypoblast remains distinct. These peculiar relations may shortly be described by saying that in the axial line the hypoblast becomes united with the epiblast at the posterior cud of the embryo; and that the cells which connect the hypoblast and epiblast are posteriorly continuous with the fused epiblast and mesoblast of the

primitive Streak, the hypo- , epiblast; ///. mesoblast; A. hypoblasl;

blast in the region of the ac- axial q>il>last <>f the primitive streak ; . . , . all. axial hypoblast attached in 15. and C. to

primitive Streak having be- the epiblast at the rudimentary blaslopore ;

/;'. medullary groove; / rudimentary bias

topore.



FlG. 143. A SERIES OH TRANSVERSE SKC TIONS THROUGH THE JUNCTION OK TIIK I'RIMITIVK. STRKAK A.N'l) MKIMM.I.AK Y GROOVE

OK A YOUNG GuiNKA-i'io. (After Schiifcr.) A. is the posterior section.


the


come distinct from other layers.

The peculiar relations just described, which hold also for the rabbit, receive their full explanation by a comparison of the Mammal with the Bird and the Lizard, but before entering into this comparison, it will be well to describe the next stage in the rabbit, which is in many respects very instructive. In this stage li in. 15


226 THE BLASTOPORE.


the thickened axial portion of the hypoblast in the region of the embryo becomes separated from the lateral part as the notochord. Very shortly after the formation of the notochord, the hypoblast grows in from the two sides, and becomes quite continuous across the middle line. The formation of the notochord takes place from before backwards ; and at the hinder end of the embryo the notochord is continued into the mass of cells which forms the axis of the primitive streak, becoming therefore at this point continuous with the epiblast. The notochord in fact behaves exactly as did the axial hypoblast in the earlier stage.

In comparison with Lacerta (pp. 203 205) it is obvious that the axial hypoblast and the notochord derived from it have exactly the same relations in Mammalia and Lacertilia. In both they are continued at the hind end of the embryo into the epiblast ; and close to where they join it, the mesoblast and epiblast fuse together to form the primitive streak. The difference between the two types consists in the fact that in Reptilia there is formed a passage connecting the neural and alimentary canals, the front wall of which is constituted by the cells which form the above junction between the notochord and epiblast ; and that in Mammalia this passage which is only a rudimentary structure in Reptilia has either been overlooked or else is absent. In any case the axial junction of the epiblast and hypoblast in Mammalia is shewn by the above comparison with Lacertilia to represent the dorsal lip of the true vertebrate blastopore. The presence of this blastopore seems to render it clear that the blastopore discovered by Ed. van Beneden cannot have the meaning he assigned to it in comparing it with the blastopore of the frog.

Kolliker adduces the fact that the notochord is continuous with the axial cells of the primitive streak as an argument against its hypoblastic origin. The above comparison with Lacertilia altogether deprives this argument of any force.

At the stage we have now reached the three layers are definitely established. The epiblast (on the view adopted above) clearly originates from epiblastic segmentation cells. The hypoblast without doubt originates from the hypoblastic segmentation spheres which give rise to the lenticular mass within the epiblast on the appearance of the cavity of the blastodermic vesicle ; while, though the history of the mesoblast is still obscure, part of it appears to originate from the hypoblastic mass, and part is undoubtedly formed from the epiblast of the primitive streak.


MAMMALIA. 227


While these changes have been taking place the rudiments of a vascular area become formed, and it is very possible that part of the hypoblastic mesoblast passes in between the epiblast and hypoblast. immediately around the embryonic area, to give rise to the area vasculosa. From Hensen's observation it seems at any rate clear that the mesoblast of the vascular area arises independently of the primitive streak: an observation which is borne out by the analogy of Birds.


General growth of the Embryo.

We have seen that the blastodermic vesicle becomes divided at an early stage of development into an embryonic area, and a non-embryonic portion. The embryonic area gives rise to the whole of the body of the embryo, while the non-embryonic part forms an appendage, known as the umbilical vesicle, which becomes gradually folded off from the embryo, and has precisely the relations of the yolk-sack of the Sauropsida. It is almost certain that the Placentalia are descended from ancestors, the embryos of which had large yolk-sacks, but that the yolk has become reduced in quantity owing to the nutriment received from the wall of the uterus taking the place of that originally supplied by the yolk. A rudiment of the yolk-sack being retained in the umbilical vesicle, this structure may be called indifferently umbilical vesicle or yolk-sack.

The yolk which fills the yolk-sack in Birds is replaced in Mammals by a coagulable fluid ; while the gradual extension of the hypoblast round the wall of the blastodermic vesicle, which has already been described, is of the same nature as the growth of the hypoblast round the yolk-sack in Birds.

The whole embryonic area would seem to be employed in the formation of the body of the embryo. Its long axis has no very definite relation to that of the blastodermic vesicle. The first external trace of the embryo to appear is the medullary plate, bounded by the medullary folds, and occupying at first the anterior half of the embryonic area (fig. 141). The two medullary folds diverge behind and enclose the front end of the primitive streak. As the embryo elongates, the medullary folds

15-2


228 GENERAL GROWTH OF THE EMBRYO.

nearly meet behind and so cut off the front portion of the primitive streak, which then appears as a projection in the hind end of the medullary groove. In an embryo rabbit, eight days after impregnation, the medullary groove is about r8o mm. in length. At this stage a division may be clearly seen in the lateral plates of mesoblast into a vertebral zone adjoining the embryo and a more peripheral lateral zone ; and in the vertebral zone indications of two somites, about O'37 mm. from the hinder end of the embryo, become apparent. The foremost of these somites marks the junction, or very nearly so, of the cephalic region and trunk. The small size of the latter as compared with the former is very striking, but is characteristic of Vertebrates generally. The trunk gradually elongates relatively to the head, by the addition behind of fresh somites. The embryo has not yet begun to be folded off from the yolk-sack. In a slightly older embryo of nine days there appears (Hensen, Kolliker) round the embryonic area a delicate clear ring which is narrower in front than behind (fig. 144 A, ap). This ring is regarded by these authors as representing the peripheral part of the area pellucida of Birds, which does not become converted into the body of the embryo. Outside the area pellucida, an area vasculosa has become very well defined. In the embryo itself (fig. 144 A) the disproportion between head and trunk is less marked than before ; the medullary plate dilates anteriorly to form a spatulashaped cephalic enlargement ; and three or four somites are established. In the lateral parts of the mesoblast of the head there may be seen on each side a tube-like structure (Jiz). Each of these is part of the heart, which arises as two independent tubes. The remains of the primitive streak (pr) are still present behind the medullary groove.

In somewhat older embryos (fig. 144 B) with about eight somites, in which the trunk considerably exceeds the head in length, the first distinct traces of the folding-off of the head end of the embryo become apparent, and somewhat later a fold also appears at the hind end. In the formation of the hind end of the embryo the primitive streak gives rise to a tail swelling and to part of the ventral wall of the post-anal gut. In the region of the head the rudiments of the heart (//) are far more definite. The medullary groove is still open for its whole length, but in


MAMMALIA..


229


the head it exhibits a series of well-marked dilatations. The foremost of these (v/t) is the rudiment of the fore-brain, from the sides of which there project the two optic vesicles (ab} ; the next


A.


ao



fc


FIG. 144. EMBRYO RABBITS OF ABOUT NINE DAYS FROM THE DORSAL SIDE.

(From Kolliker.)

A. magnified 22 times, and B. 21 times.

ap. area pellucida ; rf. medullary groove ; h' . medullary plate in the region of the future fore-brain; h". medullary plate in the region of the future mid-brain; vh. forebrain; ab. optic vesicle; mh. mid-brain; h!i. and h'" . hind-brain; tiw. mesoblastic somite; stz. vertebral zone; pz. lateral zone; hz. and h. heart; ph. pericardial section of body cavity ; vo. vitelline vein ; of. amnion fold.


is the mid-brain (ink), and the last is the hind-brain (///), which is again divided into smaller lobes by successive constrictions. The medullary groove behind the region of the somites dilates into an embryonic sinus rhomboidalis like that of the Bird. Traces of the amnion (of) are now apparent both in front of and behind the embryo.


230


GENERAL GROWTH OF THE EMBRYO.


The structure of the head and the formation of the heart at this age are illustrated in fig. 145. The widely-open medullary groove (rf) is shewn in the centre. Below it the hypoblast is thickened to form the notochord dcf ; and at the sides are seen the two tubes, which, on the folding-in of the fore-gut, give rise to the unpaired heart. Each of these is formed of an outer muscular tube of splanchnic mesoblast (a/i/i), not quite closed towards the hypoblast, and an inner epithelioid layer (ik/i) ; and is placed

A.



B.



FIG. 145. TRANSVERSE SECTION THROUGH THE HEAD OF A RABBIT OF THE SAME AGE AS FIG. 144 B. (From Kolliker.)

B. is a more highly magnified representation of part of A.

rf. medullary groove ; mp. medullary plate ; rw. medullary fold ; h. epiblast ; dd. hypoblast; dd' . notochordal thickening of hypoblast; sp. undivided mesoblast; tip. somatic mesoblast ; dfp. splanchnic mesoblast ; ph. pericardial section of body cavity; ahk. muscular wall of heart; ihh. epithelioid layer of heart; nies. lateral undivided mesoblast ; s?v. fold of hypoblast which will form the ventral wall of the pharynx ; sr. commencing throat.


in a special section of the body cavity (//^), which afterwards forms the pericardial cavity.

Before the ninth day is completed great external changes are usually effected. The medullary groove becomes closed for its whole length with the exception of a small posterior portion. The closure commences, as in Birds, in the region of the midbrain. Anteriorly the folding-off of the embryo proceeds so far



MAMMALIA. 231


that the head becomes quite free, and a considerable portion of the throat, ending blindly in front, becomes established. In the course of this folding the, at first widely separated, halves of the heart are brought together, coalesce on the ventral side of the throat, and so give rise to a median undivided heart. The fold at the tail end of the embryo progresses considerably, and during its advance the allantois is formed in the same way as in Birds. The somites increase in number to about twelve. The amniotic folds nearly meet above the embryo.

The later stages in the development proceed in the main in the same manner as in the Bird. The cranial flexure soon becomes very marked, the mid-brain forming the end of the long axis of the embryo (fig. 146). The sense organs have the usual development. Under the fore-brain appears an epiblastic involution giving rise both to the mouth and to the pituitary body. Behind the mouth are three well-marked pairs of visceral arches. The first of these is the mandibular arch (fig. 146, md\ which meets its fellow in the middle line, and forms the posterior boundary of the mouth. It sends forward on each side a superior


01$



hy


Si

FIG. 146. ADVANCED EMBRYO OF A RABBIT (ABOUT TWELVE DAYS) 1 . mb. mid-brain; th. thalamencephalon ; ce. cerebral hemisphere; op. eye; iv.v. fourth ventricle; mx. maxillary process ; md. mandibular arch ; hy. hyoid arch;//, fore-limb; hi. hind-limb; urn. umbilical stalk.

1 This figure was drawn for me by my pupil, Mr Weldon.


232 GENERAL GROWTH OF THE EMBRYO.

maxillary process (mx) which partially forms the anterior margin of the mouth. Behind the mandibular arch are present a welldeveloped hyoid (hy) and a first branchial arch (not shewn in fig. 146). There are four clefts, as in other Amniota, but the fourth is not bounded behind by a definite arch. Only the first of these clefts persists as the tympanic cavity and Eustachian tube.

At the time when the cranial flexure appears, the body also develops a sharp flexure immediately behind the head, which is thus bent forwards upon the posterior straight part of the body (fig. 146). The amount of this flexure varies somewhat in different forms. It is very marked in the dog (Bischoff). At a later period, and in some species even before the stage figured, the tail end of the body also becomes bent (fig. 146), so that the whole dorsal side assumes a convex curvature, and the head and tail become closely approximated. In most cases the embryo, on the development of the tail, assumes a more or less definite spiral curvature (fig. 146); which however never becomes nearly so marked a feature as it commonly is in Lacertilia and Ophidia. With the more complete development of the lower wall of the body the ventral flexure partially disappears, but remains more or less persistent till near the close of intra-uterine life. The limbs are formed as simple buds in the same manner as in Birds. The buds of the hind-limbs are directed somewhat forwards, and those of the fore-limb backwards.

Embryonic membranes and yolk-sack.

The early stages in the development of the embryonic membranes are nearly the same as in Aves ; but during the later stages in the Placentalia the allantois enters into peculiar relations with the uterine walls, and the two, together with the interposed portion of the subzonal membrane or false amnion, give rise to a very characteristic Mammalian organ the placenta into the structure of which it will be necessary to enter at some length. The embryonic membranes vary so considerably in the different forms that it will be advantageous to commence with a description of their development in an ideal case.



MAMMALIA. 233


We may commence with a blastodermic vesicle, closely invested by the delicate remnant of the zona radiata, at the stage in which the medullary groove is already established. Around the embryonic area a layer of mesoblast would have extended for a certain distance ; so as to give rise to an area vasculosa, in which however the blood-vessels would not have become definitely established. Such a vesicle is represented diagrammatically in fig. 147, 1. Somewhat later the embryo begins to be folded off, first in front and then behind (fig. 147, 2). These folds result in a constriction separating the embryo and the yolk-sack (ds), or as it is known in Mammalian embryology, the umbilical vesicle. The splitting of the mesoblast into a splanchnic and a somatic layer has taken place, and at the front and hind end of the embryo a fold (ks) of the somatic mesoblast and epiblast begins to rise up and grow over the head and tail of the embryo. These two folds form the commencement of the amnion. The head and tail folds of the amnion are continued round the two sides of the embryo, till they meet and unite into a continuous fold. This fold grows gradually upwards, but before it has completely enveloped the embryo, the blood-vessels of the area vasculosa become fully developed. They are arranged in a manner not very different from that in the chick.

The following is a brief account of their arrangement in the Rabbit :

The outer boundary of the area, which is continually extending further and further round the umbilical vesicle, is marked by a venous sinus terminalis (fig. 147, st). The area is not, as in the chick, a nearly complete circle, but is in front divided by a deep indentation extending inwards to the level of the heart. In consequence of this indentation the sinus terminalis ends in front in two branches, which bend inwards and fall directly into the main vitelline veins. The blood is brought from the dorsal aortas by a series of lateral vitelline arteries, and not by a single pair as in the chick. These arteries break up into a more deeply situated arterial network, from which the blood is continued partly into the sinus terminalis, and partly into a superficial venous network. The hinder end of the heart is continued into two vitelline veins, each of which divides into an anterior and a posterior branch. The anterior branch is a limb of the sinus terminalis, and the posterior and smaller branch is continued towards the hind part of the sinus, near which it ends. On its way it receives, on its outer side, numerous branches from the venous network,


234


FCETAL MEMBRANES.



FlG. 147. FIVE DIAGRAMMATIC FIGURES ILLUSTRATING THE FORMATION OF THE FCETAL MEMBRANES OF A MAMMAL. (From Kolliker.)

In i, 2, 3, 4 the embryo is represented in longitudinal section. i . Ovum with zona pellucida, blastodermic vesicle, and embryonic area. i. Ovum with commencing formation of umbilical vesicle and amnion.

3. Ovum with amnion about to close, and commencing allantois.

4. Ovum with villous subzonal membrane, larger allantois, and mouth and anus.

5. Ovum in which the mesoblast of the allantois has extended round the inner


MAMMALIA. 235


surface of the subzonal membrane and united with it to form the chorion. The cavity of the allantois is aborted. This fig. is a diagram of an early human ovum.

d. zona radiata; d' '. processes of zona; sh. subzonal membrane; ch. chorion; ch.z. chorionic villi; am. amnion; ks. head-fold of amnion ; ss. tail-fold of amnion; a. epiblast of embryo; a. epiblast of non-embryonic part of the blastodermic vesicle;

. embryonic mesoblast; m' . non-embryonic mesoblast; df. area vasculosa; st. sinus

terminalis; dd. embryonic hypoblast; i. non-embryonic hypoblast; kh. cavity of blastodermic vesicle, the greater part of which becomes the cavity of the umbilical vesicle ds. ; dg. stalk of umbilical vesicle ; al. allantois ; e. embryo ; r. space between chorion and amnion containing albuminous fluid; vl. ventral body wall; hh. pericardial cavity.

which connect by their anastomoses the posterior branch of the vitelline vein and the sinus terminalis.

While the above changes have been taking place the whole blastodermic vesicle, still enclosed in the zona, has become attached to the walls of the uterus. In the case of the typical uterus with two tubular horns, the position of each embryo, when there are several, is marked by a swelling in the walls of the uterus, preparatory to the changes which take place on the formation of the placenta. In the region of each swelling the zona around the blastodermic vesicle is closely embraced, in a ring-like fashion, by the epithelium of the uterine wall. The whole vesicle assumes an oval form, and it lies in the uterus with its two ends free. The embryonic area is placed close to the mesometric attachment of the uterus. In many cases peculiar processes or villi grow out from the ovum (fig. 147, 4, sz), which fit into the folds of the uterine epithelium. The nature of these processes requires further elucidation, but in some instances they appear to proceed from the zona (the Rabbit) and in other instances from the subzonal membrane (the Dog). In any case the attachment between the blastodermic vesicle and the uterine wall becomes so close at the time when the body of the embryo is first formed out of the embryonic area, that it is hardly possible to separate them without laceration ; and at this period from the 8th to the pth day in the Rabbit it requires the greatest care to remove the ovum from the uterus without injury. It will be understood of course that the attachment above described is at first purely superficial and not vascular.

Shortly after the establishment of the circulation of the yolk


236


FCETAL MEMBRANES.


sack the folds of the amnion meet and coalesce above the embryo (fig. 147, 3 and 4, am). After this the inner or true amnion becomes severed from the outer or false amnion, though the two sometimes remain connected by a narrow stalk. Between the true and false amnion is a continuation of the body cavity. The true amnion consists of a layer of epiblastic epithelium and generally also of somatic mesoblast, while the false amnion consists, as a rule, of epiblast only ; though it is possible that in some cases (the Rabbit ?) the mesoblast may be continued along its inner face.

Before the two limbs of the amnion are completely severed, the epiblast of the umbilical vesicle becomes separated from the mesoblast and hypoblast of the vesicle (fig. 147, 3), and, to


FIG. 147*. DIAGRAM OF THE FCETAL MEMBRANES OF A MAMMAL.

(From Turner.)

Structures which either are or have been at an earlier period of development continuous with each other are represented by the same character of shading.

pc. zona with villi; ss. subzonal membrane; E. epiblast of embryo; am. amnion; A C. amniotic cavity ; M. mesoblast of embryo ; H. hypoblast of embryo ; UV. umbilical vesicle; al. allantois; ALC. allantoic cavity.

gether with the false amnion (s/i), with which it is continuous, forms a complete lining for the inner face of the zona radiata.


MAMMALIA. 237


The space between this membrane and the umbilical vesicle with the attached embryo is obviously continuous with the body cavity (vide figs. 147, 4 and 147*). To this membrane Turner has given the appropriate name of subzonal membrane: by Von Baer it was called the serous envelope. It soon fuses with the zona radiata, or at any rate the zona ceases to be distinguishable.

While the above changes are taking place in the amnion, the allantois grows out from the hind gut as a vesicle lined by hypoblast, but covered externally by a layer of splanchnic mesoblast (fig. 147, 3 and 4, a/) 1 . The allantois soon becomes a flat sack, projecting into the now largely developed space between the subzonal membrane and the amnion, on the dorsal side of the embryo (fig. 147*, ALC). In some cases it extends so as to cover the whole inner surface of the subzonal membrane; in other cases again its extension is much more limited. Its lumen may be retained or may become nearly or wholly aborted. A fusion takes place between the subzonal membrane and the adjoining mesoblastic wall of the allantois, and the two together give rise to a secondary membrane round the ovum, known as the chorion. Since however the allantois does not always come in contact with the whole inner surface of the subzonal membrane, the term chorion is apt to be somewhat vague ; and in the rabbit, for instance, a considerable part of the so-called chorion is formed by a fusion of the wall of the yolksack with the subzonal membrane (fig. 148). The placental region of the chorion may in such cases be distinguished as the true chorion, from the remaining part which will be called the false chorion.

The mesoblast of the allantois, especially that part of it which assists in forming the chorion, becomes highly vascular ; the blood being brought to it by two allantoic arteries continued from the terminal bifurcation of the dorsal aorta, and returned to the body by one, or rarely two, allantoic veins, which join the vitelline veins from the yolk-sack. From the outer surface of the true chorion (fig. 147, 5, d, 148) villi grow out and fit into crypts or depressions which have in the meantime made their

1 The hypoblastic element in the allantois is sometimes very much reduced, so that the allantois may he mainly formed of a vascular layer of mesoblast.


238 FCETAL MEMBRANES.

appearance in the walls of the uterus 1 . The villi of the.chorion are covered by an epithelium derived from the subzonal membrane, and are provided with a connective tissue core containing an artery and vein and a capillary plexus connecting them. In most cases they assume a more or less arborescent form, and have a distribution on the surface of the chorion varying characteristically in different species. The walls of the crypts into which the villi are fitted also become highly vascular, and a nutritive fluid passes from the maternal vessels of the placenta to the fcetal vessels by a process of diffusion ; while there is probably also a secretion by the epithelial lining of the walls of the crypts, which becomes absorbed by the vessels of the fcetal villi. The above maternal and fcetal structures constitute together the organ known as the placenta. The maternal portion consists essentially of the vascular crypts in the uterine walls, and the fcetal portion of more or less arborescent villi of the true chorion fitting into these crypts.

While the placenta is being developed, the folding-off of the embryo from the yolk-sack becomes more complete ; and the yolk-sack remains connected with the ileal region of the intestine by a narrow stalk, the vitelline duct (fig. 147, 4 and 5 and fig. 147*), consisting of the same tissues as the yolk-sack, viz. hypoblast and splanchnic mesoblast. While the true splanchnic stalk of the yolk-sack is becoming narrow, a somatic stalk connecting the amnion with the walls of the embryo is also formed, and closely envelops the stalk both of the allantois and the yolk-sack. The somatic stalk together with its contents is known as the umbilical cord. The mesoblast of the somatopleuric layer of the cord develops into a kind of gelatinous tissue, which cements together the whole of the contents. The allantoic arteries in the cord wind in a spiral manner round the allantoic vein. The yolk-sack in many cases atrophies completely before the close of intra-uterine life, but in other cases it is only removed with the other embryonic membranes at birth. The intra-embryonic portion of the allantoic stalk gives rise to two structures, viz. to (-1) the urinary bladder

1 These crypts have no connection with the openings of glands in the walls of the uterus. They are believed by Ercolani to be formed to a large extent by a regeneration of the lining tissue of the uterine walls.


MAMMALIA. 239


formed by a dilatation of its proximal extremity, and to (2) a cord known as the urachus connecting the bladder with the wall of the body at the umbilicus. The urachus, in cases where the cavity of the allantois persists till birth, remains as an open passage connecting the intra- and extra-embryonic parts of the allantois. In other cases it gradually closes, and becomes nearly solid before birth, though a delicate but interrupted lumen would appear to persist in it. It eventually gives rise to the ligamentum vesicae medium.

At birth the foetal membranes, including the fcetal portion of the placenta, are shed ; but in many forms the interlocking of the fcetal villi with the uterine crypts is so close that the uterine mucous membrane is carried away with the fcetal part of the placenta. It thus comes about that in some placentae the maternal and fcetal parts simply separate from each other at birth, and in others the two remain intimately locked together, and both are shed together as the after-birth. These two forms of placenta are distinguished as non-deciduate and deciduate, but it has been shewn by Ercolani and Turner that no sharp line can be drawn between the two types ; moreover, a larger part of the uterine mucous membrane than that forming the maternal part of the placenta is often shed in the deciduate Mammalia, and in the non-deciduate Mammalia it is probable that the mucous membrane (not including vascular parts) of the maternal placenta either peels or is absorbed.

Comparative history of the Mammalian foetal membranes.

Two groups of Mammalia the Monotremata and the Marsupialia are believed not to be provided with a true placenta.

The nature of the fcetal membranes in the Monotremata is not known. Ova, presumably in an early stage of development, have been found free in the uterus of Ornithorhyncus by Owen. The lining membrane of the uterus was thickened and highly vascular. The females in which these were found were killed early in October 1 .

1 The following is Owen's account of the young after birth (Comp. Anat. of Vertebrates, Vol. in. p. 717) : " On the eighth of December Dr Bennet discovered in "the subterranean nest of Ornithorhyncus three living young, naked, not quite two


240 COMPARATIVE HISTORY OF FCETAL MEMBRANES.

Marsupialia. Our knowledge of the foetal membranes of the Marsupialia is almost entirely due to Owen. In Macropus major he found that birth took place thirty-eight days after impregnation. A foetus at the twentieth day of gestation measured eight lines from the mouth to the root of the tail. The foetus was enveloped in a large subzonal membrane, with folds fitting into uterine furrows, but not adhering to the uterus, and witlwut villi. The embryo was enveloped in an amnion reflected over the stalk of the yolk-sack, which was attached by a filamentary pedicle to near the end of the ileum. The yolksack was large and vascular, and was connected with the fostal vascular system by a vitelline artery and two veins. The yolksack was partially adherent, especially at one part, to the subzonal membrane. No allantois was observed. In a somewhat older foetus of ten lines in length there was a small allantois supplied by two allantoic arteries and one vein. The allantois was quite free and not attached to the subzonal membrane. The yolk-sack was more closely attached to the subzonal membrane than in the younger embryo 1 .

All Mammalia, other than the Monotremata and Marsupialia, have a true allantoic placenta. The placenta presents a great variety of forms, and it will perhaps be most convenient first to treat these varieties in succession, and then to give a general exposition of their mutual affinities 2 .

Amongst the existing Mammals provided with a true placenta, the most primitive type is probably retained by those forms in which the placental part of the chorion is confined to a comparatively restricted area on the dorsal side of the embryo ; while the false chorion is formed by the

"inches in length." On the i2th of August, 1864, "a female Echidna hystrix was " captured .... having a young one with its head buried in a mammary or marsupial " fossa. This young one was naked, of a bright reel colour, and one inch two lines in "length."

1 Owen quotes in the Anatomy of Vertebrates* Vol. in. p. 721, a description from Rengger of the development of Didelphis azarse, which would seem to imply that a vascular adhesion arises between the uterine walls and the subzonal membrane, but the description is too vague to be of any value in determining the nature of the fcetal membranes.

2 Numerous contributions to our knowledge of the various types of placenta have been made during the last few years, amongst which those of Turner and Ercolani may be singled out, both from the variety of forms with which they deal, and the important light they have thrown on the structure of the placenta.


MAMMALIA.


241


vascular yolk-sack fusing with the remainder of the subzonal membrane. In all the existing forms with this arrangement of foetal membranes, the placenta is deciduate. This, however, was probably not the case in more primitive forms from which these are descended 1 . The placenta would appear from Ercolani's description to be simpler in the mole (Talpa) than in other species. The Insectivora, Cheiroptera, and Rodentia are the groups with this type of placenta ; and since the rabbit, amongst the latter, has been more fully worked out than other species, we may take it first.

The Rabbit. In the pregnant female Rabbit several ova are generally found in each horn of the uterus. The general condition of the eggmembranes at the time of their full development is shewn in fig. 148.

The embryo is surrounded by the amnion, which is comparatively small. The ;yolk-sack (ds) is large and attached to the embryo by a long stalk. It has the form of a flattened sack closely applied to about two-thirds of the surface of the subzonal membrane. The outer wall of this sack, adjoining the subzonal membrane, is formed of hypoblast only ; but the inner wall is covered by the mesoblast of the area vasculosa, as indicated by the thick black line (fd}. The vascular area is bordered by the sinus terminalis (st}. In an earlier stage of development the yolk-sack had not the compressed form represented in the figure. It is, however, remarkable that the vascular area never extends over the whole yolk-sack ; but the inner vascular wall of the yolksack fuses with the outer, and with the subzonal membrane, and so forms a false chorion, which receives its blood supply from the yolksack. This part of the chorion does not develop vascular villi.

The allantois (al) is a simple vascular sack with a large cavity. Part of its wall is applied to the subzonal membrane, and gives rise to

1 Vide Ercolani, No. 197, and Harting, No. 201, and also Von Baer, Entivicklungsgeschichte table on p. 225, part I., where the importance of the limited area of attachment of the allantois as compared with the yolk-sack is distinctly recognised.

B. III. l6



sh.


FIG. 148. DIAGRAMMATIC LONGITUDINAL SECTION OF A RABBIT'S OVUM AT AN ADVANCED STAGE OF PREGNANCY. (From Kblliker after Bischoff.)

e. embryo ; a. amnion ; a. urachus ; al. allantois with blood-vessels; s/i. subzonal membrane; pi. placental villi ; fd. vascular layer of yolk-sack ; ed. hypoblastic layer of yolk-sack; ed' '. inner portion of hypoblast, and ed". outer portion of hypoblast lining the compressed cavity of the yolksack ; ds. cavity of yolk-sack ; st. sinus terminalis ; r. space filled with fluid between the amnion, the allantois and the yolk-sack.


242


FCETAL MEMBRANES OF THE RODENTIA.


the true chorion, from which there project numerous vascular villi. These fit into corresponding uterine crypts. It seems probable, from Bischoff's and Kolliker's observations, that the subzonal membrane in the area of the placenta becomes attached to the uterine wall, by means of villi, even before its fusion with the allantois. In the later periods of gestation the intermingling of the maternal and fcetal parts of the placenta becomes very close, and the placenta is truly deciduate. The cavity of the allantois persists till birth. Between the yolk-sack, the allantois, and the embryo, there is left a large cavity filled with an albuminous fluid.

The Hare does not materially differ in the arrangement of its foetal membranes from the Rabbit.

In the Rat (Mus decumanus) (fig. 149) the sack of the allantois completely atrophies before the close of fcetal life 1 , and there is developed, at



771


FIG. 149. SECTION THROUGH THE PLACENTA AND ADJACENT PARTS OF A RAT

ONE INCH AND A QUARTER LONG. (From Huxley.)

a. uterine vein ; b. uterine wall ; c. cavernous portion of uterine wall ; d. deciduous portion of uterus with cavernous structure; i. large vein passing to the foetal portion of the placenta ; f. false chorion supplied by vitelline vessels ; k. vitelline vessel ; /. allantoic vessel; g. boundary of true placenta; e, m, m, e. line of junction of the deciduate and non-deciduate parts of the uterine wall.

the junction of the maternal part of the placenta and the unaltered mucous membrane of the uterus, a fold of the mucous membrane which completely encapsules the whole chorion, and forms a separate chamber for it, distinct from the general lumen of the uterus. Folds of this nature, which are specially developed in Man and Apes, are known as a decidua reflexa. The decidua reflexa of the Rat is reduced to extreme tenuity, or even vanishes before the close of gestation.

Guinea-pig. The development of the Guinea-pig is dealt with elsewhere, but, so far as its peculiarities permit a comparison with the Rabbit, the agreement between the two types appears to be fairly close.

1 This is denied by Nasse ; vide Kolliker, No. 183, p. 361.


MAMMALIA.


243


The blastodermic vesicle of the Guinea-pig becomes completely enveloped in a capsule of the uterine wall (decidua reflexa) (fig. 150). The epithelium of the blastodermic vesicle in contact with the uterine wall is not epiblastic, but corresponds with the hypoblast of the yolk-sack of other forms, and the mesoblast of the greater part of the inner side of this becomes richly vascular (yk) ; the vascular area being bounded by a sinus terminalis.

The blastodermic vesicle is so situated within its uterine capsule that the embryo is attached to the part of it adjoining the free side of the uterus. From the opposite side of the uterus, viz. that to which the mesometrium is attached, there grow into the wall

a 11-4


y*-4



of the blastodermic vesicle numerous vascular processes of the uterine wall, which establish at this point an organic connection between the two (pi). The blood-vessels of the blastodermic vesicle (yolksack) stop short immediately around the area of attachment to the uterus ; but at a late period the allantois grows towards, and fuses with this area. The blood-vessels of the allantois and of the uterus become intertwined, and a disc-like placenta more or less similar to that in the Rabbit becomes formed (pi). developed, vanishes completely.

In all the Rodentia the placenta appears to be situated on the mesometric side of the uterus.

Insectivora. In the Mole (Talpa) and the Shrew (Sorex), the foetal membranes are in the main similar to those in the rabbit, and a deciduate discoidal placenta is always present. It may be situated anywhere in the circumference of the uterine tube. The allantoic cavity persists (Owen), but the allantois only covers the placental area of the chorion. The yolk-sack is persistent, and fuses with the non-allantoic part of the subzonal membrane ; which is rendered vascular by its blood-vessels. There would seem to be (Owen) a small decidua reflexa. A similar arrangement is found in the Hedgehog (Erinaceus Europaeus) (Rolleston), in which the placenta occupies the typical dorsal position. It is not clear from Rolleston's description whether the yolk-sack persists till the close of foetal life, but it seems probable that it does so. There is a considerable reflexa which does not,

1 6 2


FIG. 150. DIAGRAMMATIC LONGITUDINAL SECTION OF AN OVUM OF A GUINEA-PIG AND THE ADJACENT UTERINE WALLS AT AN ADVANCED STAGE OF PREGNANCY. (After Bischoff.)

yk. yolk-sack (umbilical vesicle) formed of an external hypoblastic layer (shaded) and an internal mesoblastic vascular layer (black). At the end of this layer is placed the sinus terminalis ; all. allantois ; //. placenta.

The external shaded parts are the uterine walls.


The cavity of the allantois, if



244 HUMAN PLACENTA.


however, cover the whole chorion. In the Tenrec (Centetes) the yolk-sack and non-placental part of the chorion are described by Rolleston as being absent, but it seems not impossible that this may have been owing to the bad state of preservation of the specimen. The amnion is large. In the Cheiroptera ( Vespertilio and Pteropus], the yolk-sack is large, and coalesces with part of the chorion. The large yolk-sack has been observed in Pteropus by Rolleston, and in Vespertilio by Owen. The allantoic vessels supply the placenta only. The Cheiroptera are usually uniparous.

Simiadao and Anthropidae. The foetal membranes of Apes and Man, though in their origin unlike those of the Rodentia and Insectivora, are in their ultimate form similar to them, and may be conveniently dealt with here. The early stages in the development of these membranes in the human embryo have not been satisfactorily observed ; but it is known that the ovum, shortly after its entrance into the uterus, becomes attached to the uterine wall, which in the meantime has undergone considerable preparatory changes. A fold of the uterine wall appears to grow round the blastodermic vesicle, and to form a complete capsule for it, but the exact mode of formation of this capsule is a matter of inference and not of observation. During the first fortnight of pregnancy villi grow out, according to Allen Thomson over its whole surface, but according to Reichert in a ring-like fashion round the edge of the somewhat flattened ovum, and attach it to the uterus. The further history of the early stages is extremely obscure, and to a large extent a matter of speculation : what is known with reference to it will be found in a special section, but I shall here take up the history at about the fourth week.

At this stage a complete chorion has become formed, and is probably derived from a growth of the mesoblast of the allantois (unaccompanied by the hypoblast) round the whole inner surface of the subzonal membrane. From the whole surface of the chorion there project branched vascular processes, covered by an epithelium. The allantois is without a cavity, but a hypoblastic epithelium is present in the allantoic stalk, through which it does not, however, form a continuous tube. The blood-vessels of the chorion are derived from the usual allantoic arteries and vein. The general condition of the embryo and of its membranes at this period is shewn diagrammatically in fig. 147, 5. Around the embryo is seen the amnion, already separated by a considerable interval from the embryo. The yolk-sack is shewn at ds. Relatively to the other parts it is considerably smaller than it was at an earlier stage. The allantoic stalk is shewn at al. Both it and the stalk of the yolk-sack are enveloped by the amnion (ant). The chorion with its vascular processes surrounds the whole embryo.

It may be noted that the condition of the chorion at this stage is very similar to that of the normal diffused type of placenta, described in the sequel.

While the above changes are taking place in the embryonic membranes, the blastodermic vesicle greatly increases in size, and forms a considerable projection from the upper wall of the uterus. Three regions of the uterine


MAMMALIA.


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wall, in relation to the blastodermic vesicle, are usually distinguished ; and since the superficial parts of all of these are thrown off with the afterbirth, each of them is called a decidua. They are represented at a somewhat later stage in fig. 151. There is (i) the part of the wall reflected over the blastodermic vesicle, called the decidua reflexa (dr) ; (2) the part of the wall forming the area round which the reflexa is inserted, called the decidua serotina (<&) ; (3) the general wall of the uterus, not related to the embryo, called the decidua vera (du).

The decidua reflexa and serotina together envelop the chorion, the processes of which fit into crypts in them. At this period both of them are highly and nearly uniformly vascular. The general cavity of the uterus is to a large extent obliterated by the ovum, but still persists as a space filled with mucus, between the decidua reflexa and the decidua vera.

The changes which ensue from this period onwards are fully known. The amriion continues to dilate (its cavity being intensely filled with amniotic fluid) till it comes very close to the chorion (fig. 151, am) ; from which,



FIG. 151. DIAGRAMMATIC SECTION OF PREGNANT HUMAN UTERUS WITH CONTAINED FOETUS. (From Huxley after Longet.)

al. allantoic stalk; nb. umbilical vesicle; am. amnion; ch. chorion; ds. decidua serotina; du. decidua vera; dr. decidua reflexa; /. Fallopian tube; c. cervix uteri; n. uterus; z. fcetal villi of true placenta; z. villi of non-placental part of chorion.

however, it remains separated by a layer of gelatinous tissue. The villi of the chorion in the region covered by the decidua reflexa, gradually cease to be vascular, and partially atrophy, but in the region in contact with the decidua serotina increase and become more vascular and more arborescent (fig. 151, z). The former region becomes known as the chorion lasve, and the latter as the chorion frondosum. The chorion f rondo sum, together with the decidua serotina, gives rise to the placenta.


246 HUMAN PLACENTA.


Although the vascular supply is cut off from the chorion lasve, the processes on its surface do not completely abort. It becomes, as the time of birth approaches, more and more closely united with the reflexa, till the union between the two is so close that their exact boundaries cannot be made out. The umbilical vesicle (fig. 151, ti&), although it becomes greatly reduced in size and flattened, persists in a recognisable form till the time of birth.

As the embryo enlarges, the space between the decidua vera and decidua reflexa becomes reduced, and finally the two parts unite together. The decidua vera is mainly characterised by the presence of peculiar roundish cells in its subepithelial tissue, and by the disappearance of a distinct lining of epithelial cells. During the whole of pregnancy it remains highly vascular. The decidua reflexa, on the disappearance of the vessels in the chorion lieve, becomes non-vascular. Its tissue undergoes changes in the main similar to those of the decidua vera, and as has been already mentioned, it fuses on the one hand with the chorion, and on the other with the decidua vera. The membrane resulting from its fusion with the latter structure becomes thinner and thinner as pregnancy advances, and is reduced to a thin layer at the time of birth.

The placenta has a somewhat discoidal form, with a slightly convex uterine surface and a concave embryonic surface. At its edge it is continuous both with the decidua reflexa and decidua vera. Near the centre of the embryonic surface is implanted the umbilical cord. As has already been mentioned, the placenta is formed of the decidua serotina and the fcetal villi of the chorion frondosum. The fcetal and maternal tissues are far more closely united (fig. 152) than in the forms described above. The villi of the chorion, which were originally comparatively simple, become more and more complicated, and assume an extremely arborescent form. Each of them contains a vein and an artery, which subdivide to enter the complicated ramifications ; and are connected together by a rich anastomosis. The villi are formed mainly of connective tissue, but are covered by an epithelial layer generally believed to be derived from the subzonal membrane ; but, as was first stated by Goodsir, and has since been more fully shewn by Ercolani and Turner, this epithelial layer is really a part of the cellular decidua serotina of the uterine wall, which has become adherent to the villi in the development of the placenta (fig. 161, g). The placenta is divided into a number of lobes, usually called cotyledons, by septa which pass towards the chorion. These septa, which belong to the serotina, lie between the arborescent villi of the chorion. The cotyledons themselves consist of a network of tissue permeated by large vascular spaces, formed by the dilatation of the maternal blood-vessels of the serotina, into which the ramifications of the fcetal villi project. In these spaces they partly float freely, and partly are attached to delicate trabecuke of the maternal tissue (fig. 161, G). They are, of course, separated from the maternal blood by the uterine epithelial layer before mentioned. The blood is brought to the maternal part of the placenta by spirally coiled arteries, which do not divide into capillaries, but



MAMMALIA.


247


open into the large blood-spaces already spoken of. From these spaces there pass off oblique utero-placental veins, which pierce the serotina, and form a system of large venous sinuses in the adjoining uterine wall (fig. 152, F), and eventually fall into the general uterine venous system. At birth the



FIG. 151. SECTION OF THE HUMAN UTERUS AND PLACENTA AT THE THIRTIETH WEEK OF PREGNANCY. (From Huxley after Ecker.)

A. umbilical cord; B. chorion; C. foetal villi separated by processes of the decidua serotina, D ; E, F, G. walls of uterus.

whole placenta, together with the fused decidua vera, and reflexa, with which it is continuous, is shed ; and the blood-vessels thus ruptured are closed by the contraction of the uterine wall.

The fcetal membranes and the placenta of the Simiadas (Turner, No. 225) are in most respects closely similar to those in Man ; but the placenta is, in most cases, divided into two lobes, though in the Chimpanzee, Cynocephalus, and the Apes of the New World, it appears to be single.

The types of deciduate placenta so far described, are usually classified by anatomists as discoidal placentas, although it must be borne in mind that they differ very widely. In the Rodentia, Insectivora, and Cheiroptera there is a (usually) dorsal placenta, which is co-extensive with the area of contact between the allantois and the subzonal membrane, while the yolk-sack adheres to a large part of the subzonal membrane. In Apes and Man the allantois spreads over the whole inner surface of the subzonal membrane ; the placenta is on the ventral side of the embryo, and occupies only a small part of the surface of the allantois. The placenta of Apes and Man might be


248 THE ZONARY PLACENTA.

called metadiscoidal, in order to distinguish it from the primitive discoidal placenta of the Rodentia and Insectivora.

In the Armadilloes (Dasypus) the placenta is truly discoidal and deciduate (Owen and Kolliker). Alf. Milne Edwards states that in Dasypus novemcinctus the placenta is zonary, and both Kolliker and he found four embryos in the uterus, each with its own amnion, but the placenta of all four united together ; and all four enclosed in a common chorion. A reflexa does not appear to be present. In the Sloths the placenta approaches the discoidal type (Turner, No. 218). It occupies in Cholaspus Hoffmanni about fourfifths of the surface of the chorion, and is composed of about thirty-four discoid lobes. It is truly deciduate, and the maternal capillaries are replaced by a system of sinuses (fig. 161). The amnion is close to the inner surface of the chorion. A dome-shaped placenta is also found amongst the Edentata in Myrmecophaga and Tamandua (Milne Edwards, No. 208).

Zonary Placenta. Another form of deciduate placenta is known as the zonary. This form of placenta occupies a broad zone of the chorion, leaving the two poles free. It is found in the Carnivora, Hyrax, Elephas, and Orycteropus.

It is easy to understand how the zonary placenta may be derived from the primitive arrangement of the membranes (vide p. 240) by the extension of a discoidal placental area to a zonary area, but it is possible that some of the types of zonary placenta may have been evolved from the concentration of a diffused placenta (vide p. 261) to a zonary area. The absence of the placenta at the extreme poles of the chorion is explained by the fact of their not being covered by a reflection of the uterine mucous membrane. In the later periods of pregnancy the placental area becomes, however, in most forms much more restricted than the area of contact between the uterus and chorion.

In the Dog 1 , which may be taken as type, there is a large vascular yolksack formed in the usual way, which does not however fuse with the chorion. It extends at first quite to the end of the citron-shaped ovum, and persists till birth. The allantois first grows out on the dorsal side of the embryo, where it coalesces with the subzonal membrane, over a small discoidal area.

Before the fusion of the allantois with the subzonal membrane, there grow out from the whole surface of the external covering of the ovum, except the poles, numerous non-vascular villi, which fit into uterine crypts. When the allantois adheres to the subzonal membrane vascular processes grow out from it into these villi. The vascular villi so formed are of course at first confined to the disc-shaped area of adhesion between the allantois and the subzonal membrane ; and there is thus formea a rudimentary discoidal placenta, closely resembling that of the Rodentia. The view previously stated, that the zonary placenta is derived from the discoidal one, receives from this fact a strong support.

The cavity of the allantois is large, and its inner part is in contact with

1 Vide Bischoff, No. 175.




MAMMALIA. 249


the amnion. The area of adhesion between the outer part of the allantois and subzonal membrane gradually spreads over the whole interior of the subzonal membrane, and vascular villi are formed over the whole area of adhesion except at the two extreme poles of the egg. The last part to be covered is the ventral side where the yolk-sack adjoins the subzonal membrane.

During the extension of the allantois its cavity persists, and its inner part covers not only the amnion, but also the yolk-sack. It adheres to the amnion and supplies it with blood-vessels (Bischoff).

With the full growth of the allantois there is formed a broad placental zone, with numerous branched villi, fitting into corresponding pits which become developed in the uterine walls. The maternal and fcetal structures become closely interlocked and highly vascular ; and at birth a large part of the maternal part is carried away with the placenta ; some of it however still remains attached to the muscular wall of the uterus. The villi of the chorion do not fit into uterine glands. The zone of the placenta diminishes greatly in proportion to the chorion as the latter elongates, and at the full time the breadth of the zone is not more than about one-fifth of the whole length of the chorion.

At the edge of the placental zone there is a very small portion of the uterine mucous membrane reflected over the non-placental part of the chorion, which forms a small reflexa analogous with the reflexa in Man.

The Carnivora generally closely resemble the Dog, but in the Cat the whole of the maternal part of the placenta is carried away with the fcetal parts, so that the placenta is more completely deciduate than in the Dog. In the Grey Seal (Halichcerus gryphus, Turner, No. 219) the general arrangement of the foetal membranes is the same as in the other groups of the Carnivora, but there is a considerable reflexa developed at the edge of the placenta. The fcetal part of the placenta is divided by a series of primary fissures which give off secondary and tertiary fissures. Into the fissures there pass vascular laminae of the uterine wall. The general surface of the foetal part of the placenta between the fissures is covered by a greyish membrane formed of the coalesced terminations of the fcetal villi.

The structure of the placenta in Hyrax is stated by Turner (No. 221) to be very similar to that in the Felidae. The allantoic sack is large, and covers the whole surface of the subzonal membrane. The amnion is also large, but the yolk-sack would seem to disappear at an early stage, instead of persisting, as in the Carnivora, till the close of fcetal life.

The Elephant (Owen, Turner, Chapman) is provided with a zonary deciduate placenta, though- a villous patch is present near each pole of the chorion.

Turner (No. 220) has shewn that in Orycteropus there is present a zonary placenta, which differs however in several particulars from the normal zonary placenta of the Carnivora ; and it is even doubtful whether it is truly deciduate. There is a single embryo, which fills up the body of the uterus and also projects into only one of the horns. The placenta forms a


2$0 PLACENTA OF THE UNGULATA.

broad median zone, leaving the two poles free. The breadth of the zone is considerably greater than is usual in Carnivora, one-half or more of the whole longitudinal diameter of the chorion being occupied by the placenta. The chorionic villi are arborescent, and diffusely scattered, and though the maternal and fcetal parts are closely interwoven, it has not been ascertained whether the adhesion between them is sufficient to cause the maternal subepithelial tissue to be carried away with the fcetal part of the placenta at birth. The allantois is adherent to the whole chorion, the nonplacental parts of which are vascular. In the umbilical cord a remnant of the allantoic vesicle was present in the embryos observed by Turner, but in the absence of a large allantoic cavity the Cape Ant-eater differs greatly from the Carnivora. The amnion and allantois were in contact, but no yolk sack was observed.

Non-deciduate placenta. The remaining Mammalia are characterized by a non-deciduate placenta ; or at least by a placenta in which only parts of the maternal epithelium and no vascular maternal structures are carried away at parturition. The non-deciduate placentae are divided into two groups : (i) The polycotyledonary placenta, characteristic of the true Ruminantia (Cervidae, Antilopidae, Bovida?, Camelopardalidae) ; (2) the diffused placenta found in the other non-deciduate Mammalia, viz. the Perissodactyla, the Suidae, the Hippopotamidae, the Tylopoda, the Tragulidae, the Sirenia, the Cetacea, Manis amongst the Edentata, and the Lemuridae. The polycotyledonary form is the most differentiated ; and is probably a modification of the diffused form. The diffused non-deciduate placenta is very easily derived from the primitive type (p. 240) by an extension of the allantoic portion of the chorion ; and the exclusion of the yolk-sack from any participation in forming the chorion.

The possession in common of a diffused type of placenta is by no means to be regarded as a necessary proof of affinity between two groups, and there are often, even amongst animals possessing a diffused form of placenta, considerable differences in the general arrangement of the embryonic membranes.

Ungulata. Although the Ungulata include forms with both cotyledonary and diffused placentae, the general arrangement of the embryonic membranes is so similar throughout the group, that it will be convenient to commence with a description of them, which will fairly apply both to the Ruminantia and to the other forms.

The blastodermic vesicle during the early stages of development lies freely in the uterus ; and no non-vascular villi, similar to those of the Dog or the Rabbit, are formed before the appearance of the allantois. The blastodermic vesicle has at first the usual spherical form, but it grows out at an early period, and with prodigious rapidity, into two immensely long horns ; which in cases where there is only one embryo are eventually prolonged for the whole length of the two horns of the uterus. The embryonic area is formed in the usual way, and its long axis is placed at right angles to that of the vesicle. On the formation of an amnion there



MAMMALIA. 251


is formed the usual subzonal membrane, which soon becomes separated by a considerable space from the yolk-sack (fig. 153). The yolk-sack is, how


FIG. 153. EMBRYO AND FOETAL MEMBRANES OF A YOUNG EMBRYO ROE-DEER.

(After Bischoff.)

yk. yolk-sack; all. allantois just sprouting as a bilobed sack.

ever, continued into two elongated processes (yk), which pass to the two extremities of the subzonal membrane. It is supplied with the normal blood-vessels. As soon as the allantois appears (fig. 153 all], it grows out into a right and a left process, which rapidly fill the whole free space within the subzonal membrane and in many cases, e.g. the Pig (Von Baer), break through the ends of the membrane, from which they project as the diverticula allantoidis. The cavity of the allantois remains large, but the lining of hypoblast becomes separated from the mesoblast, owing to the more rapid growth of the latter. The mesoblast of the allantois applies itself externally to the subzonal membrane to form the chorion 1 , and internally to the amnion, the cavity of which remains very small. The chorionic portion of the allantoic mesoblast is very vascular, and that applied to the amnion also becomes vascular in the later developmental periods.

The horns of the yolk-sack gradually atrophy, and the whole yolksack disappears some time before birth.

Where two or more embryos are present in the uterus, the chorions of the several embryos may unite where they are in contact.

From the chorion there grow out numerous vascular villi, which fit into corresponding pits in the uterine walls. According to the distribution of these villi, the allantois is either diffused or polycotyledonary.

The pig presents the simplest type of diffused placenta. The villi of

1 According to Bischoff the subzonal membrane atrophies, leaving the allantoic mesoblast to constitute the whole chorion.


252


PLACENTA OF THE UNGULATA.


the surface of the chorion cover a broad zone, leaving only the two poles free; their arrangement differs therefore from that in a zonary placenta in the greater breadth of the zone covered by them. The villi have the form of simple papilla;, arranged on a series of ridges, which are highly



Kit;. 154. PORTION OF THE INJECTED CHORION OF A PIG, SLIGHTLY MAGNIFIED.

(From Turner.)

The figure shews a minute circular spot (l>) (enclosed by a vascular ring) from which villous ridges (r) radiate.

vascular as compared with the intervening valleys. If an injected chorion is examined (fig. 154^ certain clear non-vascular spots are to be seen (b), from which the ridges of villi radiate. The surface of the uterus adapts itself exactly to the elevations of the chorion ; and the furrows which receive the



155. SURFACE-VIEW OF THE INJECTED UTERINE MUCOSA OF A GRAVID PIG.

(From Turner.)

The fig. shews a circular non-vascular spot where a gland opens (g ) surrounded by numerous vascular crypts (cr).


MAMMALIA.


253


chorionic ridges are highly vascular (fig. 155). On the other hand, there are non-vascular circular depressions corresponding to the non-vascular areas on the chorion ; and in these areas, and in these alone, the glands of the uterus open (fig. 155 g) (Turner). The maternal and foetal parts of the placenta in the pig separate with very great ease.



FIG. 156. VERTICAL SECTION THROUGH THE INJECTED PLACENTA OF A MARE.

(From Turner.)

ch. chorion with its villi partly in situ and partly drawn out of the crypts (cr) ; E. loose epithelial cells which formed the lining of the crypt; g. uterine glands; v. blood-vessels.

In the mare (Turner), the foetal villi are arranged in a less definite zonary band than in the pig, though still absent for a very small area at both poles of the chorion, and also opposite the os uteri. The filiform villi, though to the naked eye uniformly scattered, are, when magnified, found to be clustered together in minute cotyledons, which fit into corresponding uterine crypts (fig. 156). Surrounding the uterine crypts are reticulate ridges on which are placed the openings of the uterine glands. The remaining Ungulata with diffused placentas do not differ in any important particulars from those already described.

The polycotyledonary form of placenta is found in the Ruminantia alone. Its essential character consists in the foetal villi not being uniformly distributed, but collected into patches or cotyledons which form as it were so many small placentae (fig. 157). The foetal villi of these patches fit into corresponding pits in thickened patches of the wall of the uterus (figs. 158 and 159). In many cases (Turner), the interlocking of the maternal and foetal structures is so close that large parts of the maternal


254


PLACENTA OF THE UNGULATA.


epithelium are carried away when the foetal villi are separated from the uterus. The glands of the uterus open in the intervals between the cotyledons. The character of the cotyledons differs greatly in different types. The maternal parts are cup-shaped in the sheep, and mushroomshaped in the cow. There are from 60100 in the cow and sheep, but



Ch


FIG. 157. UTERUS OF A Cow IN THE MIDDLE OF PREGNANCY LAID OPEN.

(From Huxley after Colin.) V. vagina; U. uterus; Ch. chorion; C\ uterine cotyledons; C 2 . fcetal cotyledons.



FIG. 158. COTYLEDON OF A Cow, THE FCETAL AND MATERNAL PARTS HALF

SEPARATED. (From Huxley after Colin.) u. uterus; Ch. chorion; C 1 . maternal part of cotyledon; C 2 . fetal part.


MAMMALIA.


255


only about five or six in the Roe-deer. In the Giraffe there are, in addition to larger and smaller cotyledons, rows and clusters of short villi, so that the placenta is more or less intermediate between the polycotyledonary and diffused types (Turner). A similarly intermediate type of placenta is found in Cervus mexicanus (Turner).



FIG. 159. SEMI-DIAGRAMMATIC VERTICAL SECTION THROUGH A PORTION OF A

MATERNAL COTYLEDON OF A SHEEP. (From Turner.)

cr. crypts ; e. epithelial lining of crypts ; v. veins and c. curling arteries of subepithelial connective tissue.

The groups not belonging to the Ungulata which are characterized by the possession of a diffused placenta are the Sirenia, the Cetacea, Manis, and the Lemuridae.

Sirenia. Of the Sirenia, the placentation of the Dugong is known from some observations of Harting (No. 201).

It is provided with a diffuse and non-deciduate placenta ; with the villi generally scattered except at the poles. The umbilical vesicle vanishes early.

Cetacea. In the Cetacea, if we may generalize from Turner's observations on Orca Gladiator and the Narwhal, and those of Anderson (No. 191) on Platanista and Orcella, the blastodermic vesicle is very much elongated, and prolonged unsymmetrically into two horns. The mesoblast (fig. 160) of the allantois would appear to grow round the whole inner surface of the subzonal membrane, but the cavity of the allantois only persists as a widish sack on the ventral aspect of the embryo (al). The amnion (am) is enormous, and is dorsally in apposition with, and apparently coalesces with the chorion, and ventrally covers the inner wall of the persistent allantoic sack. The chorion, except for a small area at the two poles and opposite the os uteri, is nearly uniformly covered with villi, which are more nume


256


DIFFUSED PLACENTA.


rous than in fig. 160. In the large size of the amnion, and small dimensions of the persistent allantoic sack, the Cetacea differ considerably from the Ungulata.


cli



FIG. 160. DIAGRAM OF THE FCETAL MEMBRANES IN ORCA GLADIATOR.

(From Turner.) ck. chorion; am. amnion; al. allantois; E. embryo.

Manis. Manis amongst the Edentata presents a type of diffused placenta 1 . The villi are arranged in ridges which radiate from a non-villous longitudinal strip on the concave surface of the chorion.

Manis presents us with the third type of placenta found amongst the Edentata. On this subject, I may quote the following sentence from Turner (Journal of Anat. and Phys., vol. x., p. 706).

"The Armadilloes (Dasypus), according to Professor Owen, possess a single, thin, oblong, disc-shaped placenta ; a specimen, probably Dasypus gymnurus, recently described by Kolliker 2 , had a transversely oval placenta, which occupied the upper rds of the uterus. In Manis, as Dr Sharpey has shewn, the placenta is diffused over the surfaces of the chorion and uterine mucosa. In Myrmecophaga and Tamandua, as MM. Milne Edwards have pointed out, the placenta is set on the chorion in a dome-like manner. In the Sloths, as I have elsewhere described, the placenta is dome-like in its general form, and consists of a number of aggregated, discoid lobes. In Orycteropus, as I have now shewn, the placenta is broadly zonular. "

Lemuridae. The Lemurs in spite of their affinities with the Primates and Insectivora have, as has been shewn by Milne Edwards and Turner, an apparently very different form of placenta. There is only one embryo, which occupies the body and one of the cornua of the uterus. The yolk-sack disappears early, and the allantois (Turner) bulges out into a right and left lobe, which meet above the back of the embryo. The cavity of the allantois persists, and the mesoblast of the outer wall fuses with the subzonal membrane (the hypoblastic epithelium remaining distinct) to give rise to the chorion.

On the surface of the chorion are numerous vascular villi, which fit into uterine crypts. They are generally distributed, though absent at the two

1 The observations on this head were made by Sharpey, and are quoted by Huxley (No. 202) and with additional observations by Turner in his Memoir on the placentalion of the Sloths. Anderson (No. 191) has also recently confirmed Sharpey's account of the diffused character of the placenta of Manis.

  • Entwicklungsgcschichte des Menschen, etc., 2nd ed., p. 362. Leipzig, 1876.


MAMMALIA. 257


ends of the chorion and opposite the os uteri. Their distribution accords with Turner's diffused type. Patches bare of villi correspond with smooth areas on the surface of the uterine mucosa in which numerous utricular glands open. There is no reflexa.

Although the Lemurian type of placenta undoubtedly differs from that of the Primates, it must be borne in mind that the placenta of the Primates may easily be conceived to be derived from a Lemurian form of placenta. It will be remembered that in Man, before the true placenta becomes developed, there is a condition with simple vascular villi scattered over the chorion. It seems very probable that this is a repetition of the condition of the placenta of the ancestors of the Primates which has probably been more or less retained by the Lemurs. It was mentioned above that the resemblance between the metadiscoidal placenta of Man and that of the Cheiroptera, Insectivora and Rodentia is rather physiological than morphological.


Comparative histology of the Placenta.

It does not fall within the province of this work to treat from a histological standpoint the changes which take place in the uterine walls during pregnancy. It will, however, be convenient to place before the reader a short statement of the relations between the maternal and fetal tissues in the different varieties of placenta. This subject has been admirably dealt with by Turner (No. 222), from whose paper fig. 161 illustrating this subject is taken.

The simplest known condition of the placenta is that found in the pig (B). The papilla-like fcetal villi fit into the maternal crypts. The villi (v) are formed of a connective tissue cone with capillaries, and are covered by a layer of very flat epithelium (e) derived from the subzonal membrane. The maternal crypts are lined by the uterine epithelium (e'\ immediately below which is a capillary flexus. The maternal and fcetal vessels are here separated by a double epithelial layer. The same general arrangement holds good in the diffused placentae of other forms, and in the polycotyledonary placenta of the Ruminantia, but the fcetal villi (C) in the latter acquire an arborescent form. The maternal vessels retain the form of capillaries.

In the deciduate placenta a considerably more complicated arrangement is usually found. In the typical zonary placenta of the fox and cat (D and E), the maternal tissue is broken up into a complete trabecular meshwork, and in the interior of the trabeculae there run dilated maternal capillaries (</). The trabeculae are covered by a more or less columnar uterine epithelium (<?'), and are in contact on every side with fcetal villi. The capillaries of the fcetal villi preserve their normal size, and the villi are covered by a flat epithelial layer (e).

In the sloth (F) the maternal capillaries become still more dilated, and the epithelium covering them is formed of very flat polygonal cells.

In the human placenta (G), as in that of Apes, the greatest modification

B. III. 17


258


HISTOLOGY OF THE PLACENTA.






M

1C

gy?

^1

T^-Tr- ' ~

' ^v\v( r' /}&

M

K 5^

J*



^


IK;. iCn. DIA<;KAMMATIC REPRESENTATIONS OK THE MINUTE STRUCTURE OK i m I'l \>-\.;\\.\. (From Turner.)


MAMMALIA. 259


F. the foetal ; M. the maternal placenta ; e. epithelium of chorion ; ^. epithelium of maternal placenta; d. fcetal blood-vessels; d'. maternal blood-vessels; v. villus.

A. Placenta in its most generalized form.

B. Structure of placenta of a Pig.

C. Structure of placenta of a Cow.

D. Structure of placenta of a Fox.

E. Structure of placenta of a Cat.

F. Structure of placenta of a Sloth. On the right side of the figure the flat maternal epithelial cells are shewn in situ. On the left side they are removed, and the dilated maternal vessel with its blood-corpuscles is exposed.

G. Structure of Human placenta. In addition to the letters already referred to ds, ds. represents the decidua serotina of the placenta; /, t. trabeculse of serotina passing to the foetal villi; ca. curling artery ; up. utero-placental vein; x. a prolongation of maternal tissue on the exterior of the villus outside the cellular layer e', which may represent either the endothelium of the maternal blood-vessel or delicate connective tissue belonging to the serotina, or both. The layer e' represents maternal cells derived from the serotina. The layer of fcetal epithelium cannot be seen on the villi of the fully-formed human placenta.

is found in that the maternal vessels have completely lost their capillary form, and have become expanded into large freely communicating sinuses (d'). In these sinuses the fcetal villi hang for the most part freely, though occasionally attached to their walls (/). In the late stages of fcetal life there is only one epithelial layer (/) between the maternal and fcetal vessels, which closely invests the fcetal villi, but, as shewn by Turner and Ercolani, is part of the uterine tissue. In the fcetal villi the vessels retain their capillary form.


Evolution of the Placenta.

From Owen's observations on the Marsupials it is clear that the yolk-sack in this group plays an important, if not the most important part, in absorbing the maternal nutriment destined for the foetus. The fact that in Marsupials both the yolk-sack and the allantois are functional in rendering the chorion vascular makes it d priori probable that this was also the case in the primitive types of the Placentalia, and this deduction is supported by the fact that in the Rodentia, Insectivora and Cheiroptera this peculiarity of the fcetal membranes is actually found. In the primitive Placentalia there was probably present a discoidal allantoic region of the chorion, from which simple fcetal villi, like those of the pig (fig. 161 B), projected into uterine crypts ; but it is not certain how far the umbilical part of the chorion, which was no doubt vascular, may also have been

172


26O EVOLUTION OF THE PLACENTA.

villous. From such a primitive type of foetal membranes divergences in various directions have given rise to the types of foetal membranes now existing.

In a general way it may be laid down that variations in any direction which tended to increase the absorbing capacities of the chorion would be advantageous. There are two obvious ways in which this might be done, viz. (i) by increasing the complexity of the fcetal villi and maternal crypts over a limited area, (2) by increasing the area of the part of the chorion covered by placental villi. Various combinations of the two processes would also of course be advantageous.

The most fundamental change which has taken place in all the existing Placentalia is the exclusion of the umbilical vesicle from any important function in the nutrition of the fcetus.

The arrangement of the fcetal parts in the Rodentia, Insectivora and Cheiroptera may be directly derived from the primitive form by supposing the villi of the discoidal placental area to have become more complex, so as to form a deciduate discoidal placenta ; while the yolk-sack still plays a part, though physiologically an unimportant part, in rendering the chorion vascular.

In the Carnivora again we have to start from the discoidal placenta, as shewn by the fact that the allantoic region of the placenta is at first discoidal (p. 248). A zonary deciduate placenta indicates an increase both in area and in complexity. The relative diminution of the breadth of the placental zone in late fcetal life in the zonary placenta of the Carnivora is probably due to its being on the whole advantageous to secure the nutrition of the fcetus by insuring a more intimate relation between the fcetal and maternal parts, than by increasing their area of contact. The reason of this is not obvious, but as mentioned below, there are other cases where it can be shewn that a diminution in the area of the placenta has taken place, accompanied by an increase in the complexity of its villi.

The second type of differentiation from the primitive form of discoidal placenta is illustrated by the Lemuridae, the Suidae, and Manis. In all these cases the area of the placental villi appears to have increased so as to cover nearly the whole subzonal membrane, without the villi increasing to any great


MAMMALIA. 261


extent in complexity. From the diffused placenta covering the whole surface of the chorion, differentiations appear to have taken place in various directions. The metadiscoidal placenta of Man and Apes, from its mode of ontogeny (p. 248), is clearly derived from a diffused placenta very probably similar to that of Lemurs by a concentration of the foetal villi, which are originally spread over the whole chorion, to a disc-shaped area, and by an increase in their arborescence.

The polycotyledonary forms of placenta are due to similar concentrations of the foetal villi of an originally diffused placenta.

In the Edentata we have a group with very varying types of placenta. Very probably these may all be differentiations within the group itself from a diffused placenta, such as that found in Manis. The zonary placenta of Orycteropus is capable of being easily derived from that of Manis, by the disappearance of the fcetal villi at the two poles of the ovum. The small size of the umbilical vesicle in Orycteropus indicates that its discoidal placenta is not, like that in Carnivora, directly derived from a type with both allantoic and umbilical vascularization of the chorion. The discoidal and dome-shaped placentae of the Armadilloes, Myrmecophaga, and the Sloths may easily have been formed from a diffused placenta, just as the discoidal placenta of the Simiadae and Anthropidse appears to have been formed from a diffused placenta like that of the Lemuridae.

The presence of zonary placentae in Hyrax and Elephas does not necessarily afford any proof of affinity of these types with the Carnivora. A zonary placenta may quite easily be derived from a diffused placenta ; and the presence of two villous patches at the poles of the chorion in Elephas indicates that this was very probably the case with the placenta of this form.

Although it is clear from the above considerations that the placenta is capable of being used to some extent in classification, yet at the same time the striking resemblances which can exist between such essentially different forms of placenta, as for instance those of Man and the Rodentia, are likely to prevent it being employed, except in conjunction with other characters.


262 DEVELOPMENT OF THE GUINEA-PIG.


Special types of development.

The Guinea-pig, Cavia cobaya. Many years ago Bischoff (No. 176) shewed that the development of the guinea-pig was strikingly different from that of other Mammalia. His statements, which were at first received with some doubt, have been in the main fully confirmed by Hensen (No. 182) and Schafer (No. 190), but we are still as far as ever from explaining the mystery of the phenomenon.

The ovum, enclosed by the zona radiata, passes into the Fallopian tube and undergoes a segmentation which has not been studied with great detail. On the close of segmentation, about six days after impregnation, it assumes (Hensen) a vesicular form not unlike that of other Mammalia. To the inner side of one wall of this vesicle is attached a mass of granular cells similar to the hypoblastic mass in the blastodermic vesicle of the rabbit. The egg still lies freely in the uterus, and is invested by its zona radiata. The changes which next take place are in spite of Bischoff's, Reichert's (No. 188) and Hensen's observations still involved in great obscurity. It is certain, however, that during the course of the seventh day a ring-like thickening of the uterine mucous membrane, on the free side of the uterus, gives rise to a kind of diverticulum of the uterine cavity, in which the ovum becomes lodged. Opposite the diverticulum the mucous membrane of the mesometric side of the uterus also becomes thickened, and this thickening very soon (shortly after the seventh day) unites with the wall of the diverticulum, and completely shuts off the ovum in a closed capsule.

The history of the ovum during the earlier period of its inclusion in the diverticulum of the uterine wall is not satisfactorily elucidated. There appears in the diverticulum during the eighth and succeeding days a cylindrical body, one end of which is attached to the uterine walls at the mouth of the diverticulum. The opposite end of the cylinder is free, and contains a solid body.

With reference to the nature of this cylinder two views have been put forward. Reichert and Hensen regard it as an outgrowth of the uterine wall, while the body within its free apex is regarded as the ovum. Bischoff and Schafer maintain that the cylinder itself is the ovum attached to the uterine wall. The observations of the latter authors, and especially those of Schafer, appear to me to speak for the correctness of their view 1 .

The cylinder gradually elongates up to the twelfth day. Before this period it becomes attached by its base to the mesometric thickening of the uterus, and enters into vascular connection with it. During its elongation it

1 Schiifcr's and Hensen's statements are in more or less direct contradiction as to the structure of the ovum after the formation of the embryo; and it is not possible to decide between the two views about the ovum till these points of difference have been cleared up.


MAMMALIA. 263


becomes hollow, and is filled with a fluid not coagulable in alcohol, while the body within its apex remains unaltered till the tenth day.

On this day a cavity develops in the interior of this body which at the same time enlarges itself. The greater part of its wall next attaches itself to the free end of the cylinder, and becomes considerably thickened. The



FIG. 162. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE EMBRYO OF

A GUINEA-PIG WITH ITS MEMBRANES. (After Schafer.)

e. epiblast ; h. hypoblast ; in', amniotic mesoblast ; in" . splanchnic mesoblast ; am. amnion ; ev. cavity of amnion ; all. allantois ; f. rudimentary blastopore ; me. cavity of vesicle continuous with body cavity; mm. mucous membrane of uterus; m'm'. parts where vascular uterine tissue perforates hypoblast of blastodermic vesicle ; vt. uterine vascular tissue ; /. limits of uterine tissue.

remainder of the wall adjoining the cavity of the cylinder becomes a comparatively thin membrane. At the free end of the cylinder there appears on the thirteenth day an embryonic area similar to that of other Mammalia. It is at first round but soon becomes pyriform, and in it there appear a primitive streak and groove ; and on their appearance it becomes obvious that the outer layer of the cylinder is the hypoblast^, instead of, as in all other Mammalia, the epiblast ; and that the epiblast is formed by the wall of the inner vesicle, i.e. the original solid body placed at the end of the cylinder. Thus the dorsal surface of the embryo is turned inwards, and the ventral surface outwards, and the ordinary position of the layers is completely inverted.

1 According to Hensen the hypoblast grows round the inside of the wall of the cylinder from the body which he regards as the ovum. The original wall of the cylinder persists as a very thin layer separated from the hypoblast by a membrane.


264 DEVELOPMENT OF THE GUINEA-PIG.

The previously cylindrical egg next assumes a spherical form, and the mesoblast arises in connection with the primitive streak in the manner already described. A splanchnic layer of mesoblast attaches itself to the inner side of the outer hypoblastic wall of the egg, a somatic layer to the epiblast of the inner vesicle, and a mass of mesoblast grows out into the cavity of the larger vesicle forming the commencement of the allantois. The general structure of the ovum at this stage is represented on fig. 162, copied from Schafer ; and the condition of the whole ovum will best be understood by a description of this figure.

It is seen to consist of two vesicles, (i) an outer larger one (h] the original egg-cylinder united to the mesometric wall of the uterus by n vascular connection at ;';', and (2) an inner smaller one (ev) the originally solid body at the free end of the egg-cylinder. The outer vesicle is formed of (i) an external lining of columnar hypoblast (h) which is either pierced or invaginated at the area of vascular connection with the uterus, and (2) of an inner layer of splanchnic mesoblast (in"} which covers without a break the vascular uterine growth. At the upper pole of the ovum is placed the smaller epiblastic vesicle, and where the two vesicles come together is situated the embryonic area with the primitive streak (_/), and the medullary plate seen in longitudinal section. The thinner wall of the inner vesicle is formed of epiblast and somatic mesoblast, and covers over the dorsal face of the embryo just like the amnion. It is in fact usually spoken of as the amnion. The large cavity of the outer vesicle is continuous with the body cavity, and into it projects the solid mesoblastic allantois (//), so far without hypoblast 1 .

The outer vesicle corresponds exactly with the yolk-sack, and its mesoblastic layer receives the ordinary vascular supply.

The embryo becomes folded off from the yolk-sack in the usual way, but comes to lie not outside it as in the ordinary form, but in its interior, and is connected with it by an umbilical stalk. The yolk-sack forms the substitute for part of the subzonal membrane of other Mammalia. The so-called amnion appears to me from its development and position rather to correspond with the non-embryonic part of the epiblastic wall (true subzonal membrane) of the blastodermic vesicle of the ordinary mammalian forms than with the true amnion ; and a true amnion would seem not to be developed.

The allantois meets the yolk-sack on about the seventeenth day at the region of its vascular connection with the uterine wall, and gives rise to the placenta. A diagrammatic representation of the structure of the embryo at this stage is given in fig. 163.

The peculiar inversion of the layers in the Guinea-pig has naturally excited the curiosity of embryologists, but as yet no satisfactory explanation has been offered of it.

1 Hensen states that the hypoblast never grows into the allantois; while Bischoff, though not very precise on the point, implies that it does ; he states however that it soon disappears.


MAMMALIA.


265



At the time when the ovum first becomes fixed it will be remembered that it resembles the early blastodermic vesicle of the Rabbit, and it is natural to suppose that the apparently hypoblastic mass attached to the inner wall of the vesicle becomes the solid body at the end of the egg-cylinder. This appears to be Bischoff's view, but, as shewn above, the solid mass is really the epiblast ! Is it conceivable that the hypoblast in one species becomes the epiblast in a closely allied species? To my mind it is not conceivable, and I am reduced to the hypothesis, put forward by Hensen, that in the course of the attachment of the ovum to the wall of the uterus a rupture of walls of the blastodermic vesicle takes place, and that they become completely turned inside out. It must be admitted, however, that in the present state of our knowledge of the development of the ovum on the seventh and eighth

days it is not possible to frame a satisfactory explanation how such an inversion can take place.

The Human Embryo. Our knowledge as to the early development of the human embryo is in an unsatisfactory state. The positive facts we know are comparatively few, and it is not possible to construct from them a history of the development which is capable of satisfactory comparison with that in other forms, unless all the early embryos known are to be regarded as abnormal. The most remarkable feature in the development, which was first clearly brought to light by Allen Thomson in 1839, is the very early appearance of branched villi. In the last few years several ova, even younger than those described by Allen Thomson, have been met with, which exhibit this peculiarity.

The best-preserved of these ova is one described by Reichert (No. 237). This ovum, though probably not more than thirteen days old, was completely enclosed by a decidua reflexa. It had (fig. 164 A and B) a flattened oval form, measuring in its two diameters 5*5 mm. and 3-5 mm. The edge was covered with branched villi, while in the centre of each of the flattened surfaces there was a spot free from villi. On the surface adjoining the uterine wall was a darker area (e) formed of two layers of cells, which is interpreted by Reichert as the embryonic area, while the membrane forming


FIG. 163. DIAGRAMMATIC LONGITUDINAL SECTION OF AN OVUM OF A GUINEA-PIG AND THE ADJACENT UTERINE WALLS AT AN ADVANCED STAGE OF PREGNANCY. (After Bischoff.)

yk. inverted yolk-sack (umbilical vesicle) formed of an external hypoblastic layer (shaded) and an internal vascular layer (black). At the end of this layer is placed the sinus terminalis ; all. allantois ; //. placenta.

The external shaded parts are the uterine walls.


2 66 HUMAN OVUM.

the remainder of the ovum, including the branched villi, was stated by Reichert to be composed of a single row of epithelial cells.

Whether or no Reichert is correct in identifying his darker spot as the embryonic area, it is fairly certain from the later observations of Beigel and Lowe (No. 228), Ahlfeld (No. 227), and Kollmann (No. 234) on ova nearly as young as that of Reichert, that the wall of very young ova has a more complicated structure than Reichert is willing to admit. These authors do not however agree amongst themselves, but from Kollmann's description, which appears to me the most satisfactory, it is probable that it is composed of an outer epithelial layer, and an inner layer of connective tissue, and that the connective tissue extends at a very early period into the villi ; so that the latter are not hollow, as Reichert supposed them to be.



FIG. 164. THE HUMAN OVA DURING EARLY STAGES OF DEVELOPMENT.

(From Quain's Anatomy.)

A. and B. Front and side view of an ovum figured by Reichert, supposed to be about thirteen days. e. embryonic area.

C. An ovum of about four or five weeks shewing the general structure of the ovum before the formation of the placenta. Part of the wall of the ovum is removed to shew the embryo in situ, (After Allen Thomson.)

The villi, which at first leave the flattened poles free, seem soon to extend first over one of the flat sides, and finally over the whole ovum (fig. 164 C).

Unless the two-layered region of Reichert's ovum is the embryonic area, nothing which can clearly be identified as an embryo has been detected in these early ova. In an ovum described by Breus (No. 228), and in one described long ago by Wharton- Jones a mass found in the interior of the egg may perhaps be interpreted (His) as the remains of the yolk. It is, however, very probable that all the early ova so far discovered are more or less pathological.

The youngest ovum with a distinct embryo is one described by His (No. 232). This ovum, which is diagrammatically represented in fig. 168 in longitudinal section, had the form of an oval vesicle completely covered by villi, and about 8'5 mm. and $'5 mm. in its two diameters, and flatter on one side than on the other. An embryo with a yolk-sack was attached to the inner side of the flatter wall of the vesicle by a stalk, which must be


MAMMALIA.


267


regarded as the allantoic stalk 1 , and the embryo and yolk-sack filled up but a very small part of the whole cavity of the vesicle.

The embryo, which was probably not quite normal (fig. 165 A), was very imperfectly developed ; a medullary plate was hardly indicated, and,


am..


ch


FIG. 165. THREE EARLY HUMAN EMBRYOS. (Copied from His.) An early embryo described by His from the side. am. amnion; urn. umbilical ch. chorion, to which the embryo is attached by a stalk. Embryo described by Allen Thomson about 12 14 days. urn. umbilical


A.

vesicle

B. vesicle ; md. medullary groove.

C. Young embryo described by His.


mil. umbilical vesicle.


though the mesoblast was unsegmented, the head fold, separating the embryo from the yolk-sack (#;#), was already indicated. The amnion (am] was completely formed, and vitelline vessels had made their appearance.

Two embryos described by Allen Thomson (No. 239) are but slightly older than the above embryos of His. Both of them probably belong to the first fortnight of pregnancy. In both cases the embryo was more or less folded off from the yolk-sack, and in one of them the medullary groove was still widely open, except in the region of the neck (fig. 165 B). The allantoic stalk, if present, was not clearly made out, and the condition of the amnion was also not fully studied. The smaller of the two ova was just 6 mm. in

1 Allen Thomson informs me that he is very confident that such a form of attachment between the hind end of the embryo and the wall of the vesicle, as that described and figured by His in this embryo, did not exist in any of the younger embryos examined by him.


268


HUMAN OVUM.


its largest diameter, and was nearly completely covered with simple villi, more developed on one side than on the other.

In a somewhat later period, about the stage of a chick at the end of the second day, the medullary folds are completely closed, the region of the brain already marked, and the cranial flexure commencing. The mesoblast is divided up into numerous somites, and the mandibular and first two branchial arches are indicated. The embryo is still but incompletely folded off from the yolk-sack below.

In a still older stage the cranial flexure becomes still more pronounced, placing the mid-brain at the end of the long axis of the body. The body also begins to be ventrally curved (fig. 165 C).

Externally human embryos at this age are characterised by the small size of the anterior end of the head.

The flexure goes on gradually increasing, and in the third week of pregnancy in embryos of about 4 mm. the limbs make their appearance. The embryo at this stage (fig. 166), which is about equivalent to that of a



FIG. 166. Two VIEWS OK A HUMAN EMBRYO OF BETWEEN THE THIRD AND

FOURTH WEEK.

A. Side view. (From Kolliker; after Allen Thomson.) a. amnion; b. umbilical vesicle; c, mandibular arch; e. hyoid arch ; f. commencing anterior limb; g. primitive auditory vesicle; h. eye; i. heart.

B. Dorsal view to shew the attachment of the dilated allantoic stalk to the chorion. (From a sketch by Allen Thomson.) am- amnion; all. allantois; ys. yolksack.

chick on the fourth day, resembles in almost every respect the normal embryos of the Amniota. The cranial flexure is as pronounced as usual, and the cerebral region has now fully the normal size. The whole body soon becomes flexed ventrally, and also somewhat spirally. The yolksack (b} forms a small spherical appendage with a long wide stalk, and the embryo (B) is attached by an allantoic stalk with a slight swelling (all], probably indicating the presence of a small hypoblastic diverticulum, to the inner face of the chorion.

A remarkable exception to the embryos generally observed is afforded by an embryo which has been described by Krause (No. 235). In this


MAMMALIA. 269


embryo, which probably belongs to the third week of pregnancy, the limbs were just commencing to be indicated, and the embryo was completely covered by an amnion, but instead of being attached to the chorion by an allantoic cord, it was quite free, and was provided with a small spherical sack-like allantois, very similar to that of a fourth-day chick, projected from its hind end.




FIG. 167. FIGURES SHEWING THE EARLY CHANGES IN THE FORM OF THE HUMAN HEAD. (From Quain's Anatomy.)

A. Head of an embryo of about four weeks. (After Allen Thomson.)

B. Head of an embryo of about six weeks. (After Ecker.)

C. Head of an embryo of about nine weeks.

i. mandibular arch; i'. persistent part of hyomandibular cleft; a. auditory vesicle.

No details are given as to the structure of the chorion or the presence of villi upon it. The presence of such an allantois at this stage in a human embryo is so unlike what is usually found that Krause's statements have been received with considerable scepticism. His even holds that the embryo is a chick embryo, and not a human one ; while Kolliker regards Krause's allantois as a pathological structure. The significance to be attached to this embryo is dealt with below.

A detailed history of the further development of the human embryo does not fall within the province of this work ; while the later changes in the embryonic membranes have already been dealt with (pp. 244 248).

For the changes which take place on the formation of the face I may refer the reader to fig. 167.

The most obscure point connected with the early history of the human ovum concerns the first formation of the allantois, and the nature of the villi covering the surface of the ovum. The villi, if really formed of mesoblast covered by epiblast, have the true structure of chorionic villi ; and can hardly be compared to the early villi of the dog which are derived from the subzonal membrane, and still less to those of the rabbit formed from the zona radiata.

Unless all the early ova so far described are pathological, it seems to


2/0


HUMAN OVUM.



follow that the mesoblast of the chorion is formed before the embryo is definitely established, and even if the pathological character of these ova is admitted, it is nevertheless probable (leaving Krause's embryo out of account), as shewn by the early embryos of Allen Thomson and His, that it is formed before the closure of the medullary groove. In order to meet this difficulty His supposes that the embryo never separates from the blastodermic vesicle, but that the allantoic stalk of the youngest embryo (fig. 168) represents the persistent attachment between the two 1 . His' view has a good deal to be said for it. I would venture, however, to suggest that Reichert's embryonic area is probably not in the twolayered stage, but that a mesoblast has already become established, and that it has grown round the inner face of the FlG> l68> DIAGRAMMATIC LONGIblastodermic vesicle from the (apparent) TUDINAL SECTION OF THE OVUM TO posterior end of the primitive streak, jnnot.-.ggy-. * S A).

This growth I regard as a frecoci^ ^ amnion . A,. um hilical vesicle.

formation of the mesoblast of the allantois

an exaggeration of the early formation of the allantoic mesoblast which is characteristic of the Guinea-pig (vide p. 264). This mesoblast, together with the epiblast, forms a true chorion, so that in fig. 168, and probably also in fig. 164 A and B, a true chorion has already become established. The stalk connecting the embryo with the chorion in His' earliest embryo (fig. 168) is therefore a true allantoic stalk into which the hypoblastic allantoic diverticulum grows in for some distance. How the yolk-sack (umbilical vesicle) is formed is not clear. Perhaps, as suggested by His, it arises from the conversion of a solid mass of primitive hypoblast directly into a yolk-sack. The amnion is probably formed as a fold over the head end of the embryo in the manner indicated in His' diagram (fig. 168 Am}.

These speculations have so far left Krause's embryo out of account. How is this embryo to be treated ? Krause maintains that all the other embryos shewing an allantoic stalk at an early age are pathological. This, though not impossible, appears to me, to say the least of it, improbable ; especially when it is borne in mind that embryos, which have every appearance of being normal, of about the same age and younger than Krause's, have been frequently observed, and have always been found attached to the chorion by an allantoic stalk.

We are thus provisionally reduced to suppose either that the structure figured by Krause is not the allantois, or that it is a very abnormal allantois. It is perhaps just possible that it maybe an abnormally developed hypoblastic vesicle of the allantois artificially detached from the mesoblastic layer, the latter having given rise to the chorion at an earlier date.

1 For a fuller explanation of His' views I must refer the reader to his Memoir (No. j:V2), pp. 170. 171, and to the diagrams contained in it.


MAMMALIA. 2/1


BIBLIOGRAPHY.

General.

(168) K. E. von Baer. Ueb. Entwicklungsgeschichte d. Jhiere. Konigsberg, 1828-1837.

(169) Barry. "Researches on Embryology." First Series. Philosophical Transactions, 1838, Part II. Second Series, Ibid. 1839, Part II. Third Series, Ibid. 1840.

(170) Ed. van Beneden. La maturation deTceuf, la fecondation et les premieres phases du dcveloppement embryonaire d. Mammiferes. Bruxelles, 1875.

(171) Ed. van Beneden. " Recherches sur 1'embryologie des Mammiferes." Archives de Biologie, Vol. I. 1880.

(172) Ed. v. Beneden and Ch. Julin. "Observations sur la maturation etc. de 1'ceuf chez les Cheiropteres." Archives de Biologie, Vol. I. 1880.

(173) Th. L. W. Bischoff. Entwickhmgsgeschichte d. Sdugethiere u. des Menschen. Leipzig, 1842.

(174) Th. L. W. Bischoff. Entwicklungsgeschichte des Kanincheneies. Braunschweig, 1842.

(175) Th. L. W. Bischoff. Entwickhmgsgeschichte des Hundeeies. Braunschweig, 1845.

(176) Th. L. W. Bischoff. Entwickhmgsgeschichte des Meerschweinchens. Giessen. 1852.

(177) Th. L. W. Bischoff. Entwicklungsgeschichte des Rehes. Giessen, -1854.

(178) Th. L. W. Bischoff. " Neue Beobachtungen z. Entwicklungsgesch. des Meerschweinchens." Abh. d. bayr. Akad., Cl. II. Vol. X. 1866.

(179) Th. L. W. Bischoff. Historisch-kritische Bemerkungen z. d. neuesten Mittheilungen rib. d. erste Entwick. d. Sdugethiereier. Miinchen, 1877.

(180) M. Coste. Embryogenie comparee. Paris, 1837.

(181) E. Haeckel. Anthropogenic, Entwicklungsgeschichte des Menschen. Leipzig, 1874.

(182) V. Hensen. "Beobachtungen lib. d. Befrucht. u. Entwick. d. Kaninchens u. Meerschweinchens." Zeit.f. Anat. u. Entwick., Vol. I. 1876.

(183) A. Kolliker. Entwicklungsgeschichte d. Menschen u. d. hoheren Thiere. Leipzig, 1879.

(184) A. Kolliker. "Die Entwick. d. Keimblatter des Kaninchens." Zoologischer Anzeiger, Nos. 61, 62, Vol. Hi. 1880.

(185) N. Lieberkiihn. Ueber d. Keimbltitter d. Siiugethiere. Doctor-Jnbelfeier d. Herrn. H. Nasse. Marburg, 1879.

(186) N. Lieberkiihn. "Z. Lehre von d. Keimblattern d. Saugethiere." Sitz. d. Gesell. z. Beford. d. gesam. Naturwiss. Marburg, No. 3. 1880.

(187) Rauber. "Die erste Entwicklung d. Kaninchens." Sitzungsber. d. naturfor. Gesell. z. Leipzig. 1875.

(188) C. B. Reichert. "Entwicklung des Meerschweinchens." Abh. der. Berl. Akad. 1862.

(189) E. A. S chafer. " Description of a Mammalian ovum in an early condition of development." Proc. Roy. Soc., No. 168. 1876.


2/2 MAMMALIAN BIBLIOGRAPHY.

(190) E. A. Schiifer. " A contribution to the history of development of the guinea-pig." Journal of Anal, and Phys., Vol. x. and xi. 1876 and 1877.

Foetal Membranes and Placenta.

(191) John Anderson. Anatomical and Zoological Researches in Western Yunnan. London, 1878.

(192) K. E. von Baer. Untersuchungen ilber die Gefassverbindung swischen Mutter und Frucht, 1828.

(193) C. G. Carus. Tabulae anatomiam comparalivam illustrantes. 1831, 1840.

(194) H. C. Chapman. "The placenta and generative apparatus of the Elephant." Journ. Acad. Nat. Sc., Philadelphia. Vol. vin. 1880.

(195) C. Creighton. " On the formation of the placenta in the guinea-pig.'.' Journal of Anat. and Phys. , Vol. XII. 1 878.

(196) Ecker. Icones Physiologicae. 1852-1859.

(197) G. B. Ercolani. The utricular glands of the uterus, etc., translated from the Italian under the direction of H. O. Marcy. Boston, 1880. Contains translations of memoirs published in the Mem. delf Accad. d. Scienze d. Bologna, and additional matter written specially for the translation.

(198) G. B. Ercolani. Nuove ricerche sulla placenta nei pesci cartilaginosi e net mammiferi. Bologna, 1880.

(199) Eschricht. De organis quae respirationi et nutritioni fcetus Mammalium inservinnt. Hafniae, 1837.

(200) A. H. Garrod and W. Turner. "The gravid uterus and placenta of Hyomoschus aquaticus." Proc. Zool. Soc., London, 1878.

(201) P. Hart ing. Het ei en de placenta van Halicore Dtigong. Inaug. diss. Utrecht. "On the ovum and placenta of the Dugong." Abstract by Prof. Turner. Joitrnal of Anat. and Phys., Vol. xm.

(202) Th. H. Huxley. The Elements of Comparative Anatomy. London, 1864.

(203) A. Kolliker. " Ueber die Placenta der Gattung Tragulus." Verh. der Wiirzb. phys.-med. Gesellschaft, Bd. x.

(204) C. D. Meigs. "On the reproduction of the Opossum (Didelphis Virginiana)." Amer. Phil. Soc. Trans., Vol. x. 1853.

(205) H.Milne-Edwards. " Sur la Classification Naturelle." Ann. Sciences Nat., SeY. 3, Vol. i. 1844.

(206) Alf. Milne-Edwards. "Recherches sur la famille des Chevrotains." Ann. des Sciences Nat., Series V., Vol. II. 1864.

(207) Alf. Milne-Edwards. " Observations sur quelques points de PEmbryologie des Lemuriens, etc." Ann. Sci. Nat., Ser. v., Vol. xv. 1872.

(208) Alf. Milne- Edwards. " Sur la conformation du placenta chez le Tamandua." Ann. des Sci. Nat., xv. 1872.

(209) Alf. Milne-Edwards. " Recherches s. 1. enveloppes foetales du Tatou a neuf bandes." Ann. Sci. Nat., Ser. vi., Vol. vin. 1878.

(210) R. Owen. "On the generation of Marsupial animals, with a description of the impregnated uterus of the Kangaroo." Phil. Trans., 1834.

(211) R. Owen. "Description of the membranes of the uterine foetus of the Kangaroo." Mag. Nat. Hist., Vol. I. 1837.




MAMMALIA. 273


(212) R. Owen. "On the existence of an Allantois in a foetal Kangaroo (Macropus major)." Zool. Soc. Proc., V. 1837.

(213) R. Owen. "Description of the foetal membranes and placenta of the Elephant." Phil. Trans., 1857.

(214) R.Owen. On the Anatomy of Vertebrates, Vol. in. London, 1868.

(215) G. Rolleston. " Placental structure of the Tenrec, etc." Transactions of the Zoological Society, Vol. v. 1866.

(216) W. Turner. "Observations on the structure of the human placenta." Journal of Anat. and Phys., Vol. VII. 1868.

(217) W. Turner. "On the placentation of the Cetacea." Trans. Roy. Soc. Edinb., Vol. XXVI. 1872.

(218) W. Turner. "On the placentation of Sloths (Cholcepus Hoffrnanni)." Trans, of R. Society of Edinburgh, Vol. xxvii. 1875.

(219) W. Turner. "On the placentation of Seals (Halichcerus gryphus)." Trans, of R. Society of Edinburgh, Vol. xxvii. 1875.

(220) W. Turner. "On the placentation of the Cape Ant-eater (Orycteropus capensis)." Journal of Anat. and Phys., Vol. X. 1876.

(221) W. Turner. Lectures on the Anatomy of the Placenta. First Series. Edinburgh, 1876.

(222) W.Turner. "Some general observations on the placenta, with special reference to the theory of Evolution." Journal of Anat. and Phys., Vol. xi. 1877.

(223) W. Turner. "On the placentation of the Lemurs." Phil. Trans., Vol. 166, p. 2. 1877.

(224) W.Turner. " On the placentation of Apes." Phil. Trans., 1878.

(225) W. Turner. "The cotyledonary and diffused placenta of the Mexican deer (Cervus Americanus). " Journal of Anat. and Phys., Vol. xiii. 1879.

Human Embryo.

(226) Fried. Ahlfeld. " Beschreibung eines sehr kleinen menschlichen Eies." Archivf. Gynaekologie, Bd. xiii. 1878.

(227) Herm. Beigel und Ludwig Loewe. "Beschreibung eines menschlichen Eichens aus der zweiten bis dritten Woche der Schwangerschaft." Archiv f. Gynaekologie, Bd. xn. 1877.

(228) K. Breus. " Ueber ein menschliches Ei aus der zweiten Woche der Graviditat." Wiener medicinische Wochenschrift, 1877.

(229) M. Coste. Histoire generale et particuliere du developpement des corps organises, 1847-59.

(230) A. Ecker. Icones Physiologicae. Leipzig, 1851-1859.

(231) V. Hensen. " Beitrag z. Morphologic d. Korperform u. d. Gehirns d. menschlichen Embryos." Archivf. Anat. u. Phys., 1877.

(232) W. His. Anatomic menschticher Embryonen, Part I. Embryonen d. ersten Monats. Leipzig, 1880.

(233) J. Kollmann. "Die menschlichen Eier von 6 MM. Grosse." Archivf. Anat. und Phys., 1879.

(234) W. Krause. " Ueber d. Allantois d. Menschen." Archiv f. Anat. und Phys., 1875.

(235) W. Krause. " Ueber zwei fruhzeitige menschliche Embryonen." Zeit. f. wiss. Zool., Vol. xxxv. 1880.

B. III. 1 8


274 MAMMALIAN BIBLIOGRAPHY.

(236) L. Loewe. " Im Sachen cler Eihaute jiingster menschlicher Eier. " Archiv for Gynaekologie, Bd. xiv. 1879.

(237) C. B. Reichert. " Beschreibung einer fruhzeitigen menschlichen Frucht im blaschenformigen Bildungszustande (sackfdrmiger Keim von Baer) nebst vergleichenden Untersuchungen liber die blaschenformigen Friichte der Saugethiere und des Menschen. " Abhandlitngen der konigL Akad. d. Wiss. zu Berlin, 1873.

(238) Allen Thomson. "Contributions to the history of the structure of the human ovum and embryo before the third week after conception ; with a description of some early ova." Edinburgh Med. Surg. Journal, Vol. Lll. 1839.


CHAPTER XI. COMPARISON OF THE FORMATION OF THE GERMINAL LAYERS AND OF THE EARLY STAGES IN THE DEVELOPMENT OF VERTEBRATES

ALTHOUGH the preceding chapters of this volume contain a fairly detailed account of the early developmental stages of different groups of the Chordata, it will nevertheless be advantageous to give at this place a short comparative review of the whole subject.

In this review only the most important points will be dwelt upon, and the reader is referred for the details of the processes to the sections on the development of the individual groups.

The subject may conveniently be treated under three heads.

(1) The formation of the gastrula and behaviour of the blastopore : together with the origin of the hypoblast.

(2) The mesoblast and notochord.

(3) The epiblast.

At the close of the chapter is a short summary of the organs derived from the several layers, together with some remarks on the growth in length of the vertebrate embryo, and some suggestions as to the origin of the allantois and amnion.

Formation of the gastrula. Amphioxus is the type in which the developmental phenomena are least interfered with by the presence of food-yolk.

In this form the segmentation results in a uniform, or nearly uniform, blastosphere, one wall of which soon becomes thickened and invaginated, giving rise to the hypoblast ; while the larva takes the form of a gastrula, with an archenteric cavity opening by a blastopore. The blastopore rapidly narrows, while the

1 8 2


276


THE GASTRULA OF AMPHIOXUS.


embryo assumes an elongated cylindrical form with the blastopore at its hinder extremity (fig. 169 A). The blastopore now passes to the dorsal surface, and by the flattening of this surface a medullary plate is formed extending forwards from the blasto


FIG. 169. EMBRYOS OF AMPHIOXUS. (After Kowalevsky.) The parts in black with white lines are epiblastic; the shaded parts are hypoblastic.

A. Gastrula stage in optical section.

B. Slightly later stage after the neural plate np has become differentiated, seen as a transparent object from the dorsal side.

C. Lateral view of a slightly older larva in optical section.

D. Dorsal view of an older larva with the neural canal completely closed except for a small pore (no) in front.

E. Older larva seen as a transparent object from the side.

bl. blastopore (which becomes in D the neurenteric canal) ; ne. neurenteric canal ;

//. neural or medullary plate; no. anterior opening of neural canal; ch. notochord;

so 1 , so", first and second mesoblastic somites.

pore (fig. 169 B). On the formation of the medullary groove and its conversion into a canal, the blastopore opens into this canal, and gives rise to a neurenteric passage, leading from the neural canal into the alimentary tract (fig. 169 C and E). At a later period this canal closes, and the neural and alimentary canals become separated.

Such is the simple history of the layers in Amphioxus. In the simplest types of Ascidians the series of phenomena is almost the same, but the blastopore assumes a more definitely dorsal position.


COMPARISON OF THE GERMINAL LAYERS.


2/7


Here also the blastopore lies at the hinder end of the medullary groove, and on the closure of the groove becomes converted into a neurenteric passage.

In the true Vertebrates the types which most approach Amphioxus are the Amphibia, Acipenser and Petromyzon. We may take the first of these as typical (though Petromyzon is perhaps still more so) and fig. 170 A B C D represents four diagrammatic longitudinal vertical sections through a form

A C



FIG. 170. DIAGRAMMATIC LONGITUDINAL SECTIONS THROUGH THE EMBRYO OF BOMBINATOR AT TWO STAGES, TO SHEW THE FORMATION OF THE GERMINAL LAYERS. (Modified from Gotte.)

ep. epiblast ; m. dorsal mesoblast ; m'. ventral mesoblast ; hy. hypoblast ; yk. yolk ; x. point of junction of the epiblast and hypoblast at the dorsal side of the blastopore ; al. mesenteron ; sg. segmentation cavity.


378 THE GASTRULA OF AMPHIBIA.

belonging to this group (Bombinator). The food-yolk is here concentrated in what I shall call the lower pole of the egg, which becomes the ventral aspect of the future embryo. The part of the .egg containing the stored-up food-yolk is, as has already been explained in the chapter on segmentation (Vol. II. pp. 94 and 95), to be regarded as equivalent to part of those eggs which do not contain food-yolk ; a fact which requires to be borne in mind in any attempt to deal comparatively with the formation of the layers in the Vertebrata. It may be laid down as a general law, which holds very accurately for the Vertebrata, that in eggs in which the distribution of food-yolk is not uniform, the size of the cells resulting from segmentation is proportional to the quantity of food-material they contain. In accordance with this law the cells of the Amphibian ovum are of unequal size even at the close of segmentation. They may roughly be divided into two categories, viz. the smaller cells of the upper pole and the larger of the lower (fig. 170 A). The segmentation cavity (sg) lies between the two, but is unsymmetrically placed near the upper pole of the egg, owing to the large bulk of the ventrally placed yolk-segments. In the inequality of the cells at the close of segmentation the Amphibia stand in contrast with Amphioxus. The upper cells are mainly destined to form the epiblast, and the lower the hypoblast and mesoblast.

The next change which takes place is an invagination, the earliest traces of which are observable in fig. 170 A. The invagination is not however so simple as in Amphioxus. Owing in fact to the presence of the food-yolk it is a mixture of invagination by epibole and by embole.

At the point marked x in fig. 170 A, which corresponds with the future hind end of the embryo, and is placed on the equatorial line marking the junction of the large and small cells, there takes place a normal invagination, which gives rise solely to the hypoblast of the dorsal wall of the alimentary tract and to part of the dorsal mesoblast. The invaginated layer grows inwards from the point x along what becomes the dorsal side of the embryo ; and between it and the yolk-cells below is formed a slit-like space (fig. 170 B and C). This space is the mesenteron. It is even better shewn in fig. 171 representing the


COMPARISON OF THE GERMINAL LAYERS. 279

process of invagination in Petromyzon. The point x in fig. 170 where epiblast, mesoblast and hypoblast are continuous, is homologous with the dorsal lip of the blastopore in Amphioxus. In the course of the invagination the segmentation cavity, as in Amphioxus, becomes obliterated.

While the above invagination has been taking place, the epiblast cells have been simply growing in an epibolic fashion round the yolk; and by the stage represented in fig. 170 C and D the exposed surface of yolk has become greatly diminished ; and an obvious blastopore is thus established. Along the line of the growth a layer of mesoblast cells (iri\ continuous at the sides with the invaginated mesoblast layer, has become differentiated from the small cells (fig. 170 A) intermediate between the epiblast cells and the yolk.

Owing to the nature of the above process of invagination the mesenteron is at first only provided with an epithelial wall on its dorsal side, its ventral wall being formed of yolk-cells (fig. 170). At a later period some of the yolk-cells become transformed into the epithelial cells of the ventral wall, while the remainder become enclosed in the alimentary cavity and employed as pabulum. The whole of the yolk-cells, after the separation of the mesoblast, are however morphologically part of the hypoblast.

The final fate of the blastopore is nearly the same as in Amphioxus. It gradually narrows, and the yolk-cells which at first plug it up disappear (fig. 170 C and D). The neural groove, which becomes formed on the dorsal surface of the embryo, is continued forwards from the point x in fig. 170 C. On the conversion of this groove into a canal the canal freely opens behind into the blastopore ; and a condition is reached in which the blastopore still opens to the exterior and also into the neural canal fig. 170 D. In a later stage (fig. 172) the external opening of the blastopore becomes closed by the medullary folds meeting behind it, but the passage connecting the neural and alimentary canals is left. There is one small difference between the Frog and Amphioxus in the relation of the neural canal to the blastopore. In both types the medullary folds embrace and meet behind it, so that it comes to occupy a position at the hind extremity of the medullary groove. In Amphioxus the closure


280


THE GASTRULA OF AMPHIBIA.


of the medullary folds commences behind, so that the external opening of the blastopore is obliterated simultaneously with the commencing 7rl /

formation of the medullary canal ; but in the Frog the closure of the medullary folds commences anteriorly and proceeds backwards, so that the obliteration of the external opening of the blastopore is a late event in the formation of the medullary canal.

The anus is formed (vide fig. 172) some way in front of the blastopore, and a post-anal gut, continuous with the neurenteric canal, is thus established. Both the postanal gut and the neurenteric canal eventually disappear.

The two other types classed above with the Amphibia, viz. Petromyzon and Acipenser, agree sufficiently closely with them



FIG. 171. LONGITUDINAL VERTICAL SECTION THROUGH AN EMBRYO OF PETROMYZON OF 136 HOURS.

me. mesoblast ; yk. yolk-cells ; al. alimentary tract ; bl. blastopore ; s.c. segmentation cavity.



FIG. 172. LONGITUDINAL SECTION THROUGH AN ADVANCED EMBRYO OF BOMBINATOR. (After Gotte.)

//. mouth ; an. anus ; /. liver ; ne. neurenteric canal ; me. medullary canal ;

ch. notochord ; pn. pineal gland.

to require no special mention ; but with reference to both types it may be pointed out that the ovum contains relatively more food-yolk than that of the Amphibian type just described, and


COMPARISON OF THE GERMINAL LAYERS. 28 1


that this leads amongst other things to the lower layer cells extending up the sides of the segmentation cavity, and assisting in forming its roof.

The next type to be considered is that of Elasmobranchii. The yolk in the ovum of these forms is enormously bulky, and the segmentation is in consequence a partial one. At first sight the differences between their development and that of Amphibia would appear to be very great. In order fully to bridge over the gulf which separates them I have given three diagrammatic longitudinal sections of an ideal form intermediate between Amphibia and Elasmobranchii, which differs however mainly from the latter in the smaller amount of food-yolk; and by their aid I trust it will be made clear that the differences between the Amphibia and Elasmobranchii are of an insignificant character. In fig. 174 A B C are represented three diagrammatic longitudinal sections of Elasmobranch embryos, and in fig. 173 A B C three longitudinal sections of the ideal intermediate form. The diagrams correspond with the Amphibian diagrams already described (fig. 170). In the first stage figured there is present in all of these forms a segmentation cavity (sg) situated not centrally but near the surface of the egg. The roof of the cavity is thin, being composed in the Amphibian embryo of epiblast alone, and in the Elasmobranch of epiblast and lower layer cells. The floor of the cavity is formed of so-called yolk, which forms the main mass of the embryo. In Amphibia the yolk is segmented. In Elasmobranchii there is at first a layer of primitive hypoblast cells separating the segmentation cavity from the yolk proper; this however soon disappears, and an unsegmented yolk with free nuclei fills the place of the segmented yolk of the Amphibia. The small cells at the sides of the segmentation cavity in Amphibia correspond exactly in function and position with the lower layer cells of the Elasmobranch blastoderm.

The relation of the yolk to the blastoderm in the Elasmobranch embryo at this stage of development very well suits the view of its homology with the yolk-cells of the Amphibian embryo. The only essential difference between the two embryos arises from the roof of the segmentation cavity being formed in the Elasmobranch embryo of lower layer cells, which are absent


282


THE GASTRULA OF ELASMOBRANCHIL


in the Amphibian embryo. This difference no doubt depends upon the greater quantity of yolk in the Elasmobranch ovum, and a similar distribution of the lower layer cells is found in Acipenser and in Petromyzon.

In the next stage for the Elasmobranch (fig. 173 and 174 B) and for the Amphibian (fig. 170 C) or better still Petromyzon



FIG. 173. THREE DIAGRAMMATIC LONGITUDINAL SECTIONS THROUGH AN IDEAL TYPE OF VERTEBRATE EMBRYO INTERMEDIATE IN THE MODE OF FORMATION OF ITS LAYERS BETWEEN AMPHIBIA OR PETROMYZON AND ELASMO BRANCH1I.

s.if. segmentation cavity; ep. epiblast; m. mesoblast; hy. hypoblast; nc. neural canal; al. mesenteron; . nuclei of the yolk.

(fig. 171) the agreement between the three types is again very close. For a small arc (x) of the edge of the blastoderm the epiblast and hypoblast become continuous, while at all other


COMPARISON OF THE GERMINAL LAYERS. 283

parts the epiblast, accompanied by lower layer cells, grows round the yolk or round the large cells which correspond to it. The yolk-cells of the Amphibian embryo form a comparatively small mass, and are therefore rapidly enveloped ; while in the case of the Elasmobranch embryo, owing to the greater mass of the yolk, the same process occupies a long period. The portion of the blastoderm, where epiblast and hypoblast become continuous, forms the dorsal lip of an opening the blastopore which leads into the alimentary cavity. This cavity has the same relation in all the three cases. It is lined dorsally by lower layer cells, and ventrally by yolk-cells or what corresponds with yolk-cells ; a large part of the ventral epithelium of the alimentary canal being in both cases eventually derived from the yolk. In Amphibia this epithelium is formed directly from the existing cells, while in Elasmobranchii it is derived from cells formed around the nuclei of the yolk.

As in the earlier stage, so in the present one, the anatomical relations of the yolk to the blastoderm in the one case (Elasmobranchii) are nearly identical with those of the yolk-cells to the blastoderm in the other (Amphibia).

The main features in which the two embryos differ, during the stage under consideration, arise from the same cause as the solitary point of difference during the preceding stage.

In Amphibia the alimentary cavity is formed coincidently with a true ingrowth of cells from the point where epiblast and hypoblast become continuous ; and from this ingrowth the dorsal wall of the alimentary cavity is formed. The same ingrowth causes the obliteration of the segmentation cavity.

In Elasmobranchs, owing probably to the larger bulk of the lower layer cells, the primitive hypoblast cells arrange themselves in their final position during segmentation, and no room is left for a true invagination ; but instead of this there is formed a simple space between the blastoderm and the yolk. The homology of this space with the primitive invagination cavity is nevertheless proved by the survival of a number of features belonging to the ancestral condition in which a true invagination was present. Amongst the more important of these are the following : (i) The continuity of epiblast and hypoblast at the dorsal lip of the blastopore. (2) The continuous conversion of primitive


284 THE GASTRULA OF ELASMOBRANCHII.

hypoblast cells into permanent hypoblast, which gradually extends inwards towards the segmentation cavity, and exactly represents the course of the invagination whereby in Amphibia the dorsal wall of the alimentary cavity is formed. (3) The obliteration of the segmentation cavity during the period when the pseudo-invagination is occurring.

In the next stage there appear more important differences between the two types than in the preceding stages, though here again the points of resemblance predominate.

Figs. 170 D and 174 C represent longitudinal sections through embryos after the closure of the medullary canal. The neurenteric canal is established ; and in front and behind the epithelium of the ventral wall of the mesenteron has begun to be formed.

The mesoblast is represented as having grown in between the medullary canal and the superjacent epiblast.

There are at this stage two points in which the embryo Elasmobranch differs from the corresponding Amphibian embryo, (i) In the formation of the neurenteric canal, there is no free passage leading into the mesenteron from the exterior as in Amphibia (fig. 170 D). (2) The whole yolk is not enclosed by the epiblast, and therefore part of the blastopore is still open.

The difference between Amphibia and Elasmobranchii in the first of these points is due to the fact that in Elasmobranchii, as in Amphioxus, the neural canal becomes first closed behind ; and simultaneously with its closure the lateral parts of the lips of the blastopore, which are continuous with the medullary folds, meet together and shut in the hindmost part of the alimentary tract.

The second point is of some importance for understanding the relations of the formation of the layers in the amniotic and the non-amniotic Vertebrates. Owing to its large size the whole of the yolk in Elasmobranchii is not enclosed by the epiblast at the time when the neurenteric canal is established ; in other words a small posterior and dorsal portion of the blastopore is shut off in the formation of the neurenteric canal. The remaining ventral portion becomes closed at a later period. Its closure takes place in a linear fashion, commencing at the hind end of the embryo, and proceeding apparently backwards ; though, as this part eventually becomes folded in to form the ventral wall of the embryo, the closure of it really travels forwards. The


COMPARISON OF THE GERMINAL LAYERS.


285


process causes however the embryo to cease to lie at the edge of the blastoderm, and while situated at some distance from the edge, to be connected with it by a linear streak, representing the coalesced lips of the blastopore. The above process is diagrammatically represented in fig. 175 B; while as it actually occurs



FIG. 174.


DIAGRAMMATIC LONGITUDINAL SECTIONS OF AN ELASMOBRANCH

EMBRYO.


Epiblast without shading. Mesoblast black with clear outlines to the cells. Lower layer cells and hypoblast with simple shading.

ep. epiblast; m. mesoblast; al. alimentary cavity; sg. segmentation cavity; nc. neural canal; ch. notochord; x. point where epiblast and hypoblast become continuous at the posterior end of the embryo ; n. nuclei of yolk.

A. Section of young blastoderm, with the segmentation cavity enclosed in the lower layer cells (primitive hypoblast).

B. Older blastoderm with embryo in which hypoblast and mesoblast are distinctly formed, and in which the alimentary cavity has appeared. The segmentation cavity is still represented, though by this stage it has in reality disappeared.

C. Older blastoderm with embryo in which the neural canal is formed, and is continuous posteriorly with the alimentary canal. The notochord, though shaded like mesoblast, belongs properly to the hypoblast.

it is shewn in fig. 30, p. 63. The whole closure of the blastopore in Elasmobranchii is altogether unlike what takes place in Amphibia, where the blastopore remains as a circular opening which


286 THE GASTRULA OF THE SAUROPSIDA.

gradually narrows till it becomes completely enveloped in the medullary folds (fig. 175 A).

On the formation of the neurenteric canal the body of the embryo Elasmobranch becomes gradually folded off from the yolk, which, owing to its great size, forms a large sack appended to the ventral side of the body. The part of the somatopleure, which grows round it, is to be regarded as a modified portion of the ventral wall of the body. The splanchnopleure also envelops it, so that, morphologically speaking, the yolk lies within the mesenteron.

The Teleostei, so far as the first formation of the layers is concerned, resemble in all essential features the Elasmobranchii, but the neurenteric canal is apparently not developed (?), owing to the obliteration of the neural canal ; and the roof of the segmentation cavity is formed of epiblast only.

In the preceding pages I have attempted to shew that the Amphibia, Acipenser, Petromyzon, the Elasmobranchii and the Teleostei agree very closely in the mode of formation of the gastrula. The unsymmetrical gastrula or pseudo-gastrula which is common to them all is, I believe, to be explained by the form of the vertebrate body. In Amphioxus, where the small amount of food-yolk present is distributed uniformly, there is no reason why the invagination and resulting gastrula should not be symmetrical. In true Vertebrates, where more food-yolk is present, the shape and structure of the body render it necessary for the food-yolk to be stored away on the ventral side of the alimentary canal. It is this fact which causes the asymmetry of the gastrula, since it is not possible for the part of the ovum, which will become the ventral wall of the alimentary tract, and which is loaded with food-yolk, to be invaginated in the same fashion as the dorsal wall.

Sauropsida. The comparison of the different types of the Ichthyopsida is fairly simple, but the comparison of the Sauropsida with the Ichthyopsida is a far more difficult matter. In all the Sauropsida there is a large food-yolk, and the segmentation agrees closely with that in the Elasmobranchii. It might have been anticipated that the resemblance would continue in the subsequent development. This however is far from being the


COMPARISON OF THE GERMINAL LAYERS. 287

case. The medullary plate, instead of lying at the edge of the blastoderm, lies in the centre, and its formation is preceded by that of a peculiar structure, the primitive streak, which, on the



FIG. 175. DIAGRAMS ILLUSTRATING THE POSITION OF THE BLASTOPORE, AND THE RELATION OF THE EMBRYO TO THE YOLK IN VARIOUS MEROBLASTIC VERTEBRATE OVA.

A. Type of Frog. B. Elasmobranch type. C. Amniotic Vertebrate. mg. medullary plate ; ne. neurenteric canal ; bl. portion of blastopore adjoining the neurenteric canal. In B this part of the blastopore is formed by the edges of the blastoderm meeting and forming a linear streak behind the embryo ; and in C it forms the structure known as the primitive streak, yk. part of the yolk not yet enclosed by the blastoderm.

formation of the medullary plate, is found to lie at the hinder end of the latter and to connect it with the edge of the blastoderm.

The possibility of a comparison between the Sauropsida and the Elasmobranchii depends upon the explanation being possible of (i) the position of the embryo near the centre of the blastoderm, and (2) the nature of the primitive streak.

The answers to these two questions are, according to my view, intimately bound together.


288 THE GASTRULA OF THE SAUROPSIDA.


I consider that the embryos of the Sauropsida have come to occupy a central position in the blastoderm owing to the abbreviation of a process similar to that by which, in Elasmobranchii, the embryo is removed from the edge of the blastoderm ; and that the primitive streak represents the linear streak connecting the Elasmobranch embryo with the edge of the blastoderm after it has become removed from its previous peripheral position, as well as the true neurenteric part of the Elasmobranch blastopore.

This view of the nature of the primitive streak, which is diagrammatically illustrated in fig. 175, will be rendered more clear by a brief review of the early developmental processes in the Sauropsida.

After segmentation the blastoderm becomes divided, as in Elasmobranchii, into two layers. It is doubtful whether there is any true representative of the segmentation cavity. The first structure to appear in the blastoderm is a linear streak placed at the hind end of the blastoderm, known as the primitive streak (figs. 175 C, /5/and 176, pr). At the front end of the primitive streak the epiblast and hypoblast become continuous, just as they do at the dorsal lip of the blastopore in Elasmobranchii. Continued back from this point is a streak of fused mesoblast and epiblast to the under side of which a linear thin layer of hypoblast is more or less definitely attached.

A further structure, best developed in the Lacertilia, appears in the form of a circular passage perforating the blastoderm at the front end of the primitive streak (fig. 176, ne). This passage is bounded anteriorly by the layer of cells forming the continuation of the hypoblast into the epiblast.

In the next stage the medullary plate becomes formed in front of the primitive streak (fig. 175 C), and the medullary folds are continued backwards so as to enclose the upper opening of the passage through the blastoderm. On the closure of the medullary canal (fig. 177) this passage leads from the medullary canal into the alimentary tract, and is therefore the neurenteric canal ; and a post-anal gut also becomes formed. The latter part of the above description applies especially to the Lizard: but in Chelonia and most Birds distinct remnants (vide pp. 162 164) of the neurenteric canal are developed.

On the hypothesis that the Sauropsidan embryos have come


COMPARISON OF THE GERMINAL LAYERS. 289

to occupy their central position, owing to an abbreviation of a process analogous to the linear closing of the blastopore behind the embryos of Elasmobranchii, all the appearances above described receive a satisfactory explanation. The passage at the front end of the primitive streak is the dorsal part of the blastopore, which in Elasmobranchii becomes converted into the neurenteric canal. The remainder of the primitive streak represents, in a rudimentary form, the linear streak in Elasmobranchii, formed by the coalesced edges of the blastoderm, which connects the hinder end of the embryo with the still open yolk blastopore. That it is in later stages not continued to the edge of the blastoderm, as in Elasmobranchii, is due to its being a rudimentary organ. The more or less complete fusion of the layers in the primitive streak is simply to be explained by this structure representing the coalesced edges of the blastopore ; and the growth outwards from it of the mesoblast is probably a remnant of a primitive dorsal invagination of the mesoblast and hypoblast like that in the Frog.



FIG. 176. DIAGRAMMATIC LONGITUDINAL SECTION OF AN EMBRYO OF LACERTA. //. body cavity; am. amnion; ne. neurenteric canal; ch. notochord; hy. hypoblast; ep. epiblast; pr. primitive streak. In the primitive streak all the layers are partially fused.

The final enclosure of the yolk in the Sauropsida takes place at the pole of the yolk-sack opposite the embryo, so that the blastopore is formed of three parts, (i) the neurenteric canal, (2) the primitive streak behind this, (3) the blastopore at the pole of the yolk-sack opposite the embryo.

Mammalia. The features of the development of the placental Mammalia receive their most satisfactory explanation on the hypothesis that their ancestors were provided with a large-yolked ovum like that of the Sauropsida. The food-yolk must be supposed to have ceased to be developed on the establishment of a maternal nutrition through the uterus.

On this hypothesis all the developmental phenomena subseB. in 19


290


MAMMALIAN GASTRULA.


quently to the formation of the blastodermic vesicle receive a satisfactory explanation.

The whole of the blastodermic vesicle, except the embryonic area, represents the yolk-sack, and the growth of the hypoblast and then of the mesoblast round its inner wall represents the



Air


FIG. 177. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR END OF AN EMBRYO BlRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS.

ep. epiblast ; Sp.c. spinal canal ; ch. notochord ; n.e. neurenteric canal ; hy. hypoblast ; p.a.g. post-anal gut ; pr. remains of primitive streak folded in on the ventral side ; al. allantois ; me. mesoblast ; an. point where anus will be formed ; p.c. perivisceral cavity am. amnion; so. somatopleure ; sp. splanchnopleure.

corresponding growths in the Sauropsida. As in the Sauropsida it becomes constricted off from the embryo, and the splanchnopleuric stalk of the sack opens into the ileum in the usual way.


R



FIG. 178. OPTICAL SECTIONS OF A RABBIT'S OVUM AT TWO STAGES CLOSELY

FOLLOWING UPON THE SEGMENTATION. (After E. van Beneden.) ep. epiblast; hy. primary hypoblast; bp. Van Beneden's so-called blastopore. The shading of the epiblast and hypoblast is diagrammatic.



COMPARISON OF THE GERMINAL LAYERS.


291


In the formation of the embryo out of the embryonic area the phenomena which distinguish the Sauropsida from the Ichthyopsida are repeated. The embryo lies in the centre of the area ; and before it is formed there appears a primitive streak, from which there grows out the greater part of the mesoblast. At the front end of the primitive streak the hypoblast and epiblast become continuous, though a perforated neurenteric blastopore has not yet been detected.

All these Sauropsidan features are so obvious that they need not be insisted on further. The embryonic evidence of the common origin of Mammalia and Sauropsida, both as concerns the formation of the layers and of the embryonic membranes, is as clear as it can be. The only difficulty about the early development of Mammalia is presented by the epibolic gastrula and the



FIG. 179. RABBIT'S OVUM BETWEEN 70 90 HOURS AFTER IMPREGNATION.

(After E. van Beneden.)

bv. cavity of blastodermic vesicle (yolk-sack) ; ep. epiblast ; hy. primitive hypoblast ; Zp. mucous envelope.

formation of the blastodermic vesicle (figs. 178 and 179). That the segmentation is a complete one is no doubt a direct consequence of the reduction of the food-yolk, but the growth of the epiblast cells round the hypoblast and the final enclosure of the latter, which I have spoken of as giving rise to the epibolic gastrula, are not so easily explained.

19 2


292 MESOBLAST AND NOTOCHORD.

It might have been supposed that this process was equivalent to the growth of the blastoderm round the yolk in the Sauropsida, but then the blastopore ought to be situated at the pole of the egg opposite to the embryonic area, while, according to Van Beneden, the embryonic area corresponds approximately to the blastopore.

Van Beneden regards the Mammalian blastopore as equivalent to that in the Amphibia, but if the position previously adopted about the primitive streak is to be maintained, Van Beneden's view must be abandoned. No satisfactory phylogenetic explanation of the Mammalian gastrula by epibole has in my opinion as yet been offered.

The formation of the blastodermic vesicle may perhaps be explained on the view that in the Proto-mammalia the yolk-sack was large, and that its blood-vessels took the place of the placenta of higher forms. On this view a reduction in the bulk of the ovarian ovum might easily have taken place at the same time that the presence of a large yolk-sack was still necessary for the purpose of affording surface of contact with the uterus.


The formation of the Mesoblast and of the Notochord.

Amphioxus. The mcsoblast originates in Amphioxus, as in several primitive invertebrate types, from a pair of lateral



FIG. 180. SECTIONS OF AN AMPHIOXUS EMBRYO AT THREE STAGES. (After Kowalevsky.)

A. Section at gastrula stage.

B. Section of an embryo slightly younger than that represented in fig. 169 D.

C. Section through the anterior part of an embryo at the stage represented in fig. 169 !:.

/. neural plate ; nc. neural canal ; mes. archenteron in A and B, and mesenteron in C; ch. notochord ; so. mesoblastic somite.



COMPARISON OF THE GERMINAL LAYERS. 293


diverticula, constricted off from the archenteron (fig. 180). Their formation commences at the front end of the body and is thence carried backwards, and each diverticulum contains a prolongation of the cavity of the archenteron. After their separation from the archenteron the dorsal parts of these diverticula become divided by transverse septa into successive somites, the cavities of which eventually disappear ; while the walls become mainly converted into the muscle-plates, but also into the tissue around the notochord which corresponds with the vertebral tissue of the higher Chordata.

The ventral part of each diverticulum, which is prolonged so as to meet its fellow in the middle ventral line, does not become divided into somites, but contains a continuous cavity, which becomes the body cavity of the adult. The inner layer of this part forms the splanchnic mesoblast, and the outer layer the somatic mesoblast.

The notochord would almost appear to arise as a third median and dorsal diverticulum of the archenteron (fig. 1 80 ch). At any rate it arises as a central fold of the wall of this cavity, which is gradually constricted off from before backwards.

Urochorda. In simple Ascidians the above processes undergo a slight modification, which is mainly due (i) to a general simplification of the FIG igj TRANSVERSE OPTI . organization, and (2) to the non- CAL SECTION OF THE TAIL OF AN continuation of the notochord into ^SSSSSSSST'

the trunk. The section is from an embryo

The whole dorsal wall of the of the same age as fig. 8 iv. posterior part of the archenteron is * converted into the notochord (fig. bla st of tail. 181 ck), and the lateral walls into the mesoblast (me) ; so that the original lumen of the posterior part of the archenteron ceases to be bounded by hypoblast cells, and disappears as such. Part of the ventral wall remains as a solid cord of cells (al 1 ) The anterior part of the archenteron in front of the notochord passes wholly into the permanent alimentary tract.

The derivation of the mesoblast from the lateral walls of the



294


MESOBLAST AND NOTOCHORD.



n.al


posterior part of the archenteron is clearly comparable with the analogous process in Amphioxus.

Vertebrata. In turning from Amphioxus to the true Vertebrata we find no form in which diverticula of the primitive alimentary tract give rise to the mesoblast. There is reason to think that the type presented by the Elasmobranchii in the formation of the mesoblast is as primitive as that of any other group. In this group the mesoblast is formed, nearly coincidently with the hypoblast of the dorsal wall of the mesenteron, as two lateral sheets, one on each side of the middle line (fig. 182 m). These two sheets are at first solid masses ; and their differentiation commences in front and is continued backwards. After their formation the notochord arises from the axial portion of the hypo


FlG. 182. TWO TRANSVERSE SECTIONS OF AN EMBRYO PRISTIURUS OF THE SAME AGE AS FIG. 17.

A. Anterior section.

B. Posterior section.

mg. medullary groove ; ep. epiblast ; hy. hypoblast ; n.al cells formed round the nuclei of the yolk which have entered the hypoblast ; m. mesoblast.

The sections shew the origin of the mesoblast.


blast (which had no share in giving rise to the two mesoblast plates) as a solid thickening (fig. 183 //), which is separated from it as a circular rod. Its differentiation, like that of the mesoblastic plates, commences in front. The mesoblast plates subsequently become divided for their whole length into two layers, between which a cavity is developed (fig. 184). The dorsal parts of the plates become divided by transverse partitions into somites, and these somites with their contained cavities are next separated from the more ventral parts of the plates (fig. 185 mp). In the somites the cavities become eventually obliterated, and from their inner sides plates of tissue for the vertebral bodies (fig. 186 Vr) are separated ; while the outer parts, consisting of two sheets, containing the remains of the original cavity, form the muscleplates (mp).



COMPARISON OF THE GERMINAL LAYERS.


295


The undivided ventral portion gives rise to the general A



FIG. 183. THREE SECTIONS OF A PRISTIURUS EMBRYO SLIGHTLY OLDER THAN

FIG. 18 B.

The sections shew the development of the notochord.

Ch. notochord; CK. developing notochord; mg. medullary groove; lp. lateral plate of mesoblast ; ep. epiblast ; hy. hypoblast.

somatic and splanchnic mesoblast (fig. 185), and the cavity between its two layers constitutes the body cavity. The originally separate halves of the body cavity eventually meet and unite in the ventral median line throughout the greater part of the body, though in the tail they remain distinct and are finally obliterated. Dorsally they are separated by the mesentery. From the mesoblast at the junction of the dorsal and



FIG. 184. TRANSVERSE SECTION THROUGH THE TAIL-REGION OF A PRISTIURUS EMBRYO OF THE SAME AGE AS FIG. 28 E.

df. dorsal fin; sp.c. spinal cord; pp. body cavity; sp. splanchnic layer of mesoblast; so. somatic layer of mesoblast; mp'. commencing differentiation of muscles ; ch. notochord ; x. subnotochordal rod arising as an outgrowth of the dorsal wall of the alimentary tract ; a/, alimentary tract.


296


MESOBLAST AND NOTOCHORD.



ventral parts of the primitive plates is formed the urinogenital

system.

That the above mode of origin of the mesoblast and noto chord is to be regarded as a modification of that observable in Am phioxus seems probable from the

following considerations :

In the first place, the mesoblast is

split off from the hypoblast not as a

single mass but as a pair of distinct

masses, comparable with the paired di vcrticula in Amphioxus. Secondly,

the body cavity, when it appears in

the mesoblast p\a.tes,does not arise as a

single cavity, but as a pair of cavities,

one for each plate of mesoblast ; and

these cavities remain permanentlydis tinct in some parts of the body, and

nowhere unite till a comparatively

late period. Thirdly, the primitive body cavity of the embryo is not confined to the region in which a body cavity exists in the adult, but extends to the summit of tJie muscleplates, at first separating parts which become completely fused in the adult to form the great lateral muscles of the body.

It is difficult to understand how the body cavity could thus extend into the muscle-plates on the supposition that it represents a primitive split in the mesoblast between the wall of the gut and the body-wall ; but its extension to this part is quite intelligible, on the hypothesis that it represents the cavities of two diverticula of the alimentary tract, from the muscular walls of which the voluntary muscular system has been derived ; and it may be pointed out that the derivation of part of the muscular system from what is apparently splanchnic mesoblast is easily explained on the above hypothesis, but not, so far as I see, on any other.


FIG. 185. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNG KK

THAN 28 F.

sp.c. spinal canal; W. white matter of spinal cord ; pr. posterior nerve-roots ; ch. notochord ; x. subnotochordal rod ; ao. aorta ; vip. muscle-plate ; mp'. inner layer of muscle-plate already converted into muscles ; Vr. rudiment of vertebral body ; si. segmental tube ; sd. segmental duct ; sp.v. spiral valve ; v. subintestinal vein ; p.o. primitive generative cells.


COMPARISON OF THE GERMINAL LAYERS.


297



Such are the main features, presented by the mesoblast in Elasmobranchii, which favour the view of its having originally formed the walls of the alimentary diverticula. Against this view of its nature are the facts (i) of the mesoblast plates being at first solid, and (2) of the body cavity as a consequence of this never communicating with the alimentary canal. These points, in view of our knowledge of embryological modifications, cannot be regarded as great difficulties in my hypothesis. We have many examples of organs, which, though in most cases arising as involutions, yet appear in other cases as solid ingrowths. Such examples are afforded by the optic vesicle, auditory vesicle, and probably also by the central nervous system of Osseous Fishes. In most Vertebrates these organs are formed as hollow involutions from the exterior ; in Osseous Fishes, however, as solid involutions, in which a cavity is secondarily established.

There are strong grounds for thinking that in all Vertebrates the mesoblast plates on each side of the notochord originate independently, much as in Elasmobranchii, and that the notochord is derived from the axial hypoblast ; but there are some difficulties in the application of this general statement to all cases. In Amphibia, Ganoids, and Petromyzon, where the dorsal hypoblast is formed by a process of invagtnation as in Amphioxus, the dorsal mesoblast also owes its origin to this invagination, in that the indifferent invaginated layer becomes divided into hypoblast and mesoblast. Amongst these forms the mesoblast sheet, when separated from the hypoblast, is certainly not continuous across the middle line in Petromyzon (Calberla) and the Newt (Scott and Osborn), and doubtfully so


FIG. 1 86. HORIZONTAL SECTION THROUGH THE TRUNK OF AN EMBRYO OF SCYLLIUM CONSIDERABLY YOUNGER THAN 28 F.

The section is taken at the level of the notochord, and shews the separation of the cells to form the vertebral bodies from the muscle-plates.

ch. notochord ; ep. epiblast ; Vr. rudiment of vertebral body ; mp. muscle-plate ; mp'. portion of muscle-plate already differentiated into longitudinal muscles.


298 MESOBLAST AND NOTOCHORD.

in the other forms. It arises, in fact, as in Elasmobranchii, as two independent plates. The fact of these plates originating from an invaginated layer can only be regarded in the light of an approximation to the primitive type found in Amphioxus.

In Petromyzon and the Newt the whole axial plate of dorsal hypoblast becomes separated off from the rest of the hypoblast as the notochord, and this mode of origin for the notochord resembles more closely that in Amphioxus than the mode of origin in Elasmobranchii.

In Teleostei, there is reason to think that the processes in the formation of the mesoblast accord closely with what has been described as typical for the Ichthyopsida, but there are still some points involved in obscurity.

Leaving the Ichthyopsida, we may pass to the consideration of the Sauropsida and Mammalia. In both of these types there is evidence to shew that a part of the mesoblast is formed in situ at the same time as the hypoblast, from the lower strata of segmentation spheres. This mesoblast is absent in the front part of the area pellucida, and on the formation of the primitive streak (blastopore), an outgrowth of mesoblast arises from it as



FIG. 187. TRANSVERSE SECTION THROUGH AN EMBRYO RABBIT OF EIGHT DAYS. ep. epiblast ; me. mesoblast ; ky. hypoblast ; mg. medullary groove.

in Amphibia, etc. From this region the mesoblast spreads as a continuous sheet to the sides and posterior part of the blastoderm. In the region of the embryo, its exact behaviour has not in some cases been quite satisfactorily made out. There are reasons for thinking that it appears as two sheets not tinited in the axial line in both Lacertilia (fig. 126) and Mammalia (fig. 187), and this to some extent holds true for Aves (vide p. 156). In Lacertilia (fig. 188) and Mammalia, the axial hypoblast becomes wholly converted into the notochord, which at the posterior end of the body is continued into the epiblast at the dorsal lip of the blastopore ; while in Birds the notochord is formed by a very similar (fig. 189 cfi) process.




COMPARISON OF THE GERMINAL LAYERS.


299


The above processes in the formation of the mesoblast are for the most part easily explained by a comparison with the lower types. The outgrowth of the mesoblast from the sides of the primitive streak is a rudiment of the dorsal invagination of hypoblast and mesoblast found in Amphibia ; and the apparent



FIG. 188. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH AN EMBRYO LIZARD TO SHEW THE RELATIONS OF THE NEURENTERIC CANAL (ne) AND OF

THE PRIMITIVE STREAK (pr).

am. amnion; ep. epiblast; hy. hypoblast; ch. notochord ; //. body cavity; ne. neurenteric canal ; pr. primitive streak.

outgrowth of the mesoblast from the epiblast in the primitive streak is no more to be taken as a proof of the epiblastic origin of the mesoblast, than the continuity of the epiblast with the invaginated hypoblast and mesoblast at the lips of the blastopore in the Frog of the derivation of these layers from the epiblast in this type.

The division of the mesoblast into two plates along the dorsal line of the embryo, and the formation of the notochord from the



ky.


FIG. 189. TRANSVERSE SECTION THROUGH THE EMBRYONIC REGION OF THE BLASTODERM OF A CHICK AT THE TIME OF THE FORMATION OF THE NOTOCHORD, BUT BEFORE THE APPEARANCE OF THE MEDULLARY GROOVE.

ep. epiblast; ky. hypoblast; ch. notochord; me. mesoblast; n. nuclei in the yolk of the germinal wall yk.

axial hypoblast, are intelligible without further explanation. The appearance of part of the mesoblast before the formation of the primitive streak is a process of the same nature as the


300 THE EPIBLAST.


differentiation of hypoblast and mesoblast in Elasmobranchii without an invagination.

In the Sauropsida, some of the mesoblast of the vascular area would appear to be formed in situ out of the germinal wall, by a process of cell-formation similar to that which takes place in the yolk adjoining the blastoderm in Elasmobranchii and Teleostei. The mesoblast so formed is to be compared with that which arises on the ventral side of the embryo in the Frog, by a direct differentiation of the yolk-cells.

What was stated for the Elasmobranchii with reference to the general fate of the mesoblast holds approximately for all the other forms.

The Epiblast.

The epiblast in a large number of Chordata arises as a single row of more or less columnar cells. Since the epidermis, into which it becomes converted, is formed of two more or less distinct strata in all Chordata except Amphioxus and Ascidians, the primitive row of epiblast cells, when single, necessarily becomes divided in the course of development into two layers.

In some of the Vertebrata, viz. the Anurous Amphibia, Teleostei, Acipenser, and Lepidosteus, the epiblast is from the first formed of two distinct strata. The upper of these, formed of a single row of cells, is known as the epidermic stratum, and the lower, formed of several rows, as the nervous stratum. In these cases the two original strata of the epiblast are equivalent to those which appear at a later period in the other forms. Thus Vertebrates may be divided into groups according to the primitive condition of their epiblast, viz. a larger group with but a single stratum of cells at first ; and a smaller group with two strata.

While there is no great difficulty in determining the equivalent parts of the epidermis in these two groups, it still remains an open question in which of them the epiblast retains its primitive condition.

Though it is not easy to bring conclusive proofs on the one side or the other, the balance of argument appears to me to be


COMPARISON OF THE GERMINAL LAYERS. 301

decidedly in favour of regarding the condition of the epiblast in the larger group as primitive, and its condition in the smaller group as secondary, and due to the throwing back of the differentiation of the epiblast to a very early period of development.

In favour of this view may be urged (i) the fact that the simple condition is retained in Amphioxus through life. (2) The correlation in Amphibia, and the other forms belonging to this group, between a closed auditory pit and the early division of the epiblast into two strata; there being no doubt that the auditory pit was at. first permanently open, a condition of the epiblast which necessitates its never having an external opening must clearly be secondary. (3) It appears more likely that a particular genetic feature should be thrown back in development, than that such an important feature, as a distinction between two primary layers, should be absolutely lost during an early period of development, and then re-appear in later stages.

The fact of the epiblast of the neural canal being divided, like the remainder of the layer, into nervous and epidermic parts, cannot, I think, be used as an argument in favour of the opposite view to that here maintained. It seems probable that the central canal of the nervous system arose phylogenetically as an involution from the exterior, and that the epidermis lining it is merely part of the original epidermis, which has retained its primitive structure as a simple stratum, but is naturally distinguishable from the nervous structures adjacent to it.

Where the epiblast is divided at an early period into two strata, the nervous stratum is always the active one, and takes the main share in forming all the organs derived from the layer.

Formation of the central nervous system. In all Chordata an axial strip of the dorsal epiblast, extending from the lip of the blastopore to the anterior extremity of the head, and known as the medullary plate, becomes isolated from the remainder of the layer to give rise to the central nervous axis.

According to the manner in which this takes place, three types may, however, be distinguished. In Amphioxus the axial


3O2


THE CENTRAL NERVOUS SYSTEM.


strip becomes first detached from the adjoining epiblast, which then meets and forms a continuous layer above it (fig. 190 A and B ;//). The sides of the medullary plate, which is thus shut off from the surface, bend over and meet so as to convert the



FIG. 190. SECTIONS OF AN AMPHIOXUS EMBRYO AT THREE STAGES. (After Kowalevsky. )

A. Section at gastrula stage.

B. Section of an embryo slightly younger than that represented in fig. 169 D.

C. Section through the anterior part of an embryo at the stage represented in fig. 169 E.

//. neural plate; nc. neural canal; mes. archenteron in A and B, and mesenteron

in C ; ch. notochord ; so. mesoblastic somite.

plate into a canal (fig. 190 C nc). In the second and ordinary type the sides of the medullary plate fold over and meet so as to form a canal before the plate becomes isolated from the external epiblast.

The third type is characteristic of Lepidosteus, Teleostei, and Petromyzon. Here the axial plate becomes narrowed in such a way that it forms a solid keel-like projection towards the ventral surface (fig. 191 Me). This keel subsequently becomes separated from the remainder of the epidermis, and a central canal is afterwards developed in it. Calberla and Scott hold that the epidermic layer of the skin is involuted into this keel in Petromyzon, and Calberla maintains the same view for Teleostei (fig. 32), but further observations on this subject are required. In the Teleostei a very shallow depression along the axis of the keel is the only indication of the medullary groove of other forms.

In Amphioxus (fig. 190), the Tunicata, Petromyzon (?), Elasmobranchii (fig. 182), the Urodela and Mammalia (fig. 187), the epiblast of the medullary plate is only formed of a single row of cells at the time when the formation of the central nervous system commences; but, except in Amphioxus and the Tuni


COMPARISON OF THE GERMINAL LAYERS. 303

cata, it becomes several cells deep before the completion of the process. In other types the epiblast is several cells deep even before the differentiation of a medullary plate. In the Anura, the nervous layer of the epidermis alone is thickened in the



FIG. 191. SECTION THROUGH AN EMBRYO OF LEPIDOSTEUS ON THE FIFTH DAY

AFTER IMPREGNATION. MC. medullary cord; Ep. epiblast; Me. mesoblast ; hy. hypoblast; Ch. notochord.

formation of the central nervous system (fig. 72) ; and after the closure of the medullary canal, the epidermic layer fuses for a period with the nervous layer, though on the subsequent formation of the central epithelium of the nervous canal, there can be little doubt that it becomes again distinct.

It seems almost certain that the formation of the central nervous system from a solid keel-like thickening of the epidermis is a derived and secondary mode ; and that the folding of the medullary plate into a canal is primitive. Apart from its greater frequency the latter mode of formation of the central nervous system is shewn to be the primitive type by the fact that it offers a simple explanation of the presence of the central canal of the nervous system ; while the existence of such a canal cannot easily be explained on the assumption that the central nervous system was originally developed as a keel-like thickening of the epiblast.

It is remarkable that the primitive medullary plate rarely exhibits any indication of being formed of two symmetrical halves. Such indications are, however, found in the Amphibia (fig. 192 and fig. 72) ; and, since in the adult state the nervous cord exhibits nearly as distinct traces of being formed of two united strands as does the ventral nerve-cord of many Chaetopods, it is


304 ORGANS DERIVED FROM THE GERMINAL LAYERS.


quite possible that the structure of the medullary plate in Amphibia may be more primitive than that in other types 1 .

Formation of the organs of special sense. The more important parts of the organs of smell, sight, and hearing are derived from the epiblast ; and it has been asserted that the olfactory pit, optic vesicles and auditory pit take their origin from a special sense plate, continuous at first with this medullary plate. In my opinion this view cannot be maintained.

In the case of the group of forms in which the epiblast is early divi


al


FIG. 192. TRANSVERSE SECTION THROUGH THE CEPHALIC REGION OF A YOUNG NEWT EMBRYO. (After Scott and Osborn.)

In.hy. invaginated hypoblast, the dorsal part of which will form the notochord ; ep. epiblast of neural plate ; sp. splanchnopleure ; al. alimentary tract ; yk. and Y. hy. yolk-cells.


ded into nervous and epidermic layers, the former layer alone becomes involuted in the formation of the auditory pit and the lens, the external openings of which are never developed, while it is also mainly concerned in the formation of the olfactory pit.


Summary of the more important Organs derived from the three germinal layers.

The epiblast primarily gives origin to two very important parts of the body, viz. the central nervous system and the epidermis.

It is from the involuted epiblast of the neural tube that the whole of the grey and white matter of the brain and spinal cord appears to be developed, the simple columnar cells of the epiblast being directly transformed into the characteristic multipolar nerve cells. The whole of the sympathetic nervous system

1 A parallel to the unpaired medullary plate of most Chordata is supplied by the embryologically unpaired ventral cord of most Gephyrea and some Crustacea. In these forms there can be little doubt that the ventral cord has arisen from the fusion of two originally independent strands, so that it is not an extremely improbable hypothesis to suppose that the same may have been the case in the Chordata.


COMPARISON OF THE GERMINAL LAYERS. 305

and the peripheral nervous elements of the body, including both the spinal and the cranial nerves and ganglia, are epiblastic in origin.

The epithelium (ciliated in the young animal) lining the canalis centralis of the spinal cord, together with that lining the ventricles of the brain, is the undifferentiated remnant of the primitive epiblast.

The epiblast also forms the epidermis ; not however the dermis, which is of mesoblastic origin. The line of junction between the epiblast and the mesoblast coincides with that between the epidermis and the dermis. From the epiblast are formed all such tegumentary organs or parts of organs as are epidermic in nature.

In addition to the above, the epiblast plays an important part in the formation of the organs of special sense.

According to their mode of formation, these organs may be arranged into two divisions. In the first come the organs where the sensory expansion is derived from the involuted epiblast of the medullary canal. To this class belongs the retina, including the pigment epithelium of the choroid, which is formed from the original optic vesicle budded out from the fore-brain.

To the second class belong the epithelial expansions of the membranous labyrinth of the ear, and the cavity of the nose, which are formed by an involution of the epiblast covering the external surface of the embryo. These accordingly have no primary connection with the brain. ' Taste bulbs ' and other terminal nervous organs, such as those of the lateral line in fishes, are also structures formed from the external epiblast.

In addition to these we have the crystalline lens formed of involuted epiblast as well as the cavity of the mouth and anus, and the glands derived from them. The pituitary body is also epiblastic in origin.

From the hypoblast are derived the epithelium of the digestive canal, the epithelium of the trachea, bronchial tubes and air cells, the cylindrical epithelium of the ducts of the liver, pancreas, thyroid body, and other glands of the alimentary canal, as well as the hepatic cells constituting the parenchyma of the liver, developed from the hypoblast cylinders given off around the primary hepatic diverticula.

B. III. 20


306 GROWTH IN LENGTH OF THE EMBRYO.

Homologous probably with the hepatic cells, and equally of hypoblastic origin, are the spheroidal 'secreting cells' of the pancreas and other glands. The epithelium of the salivary glands, though these so closely resemble the pancreas, is probably of epiblastic origin, inasmuch as the cavity of the mouth is entirely lined by epiblast.

The hypoblast also lines the allantois. To these parts must be added the notochord and subnotochordal rod. From the mesoblast are formed all the remaining parts of the body. The muscles, the bones, the connective tissue and the vessels, both arteries, veins, capillaries and lymphatics with their appropriate epithelium, are entirely formed from the mesoblast.

The generative and urinary organs are entirely derived from the mesoblast. It is worthy of notice that the epithelium of the urinary glands, though resembling the hypoblastic epithelium of the alimentary canal, is undoubtedly mesoblastic.

From the mesoblast are lastly derived all the muscular, connective tissue, and vascular elements, as well of the alimentary canal and its appendages as of the skin and the tegumentary organs. Just as it is only the epidermic moiety of the latter which is derived from the epiblast, so it is only the epithelium of the former which comes from the hypoblast.

Growth in length of the Vertebrate Embryo.

With reference to the formation and growth in length of the body of the Vertebrate embryo two different views have been put forward, which can be best explained by taking the Elasmobranch embryo as our type. One of these views, generally held by embryologists and adopted in the previous pages, is that the Elasmobranch embryo arises from a differentiation of the edge of the blastoderm ; which extends inwards from the edge for some little distance. This differentiation is supposed to contain within itself the rudiments of the whole of the embryo with the exception of the yolk-sack ; and the hinder extremity of it, at the edge of the blastoderm, is regarded as corresponding with the hind end of the body of the adult. The growth in length takes place by a process of intussusception, and, till there are formed the full number of mesoblastic somites, it is effected, as in Chastopods, by the continual addition of fresh somites between the last-formed somite and the hind end of the body.

A second and somewhat paradoxical view has been recently brought into prominence by His and Rauber. This view has moreover since been taken up by many embryologists, and has led to strange comparisons between the


COMPARISON OF THE GERMINAL LAYERS. 307

formation of the mesoblastic plates of the Chastopods and the medullary folds of Vertebrata. According to this view the embryo grows in length by the coalescence of the two halves of the thickened edges of the blastoderm in the dorsal median line. The groove between the coalescing edges is the medullary groove, which increases in length by the continued coalescence of fresh portions of the edge of the blastoderm.

The following is His' own statement of his view: "I have shewn that the embryo of Osseous Fishes grows together in length from two symmetricallyplaced structures in the thickened edge of the blastoderm. Only the foremost end of the head and the hindermost end of the tail undergo no concrescence, since they are formed out of that part of the edge of the blastoderm which, together with the two lateral halves, completes the ring. The whole edge of the blastoderm is used in the formation of the embryo."

The edges of the blastoderm which meet to form the body of the embryo are regarded as the blastopore, so that, on this view, the blastopore primitively extends for the whole length of the dorsal side of the embryo, and the groove between the coalesced lips becomes the medullary groove.

It is not possible for me to enter at any great length into the arguments used to support this position.

They may be summarised as (i) The general appearance ; i.e. that the thickened edge of the blastoderm is continuous with the medullary fold.

(2) Certain measurements (His) which mainly appear to me to prove that the growth takes place by the addition of fresh somites between that last formed and the end of the body.

(3) Some of the phenomena of double monsters (Rauber).

None of these arguments appear to be very forcible, but as the view of His and Rauber, if true, would certainly be important, I shall attempt shortly to state the arguments against it, employing as my type the Elasmobranchii, by the development of which, according to His, the view which he adopts is more conclusively proved than by that of any other group.

(1) The general appearance of the thickened edge of the blastoderm becoming continuous with the medullary folds has been used as an argument for the medullary folds being merely the coalesced thickened edges of the blastoderm. Since, however, the medullary folds are merely parts of the medullary plate, and since the medullary plate is continuous with the adjoining epiblast of the embryonic rim, the latter structure must be continuous with the medullary folds however they are formed, and the mere fact of their being so continuous cannot be used as an argument either way. Moreover, were the concrescence theory true, the coalescing edges of the blastoderm might be expected to form an acute angle with each other, which they are far from doing.

(2) The medullary groove becomes closed behind earlier than in front, and the closure commences while the embryo is still quite short, and before the hind end has begun to project over the yolk. After the medullary canal becomes closed, and is continued behind into the alimentary canal by the neurenteric passage, it is clearly impossible for any further increase in length

20 2


308 GROWTH IN LENGTH OF THE EMBRYO.

to take place by concrescence. If therefore His' and Rauber's view is accepted, it will have to be maintained that only a small part of the body is formed by concrescence, while the larger posterior part grows by intussusception. The difficulty involved in this supposition is much increased by the fact that long after the growth by concrescence must have ceased the yolk blastopore still remains open, and the embryo is still attached to the edge of the blastoderm ; so that it cannot be maintained that the growth by concrescence has come to an end because the thickened edges of the blastoderm have completely coalesced.

The above are arguments derived simply from a consideration of the growth of the embryo ; and they prove (i) that the points adduced by His and Rauber are not at all conclusive ; (2) that the growth in length of the greater part of the body takes place by the addition of fresh somites behind, as in Chaetopods, and it would therefore be extremely surprising that a small middle part of the body should grow in quite a different way.

Many minor arguments used by His might be replied to, but it is hardly necessary to do so, and some of them depend upon erroneous views as to the course of development, such as an argument about the notochord, which depends for its validity upon the assumption that the notochord ridge appears at the same time as the medullary plate, while, as a matter of fact, the ridge does not appear till considerably later. In addition to the arguments of the class hitherto used, there may be brought against the His-Rauber view a series of arguments from comparative embryology.

(1) Were the vertebrate blastopore to be co- extensive with the dorsal surface, as His and Rauber maintain, clear evidence of this ought to be apparent in Amphioxus. In Amphioxus, however, the blastopore is at first placed exactly at the hind end of the body, though later it passes up just on to the dorsal side (vide p. 4). It nearly closes before the appearance of the medullary groove or mesoblastic somites ; and the medullary folds have nothing to do with its lips, except in so far as they are continuous with them behind, just as in Elasmobranchii.

(2) The food-yolk in the Vertebrata is placed on the ventral side of the body, and becomes enveloped by the blastoderm ; so that in all large-yolked Vertebrates the ventral walls of the body are obviously completed by the closure of the lips of the blastopore, on the ventral side.

If His and Rauber are right the dorsal walls are also completed by the closure of the blastopore, so that the whole of the dorsal, as well as of the ventral wall of the embryo, must be formed by the concrescence of the lips of the blastopore ; which is clearly a reductio adabsurdum of the whole theory. To my own arguments on the subject I may add those of Kupffer, who has very justly criticised His' statements, and has shewn that growth of the blastoderm in Clupea and Gasterosteus is absolutely inconsistent with the concrescence theory.

The more the theory of His and Rauber is examined by the light of comparative embryology, the more does it appear quite untenable ; and it may be laid down as a safe conclusion from a comparative study of vertebrate



COMPARISON OF THE GERMINAL LAYERS. 309

embryology that the blastopore of Vertebrates is primitively situated at the hind end of the body, but that, owing to the development of a large food-yolk, it also extends, in most cases, over a larger or smaller part of the ventral side.

The origin of the Allantois and Amnion.

The development and structure of the allantois and amnion have already been dealt with at sufficient length in the chapters on Aves and Mammalia ; but a few words as to the origin of these parts will not be out of place here.

The Allantois. The relations of the allantois to the adjoining organs, and the conversion of its stalk into the bladder, afford ample evidence that it has taken its origin from a urinary bladder such as is found in Amphibia. We have in tracing the origin of the allantois to deal with a case of what Dohrn would call ' change of function.' The allantois is in fact a urinary bladder which, precociously developed and enormously extended in the embryo, has acquired respiratory (Sauropsida) and nutritive (Mammalia) functions. No form is known to have been preserved with the allantois in a transitional state between an ordinary bladder and a large vascular sack.

The advantage of secondary respiratory organs during fcetal life, in addition to the yolk-sack, is evinced by the fact that such organs are very widely developed in the Ichthyopsida. Thus in Elasmobranchii we have the external gills (cf. p. 62). Amongst Amphibia we have the tail modified to be a respiratory organ in Pipa Americana ; and in Notodelphis, Alytes and Cascilia compressicanda the external gills are modified and enlarged for respiratory purposes within the egg (cf. pp. 140 and 143).

The Amnion. The origin of the amnion is more difficult to explain than that of the allantois ; and it does not seem possible to derive it from any pre-existing organ.

It appears to me, however, very probable that it was evolved part flassu with the allantois, as a simple fold of the somatopleure round the embryo, into which the allantois extended itself as it increased in size and became a respiratory organ. It would be obviously advantageous for such a fold, having once started, to become larger and larger in order to give more and more room for the allantois to spread into.

The continued increase of this fold would lead to its edges meeting on the dorsal side of the embryo, and it is easy to conceive that they might then coalesce.

To afford room for the allantois close to the surface of the egg, where respiration could most advantageously be carried on, it would be convenient that the two laminae of the amnion the true and false amnion should then separate and leave a free space above the embryo, and thus it may have come about that a separation finally takes place between the true and false amnion.

This explanation of the origin of the amnion, though of course hypothetical, has the advantage of suiting itself in most points to the actual ontogeny


310 ORIGIN OF ALLANTOIS AND AMNION.

of the organ. The main difficulty is the early development of the head-fold of the amnion, since, from the position of the allantois, it might have been anticipated that the tail-fold would be the first formed and most important fold of the amnion.

BIBLIOGRAPHY.

(239) F. M. Balfour. " A comparison of the early stages in the development of Vertebrates." Q:tarf. J. of Micr. Science, Vol. xv. 1875.

(240) F. M. Balfour. "A monograph on the development of Elasmobranch Fishes." London, 1878.

(241) F. M. Balfour. " On the early development of the Lacertilia together with some observations, etc." Quart, y. of Micr. Science, Vol. xix. 1879.

(242) A. Gotte. Die Entwicklungsgeschichte d. Unke. Leipzig, 1875.

(243) W. His. "Ueb. d. Bildung d. Haifischembryonen." Zeit. f. Anat, u. Entwick., Vol. u. 1877. Cf. also His' papers on Teleostei, Nos. 65 and 66.

(244) A. Kowalevsky. " Entwick. d. Amphioxus lanceolatus." Mem. Acad. des Sciences St Petersbourg, Ser. vn. Tom. xi. 1867.

(245) A. Kowalevsky. " Weitere Studien lib. d. Entwick. d. Amphioxus lanceolatus." Archivf. mikr. Anat., Vol. xiil. 1877.

(246) C. Kupffer. "Die Entstehung d. Allantois u. d. Gastrula d. Wirbelthiere." Zool. Anzeiger, Vol. II. 1879, PP- 5 2 ' 593> 612.

(247) R. Remak. Untersuchimgen iib. d. Entwicklung d. Wirbelthiere, 1850 1858.

(248) A. Rauber. Primitimtreifen u. Neurula d. Wirbelthiere. Leipzig, 1877.



CHAPTER XII.

OBSERVATIONS ON THE ANCESTRAL FORM OF THE CHORDATA.

THE present section of this work would not be complete without some attempt to reconstruct, from the materials recorded in the previous chapters, and from those supplied by comparative anatomy, the characters of the ancestors of the Chordata ; and to trace as far as possible from what invertebrate stock this ancestor was derived.

The second of these questions has been recently dealt with in a very suggestive manner by both Dohrn (No. 250) and Semper (Nos. 255 and 256), but it is still so obscure that I shall refrain from any detailed discussion of it.

While differing very widely in many points both Dohrn and Semper have arrived at the view, already tentatively put forward by earlier anatomists, that the nearest allies of the Chordata are to be sought for amongst the Chaetopoda, and that the dorsal surface of the Chordata with the spinal cord corresponds morphologically with the ventral surface of the Chaetopods with the ventral ganglion chain. In discussing this subject some time ago x I suggested that we must look for the ancestors of the Chordata, not in allies of the present Chaetopoda, but in a stock of segmented forms descended from the same unsegmented types as the Chaetopoda, but in which two lateral nerve-cords, like those of Nemertines, coalesced dorsally, instead of ventrally to form a median nervous cord. This group of forms, if my suggestion as to its existence is well founded, appears now to have perished. The recent researches of Hubrecht on the anatomy of the Nemertines a have, however, added somewhat to the probability of my views, in that they shew that in some existing Nemertines the nerve-cords approach each other very closely in the dorsal line.

With reference to the characters of the ancestor of the Chordata the following pages contain a few tentative suggestions rather than an attempt to deal with the whole subject ; while the

1 Monograph on the development of Elasmobranch Fishes, pp. 170 173.

2 Hubrecht, "Zur Anat. u. Phys. d. Nervensystems der Nemertinen. " Kon. Akad. Wiss. Amsterdam; and "Researches on the Nervous System of Nemertines." Quart. Journ. of Micr. Science, 1880.


312 THE PR^iORAL LOBE.

origin of certain of the organs is dealt with in a more special manner in the chapters on organogeny which form the second part of this work.

Before entering upon the more special subject of this chapter, it will be convenient to clear the ground by insisting on a few morphological conclusions to be drawn from the study of Amphioxus, a form which, although probably in some respects degenerate, is nevertheless capable of furnishing on certain points very valuable evidence.

(1) In the first place it is clear from Amphioxus that the ancestors of the Chordata were segmented, and that their mesoblast was divided into myotomes which extended even into the region in front of the mouth. The mesoblast of the greater part of what is called the head in the Vertebrata proper was therefore segmented like that of the trunk.

(2) The only internal skeleton present was the unsegmented notochord a fact which demonstrates that the skeleton is of comparatively little importance for the solution of a large number of fundamental questions, as for example the point which has been mooted recently as to whether gill-clefts existed at one time in front of the present mouth ; and for this reason : that from the evidence of Amphioxus and the lower Vertebrata 1 it is clear that such clefts, if they ever existed, had atrophied

1 The greater part of the branchial skeleton of Petromyzon appears clearly to belong to an extra-branchial system much more superficially situated than the true branchial bars of the higher forms. At the same time-there is no doubt that certain parts of the skeleton of the adult Lamprey have, as pointed out by Huxley, striking points of resemblance to parts of a true mandibular and hyoid arches. Further embryological evidence is required on the subject, but the statements on this head on p. 84 ought to be qualified.

Should Huxley's views on this subject be finally proved correct, it is probable that, taking into consideration the resemblance of these skeletal parts in the Tadpole to those in the Lamprey, the cartilaginous mandibular bar, before being in any way modified to form true jaws, became secondarily adapted to support a suctorial mouth, and that it subsequently became converted into the true jaws. Thus the evolution of this bar in the Frog would be a true repetition of the ancestral history, while its ontogeny in Elasmobranchii and other types would be much abbreviated. For a fuller statement on this point I must refer the reader to the chapter on the skull.

It is difficult to believe that the posterior branchial bars could have coexisted with such a highly developed branchial skeleton as that in Petromyzon, so that the absence of the posterior branchial bars in Petromyzon receives by far its most plausible explanation on the supposition that Petromyzon is descended from a vertebrate stock in which true branchial bars had not been evolved.


ON THE ANCESTRAL FORM OF THE CHORDATA. 313

completely before the formation of cartilaginous branchial bars ; so that any skeletal structures in front of the mouth, which have been interpreted by morphologists as branchial bars, can never have acted in supporting the walls of branchial clefts.

(3) The region which, in the Vertebrata, forms the oesophagus and stomach, was, in the ancestors of the Chordata, perforated by gill-clefts. This fact, which has been clearly pointed out by Gegenbaur, is demonstrated by the arrangement of the gill-clefts in Amphioxus, and by the distribution of the vagus nerve in the Vertebrata 1 . On the other hand the insertion of the liver, which was probably a very primitive organ, appears to indicate with approximate certainty the posterior limit of the branchial clefts.

With these few preliminary observations we may pass to the main subject of this section. A fundamental question which presents itself on the threshold of our enquiries is the differentiation of the head.

In the Chaetopoda the head is formed of a praeoral lobe and of the oral segment ; while in Arthropods a somewhat variable number of segments are added behind to this primitive head, and form with it what may be called a secondary compound head. It is fairly clear that the section of the trunk, which, in Amphioxus, is perforated by the visceral clefts, has become the head in the Vertebrates proper, so that the latter forms are provided with a secondary head like that of Arthropods. There remain however difficult questions (i) as to the elements of which this head is composed, and (2) as to the extent of its differentiation in the ancestors of the Chordata.

In Arthropods and Chaetopods there is a very distinct element in the head known as the procephalic lobe in the case of Arthropods, and the praeoral lobe in that of Chaetopods ; and this lobe is especially characterized by the fact that the supracesophageal ganglia and optic organs are formed as differentia 1 The extension forwards in the vertebrata of an uninterrupted body-cavity into the region previously occupied by visceral clefts presents no difficulty. In Amphioxus the true body cavity extends forwards, more or less divided by the branchial clefts, for the whole length of the branchial region, and in embryos of the lower Vertebrata there is a section of the body cavity the so-called head-cavities between each pair of pouches. On the disappearance of the pouches all these parts would naturally coalesce into a continuous whole.


314 THE PR/KORAL LOBE.

tions of part of the epiblast covering it. Is such an element to be recognized in the head of the Chordata ? From a superficial examination of Amphioxus the answer would undoubtedly be no ; but then it has to be borne in mind that Amphioxus, in correlation with its habit of burying itself in sand, is especially degenerate in the development of its sense-organs ; so that it is not difficult to believe that its praeoral lobe may have become so reduced as not to be recognizable. In the true Vertebrata there is a portion of the head which has undoubtedly many features of the praeoral lobe in the types already alluded to, viz. the part containing the cerebral hemispheres and the thalamencephalon. If there is any part of the brain homologous with the supracesophageal ganglia of the Invertebrates, and it is difficult to believe there is not such a part, it must be part of, or contain, the fore-brain. The fore-brain resembles the supraoesophageal ganglia in being intimately connected in its development with the optic organs, and in supplying with nerves only organs of sense. Its connection with the olfactory organs is an argument in the same direction. Even in Amphioxus there is a small bulb at the end of the nervous tube supplying what is very probably the homologue of the olfactory organ of the Vertebrata ; and it is quite possible that this bulb is the reduced rudiment of what forms the fore-brain in the Vertebrata.

The evidence at our disposal appears to me to indicate that the third nerve belongs to the cranio-spinal series of segmental nerves, while the optic and olfactory nerves appear to me equally clearly not to belong to this series 1 . The mid-brain, as giving origin to the third nerve, would appear not to have been part of the ganglion of the prseoral lobe.

These considerations indicate with fair probability that the part of the head containing the fore-brain is the equivalent of the praeoral lobe of many Invertebrate forms ; and the primitive position of the Vertebrate mouth on the ventral side of the head affords a distinct support for this view. It must however be admitted that this part of the head is not sharply separated in development from that behind ; and, though the fore-brain is

1 Marshall, in his valuable paper on the development of the olfactory organ, takes a very different view of this subject. For a discussion of this view I must refer the reader to the chapter on the nervous system.


ON THE ANCESTRAL FORM OF THE CHORDATA. 315

usually differentiated very early as a distinct lobe of the primitive nervous tube, yet that such differentiation is hardly more marked than in the other parts of the brain. The termination of the notochord immediately behind the fore-brain is, however, an argument in favour of the morphological distinctness of the latter structure.

The evidence at our disposal appears to indicate that the posterior part of the head was not differentiated from the trunk in lower Chordata ; but that, as the Chordata rose in the scale of development, more and more centralizing work became thrown on the anterior part of the nervous cord, and part passu this part became differentiated into the mid- and hind-brain. An analogy for such a differentiation is supplied in the compound subcesophageal ganglion of many Arthropods ; and, as will be shewn in the chapter on the nervous system, there is strong embryological evidence that the mid- and hind-brains had primitively the same structure as the spinal cord. The head appears however to have suffered in the course of its differentiation a great concentration in its posterior part, which becomes progressively more marked, even within the limits of the surviving Vertebrata. This concentration is especially shewn in the structure of the vagus nerve, which, as first pointed out by Gegenbaur, bears evidence of having been originally composed of a great series of nerves, each supplying a visceral cleft. Rudiments of the posterior nerves still remain as the branches to the oesophagus and stomach 1 .

The atrophy of the posterior visceral clefts seems to have taken place simultaneously with the concentration of the neural part of the head ; but the former process did not proceed so rapidly as the latter, so that the visceral region of the head is longer in the lower Vertebrata than the neural region, and is dorsally overlapped by the anterior part of the spinal cord and the anterior muscle-plates (vide fig. 47).

On the above view the posterior part of the head must have been originally composed of a series of somites like those of the

1 The lateral branch of the vagus nerve probably became differentiated in connection with the lateral line, which seems to have been first formed in the head, and subsequently to have extended into the trunk (vide section on Lateral Line).


3'6


Till. MEDULLARY CANAL.


trunk, but in existing Vertebrata all trace of these, except in so far as they are indicated by the visceral clefts, has vanished in the adult. The cranial nerves however, especially in the embryo, still indicate the number of anterior somites ; and an embryonic segmentation of the mesoblast has also been found in many lower forms in the region of the head, giving rise to a series of cavities known as head-cavities, enclosed by mesoblastic walls which afterwards break up into muscles. These cavities correspond with the nerves, and it appears that there is a praemandibular cavity corresponding with the third nerve (fig. 193, \pp) and a mandibular cavity (2pp) and a cavity in each of the succeeding visceral arches. The fifth nerve, the seventh nerve, the glossopharyngeal nerve, and the successive elements of the vagus nerve correspond with the posterior head-cavities.

The medullary canal. The general history of the medullary plate seems to point to the conclusion that the central canal of the nervous system has been formed by a groove having appeared in the ancestor of the Chordata along the median dorsal line, which caused the sides of the nervous plate, which was placed immediately below the skin, or may perhaps at that stage not have been distinctly differentiated from the skin, to be bent upwards ; and that this groove subsequently became converted into a canal. This view is not only supported by the actual development of the central canal of the nervous system (the types of Teleostei, Lepidosteus and Petromyzon being undoubtedly secondary), but also (i) by the presence of cilia in the epithelium lining the canal, probably inherited from cilia coating the external skin, and (2) by



FIG. 193. TRANSVERSE SECTION THROUGH THE FRONT PART OF THE HEAD OF A YOUNG PRISTIURUS

EMBRYO.

The section, owing to the cranial flexure, cuts both the fore- and the hind-brain. It shews the prsemandibular and mandibular head-cavities ipp and ipp, etc.

fb. fore-brain; /. lens of eye; /. mouth ; pt. upper end of mouth, forming pituitary involution; iao.. mandibular aortic arch; ipp. and ipp. first and second head-cavities ; ivc. first visceral cleft ; V. fifth nerve ; aun. ganglion of auditory nerve ; VII. seventh nerve ; aa, dorsal aorta ; acv. anterior cardinal vein; ^..notochord.


ON THE ANCESTRAL FORM OF THE CHORDATA.


317


the posterior roots arising from the extreme dorsal line (fig. 194), a position which can most easily be explained on the supposition that the two sides of the plate, from which the nerves originally proceeded have been folded up so as to meet each other in the median dorsal line 1 .

The medullary plate, before becoming folded to form the medullary groove, is (except in Amphibia) without any indication of being composed of two halves. In both the embryo and adult the walls of the tube have however a structure which points to their having arisen from the coalescence of two lateral, and most probably at one time independent, cords ; and as already indicated this is the view I am myself inclined to adopt ; vide pp. 303 and

304 The origin and nature of the mouth. The most obvious point connected with the development of the mouth is the fact that in all vertebrate embryos it is placed ventrally, at some little distance from the front end of the body. This feature is retained in the adult stage in Elasmobranchii, the Myxinoids, and some Ganoids, but is lost in other vertebrate forms. A mouth, situated as is the embryonic vertebrate mouth, is very ill adapted for biting ; and though it acquires in this position a distinctly biting character in the Elasmobranchii, yet it is almost certain that it had not such a character in the ancestral Chordata, and that its terminal position in higher types indicates a step in advance of the Elasmobranchii.

On the structure of the primitive mouth there appears to me



al


FIG. 194. TRANSVERSE SECTION THROUGH THE TRUNK OF AN EMBRYO SLIGHTLY OLDER THAN FIG. 28 E.

nc. neural canal ; pr. posterior root of spinal nerve ; x. subnotochordal rod ; ao. aorta ; sc. somatic mesoblast ; sp. splanchnic mesoblast ; mp. muscle-plate ; mp'. portion of muscle-plate converted into muscle ; Vv. portion of the vertebral plate which will give rise to the vertebral bodies ; al. alimentary tract.


1 Vidf for further details the chapter on the nervous system.


318 PRIMITIVE SUCTORIAL MOUTH.

to be some interesting embryological evidence, to which attention has already been called in the preceding chapters. In a large number of the larvae or embryos of the lower Vertebrates the mouth has a more or less distinctly suctorial character, and is connected with suctorial organs which may be placed either in front of or behind it. The more important instances of this kind are (i) the Tadpoles of the Anura, with their posteriorly placed suctorial disc, (2) Lepidosteus larva (fig. 195) with its anteriorly placed suctorial disc, (3) the adhesive papillae of the larvae of the Tunicata. To these may be added the suctorial mouth of the Myxinoid fishes 1 .

All these considerations point to the conclusion that in the ancestral Chordata the mouth had a more or less definitely suctorial character 2 , and was placed on the ventral surface immediately behind the praeoral lobe; and that this mouth has become in the higher types gradually modified for biting purposes, and has been carried to the front end of the head.

The mouth in Elasmobranchii and other Vertebrates is originally a wide somewhat rhomboidal cavity (fig. 28 G) ; on the development of the mandibular and its maxillary (pterygoquadrate) process the opening of the mouth becomes narrowed to a slit. The wide condition of the mouth may not improbably be interpreted as a remnant of the suctorial state. The fact that no more definite remnants of the suctorial mouth are found in so primitive a group as the Elasmobranchii is probably to be explained by the fact that the members of this group undergo an abbreviated development within the egg.


1 The existing Myxinoid P'ishes are no doubt degenerate types, as was first clearly pointed out by Dohrn ; but at the same time (although Dohrn does not share this view) it appears to me almost certain that they are the remnants of a large and very primitive group, which have very likely been preserved owing to their parasitic or semiparasitic habits ; much in the same way as many of the Insectivora have been preserved owing to their subterranean habits. I am acquainted with no evidence, embryological or otherwise, that they are degraded gnathostomatous forms, and the group probably disappeared as a whole from its incapacity to compete successfully with Vertebrata in which true jaws had become developed.

3 I do not conceive that the existence of suctorial structures necessarily implies parasitic habits. They might be used for various purposes, especially by predaceous forms not provided with jaws.


ON THE ANCESTRAL FORM OF THE CHORDATA. 319

While the embryological data appear to me to point to the existence of a primitive suctorial mouth, very different conclusions have been put forward by other embryologists, more especially by Dohrn, which are sufficiently striking and suggestive to merit a further discussion.

As mentioned above, both Dohrn and Semper hold that the Vertebrata are descended from Chastopod-like forms, in which the ventral surface has become the dorsal. In consequence of this view Dohrn has arrived at the following conclusions : (i) that primitively the alimentary canal perforated the nervous system in the region of the original cesophageal nerve-ring ; (2) that there was therefore an original dorsal mouth (the present ventral mouth of the Cheetopoda) ; and (3) that the present mouth was secondary and derived from two visceral clefts which have ventrally coalesced.

A full discussion of these views 1 is not within the scope of this work ; but, while recognizing that there is much to be said in favour of the interchange of the dorsal and ventral surfaces, I am still inclined to hold that the difficulties involved in this view are so great that it must, provisionally at least, be rejected; and that there are therefore no reasons against supposing



-sd


op

FIG. 195. VENTRAL VIEW OF THE HEAD OF A LEPIDOSTEUS EMBRYO SHORTLY

BEFORE HATCHING, TO SHEW THE LARGE SUCTORIAL DISC.

m. mouth ; op. eye ; sd. suctorial disc.

the present vertebrate mouth to be the primitive mouth. There is no embryological evidence in favour of the view adopted by Dohrn that the present mouth was formed by the coalescence of two clefts.

If it is once admitted that the present mouth is the primitive mouth, and is more or less nearly in its original situation, very strong evidence will be required to shew that any structures originally situated in front of it are the remnants of visceral clefts ; and if it should be proved that such remnants of visceral clefts were present, the views so far arrived at in this section would, I think, have to be to a large extent reconsidered.

The nasal pits have been supposed by Dohrn to be remnants of visceral

1 For a partial discussion of this subject I would refer the reader to my Monograph on Elasmobranch Fishes, pp. 165 172.


320 FORMATION OF THE JAWS.

clefts, and this view has been maintained in a very able manner by Marshall. The arguments of Marshall do not, however, appear to me to have any great weight unless it is previously granted that there is an antecedent probability in favour of the presence of a pair of gill-clefts in the position of the nasal pits ; and even then the development of the nasal pits as epiblastic involutions, instead of hypoblastic outgrowths, is a serious difficulty which has not in my opinion been successfully met. A further argument of Marshall from the supposed segmental nature of the olfactory nerve has already been spoken of.

While most of the structures supposed to be remains of gill-clefts in front of the mouth do not appear to me to be of this nature, there is one organ which stands in a more doubtful category. This organ is the so-called choroid gland. The similarity of this organ to the pseudo-branch of the mandibular or hyoid arch was pointed out to me by Dohrn, and the suggestion was made by him that it is the remnant of a praemandibular gill which has been retained owing to its functional connection with the eye 1 . Admitting this explanation to be true (which however is by no means certain) are we necessarily compelled to hold that the choroid gland is the remnant of a gill-cleft originally situated in front of the mouth ? I believe not. It is easy to conceive that there may originally have been a praemandibular cleft behind the suctorial mouth, but that this cleft gradually atrophied (for the same reasons that the mandibular cleft shews a tendency to atrophy in existing fishes, &c.), the rudiment of the gill (choroid gland) alone remaining to mark its situation. After the disappearance of this cleft the suctorial mouth may have become relatively shifted backwards. In the meantime the branchial bars became developed, and as the mouth was changed into a biting one, the

1 The probability of the choroid gland having the meaning attributed to it by Dohrn is strengthened by the existence of a praemandibular segment as evidenced by the presence of a pnemandibular head-cavity, the walls of which as shewn by Marshall and myself give rise to the majority of the eye-muscles and of a nerve (the third nerve, cf. Marshall) corresponding to it; so that these parts together with the choroid gland may be rudiments belonging to the same segment. On the other hand the absence of the choroid gland in Ganoidei and Elasmobranchii, where a mandibular pseudo-branch is present, coupled with the absence of a mandibular pseudo-branch in Teleostei where alone a choroid gland is present, renders the above view about the choroid gland somewhat doubtful. A thorough investigation of the ontogeny of the choroid gland might throw further light on this interesting question, but I think it not impossible that the" choroid gland may be nothing else but the modified mandibtddr pseudo-branch, a view which fits in very well with the relations of the vessels of the Elasmobranch mandibular pseudo-branch to the choroid. For the relations and structure of the choroid gland vide F. Miiller, Vergl. Anal. Myxinoiden, Part in. p. 82.

It is possible that the fourth nerve and the superior oblique muscle of the eye which it supplies may be the last remaining remnants of a second praemandibular segment originally situated between the segment of the third nerve and that of the fifth nerve (mandibular segment).



ON THE ANCESTRAL FORM OF THE CHORDATA. 321


bar (the mandibular arch) supporting the then first cleft became gradually modified and converted into a supporting apparatus for the mouth, and finally formed the skeleton of the jaws. In the hyostylic Vertebrata the hyoid arch also became modified in connection with the formation of the jaws.

The conclusions arrived at may be summed up as follows : The relations which exist in all jaw-bearing Vertebrates between the mandibular arch and the oral aperture are secondary, and arose paripassu with the evolution of the jaws 1 .

The cranial flexure and the form of the head in vertebrate embryos. All embryologists who have studied the embryos of the various vertebrate groups have been struck with the remarkable similarity


Vgr


aur


vir



FIG. 196. THE HEADS OF ELASMOBRANCH EMBRYOS AT TWO STAGES VIEWED

AS TRANSPARENT OBJECTS.

A. Pristiurus embryo of the same stage as fig. 28 F. B. Somewhat older Scyllium embryo.

///. third nerve; V. fifth nerve; VII. seventh nerve; au.n. auditory nerve; gl. glossopharyngeal nerve; Vg. vagus nerve; fb. fore-brain; pn. pineal gland; mb. midbrain; hb. hind-brain; iv.v. fourth ventricle; cb. cerebellum; ol. olfactory pit; op. eye; au.V. auditory vesicle; m. mesoblast at base of brain; ch. notochord; ht. heart; Vc. visceral clefts ; eg. external gills ; //. sections of body cavity in the head.

1 I do not mean to exclude the possibility of the mandibular arch having supported a suctorial mouth before it became converted into a pair of jaws.

B. III. 21


322 POST-ANAL GUT.


which exists between them, more especially as concerns the form of the head. This similarity is closest between the members of the Amniota, but there is also a very marked resemblance between the Amniota and the Elasmobranchii. The peculiarity in question, which is characteristically shewn in fig. 196, consists in the cerebral hemispheres and thalamencephalon being ventrally flexed to such an extent that the mid- brain forms the termination of the long axis of the body. At a later period in development the cerebral hemispheres come to be placed at the front end of the head ; but the original nick or bend of the floor of the brain is never got rid of.

It is obvious that in dealing with the light thrown by embryology on the ancestral form of the Chordata the significance of this peculiar character of the head of many vertebrate embryos must be discussed. Is the constancy of this character to be explained by supposing that at one period vertebrate ancestors had a head with the same features as the embryonic head of existing Vertebrata ?

This is the most obvious explanation, but it does not at the same time appear to me satisfactory. In the first place the mouth is so situated at the time of the maximum cranial flexure that it could hardly have been functional ; so that it is almost impossible to believe that an animal with a head such as that of these embryos can have existed.

Then again, this type of embryonic head is especially characteristic of the Amniota, all of which are developed in the egg. It is not generally so marked in the Ichthyopsida. In Amphibia, Teleostei, Ganoidae and Petromyzontidae, the head never completely acquires the peculiar characteristic form of the head of the Amniota, and all these forms are hatched at a relatively much earlier phase of development, so that they are leading a free existence at a stage when the embryos of the Amniota are not yet hatched. The only Ichthyopsidan type with a head like that of the Amniota is the Elasmobranchii, and the Elasmobranchii are the only Ichthyopsida which undergo the major part of their development within the egg.

These considerations appear to shew that the peculiar characters of the embryonic head above alluded to are in some way connected with an embryonic as opposed to a larval development ; and for reasons which are explained in the section on larval forms, it is probable that a larval development is a more faithful record of ancestral history than an embryonic development. The flexure at the base of the brain appears however to be a typical vertebrate character, but this flexure never led to a conformation of the head in the adult state similar to that of the embryos of the Amniota. The form of the head in these embryos is probably to be explained by supposing that some advantage is gained by a relatively early development of the brain, which appears to be its proximate cause ; and since these embryos had not to lead a free existence (for which such a form of the head would have been unsuited) there was nothing to interfere with the action of natural selection in bringing about this form of head during fcetal life.

Post-anal gut and neurenteric canal. One of the most


ON THE ANCESTRAL FORM OF THE CHORDATA. 323

remarkable structures in the trunk is the post-anal gut (fig. 197). Its structure is fully dealt with in the chapter on the alimentary tract, but attention may here be called to the light which it appears to throw on the characters of the ancestor of the Chordata.

In face of the facts which are known with reference to the post-anal section of the alimentary tract, it can hardly be doubted that this portion of the alimentary tract must have been at one time functional. This seems to me to be shewn (i) by the constancy and persistence of this obviously now functionless rudiment, (2) by its greater development in the lower than in the higher forms, (3) by its relation to the formation of the notochord and subnotochordal rod.

If the above position be admitted, it is not permissible to shirk the conclusions which seem necessarily to follow, however great the difficulties may be which are involved in their accept


FIG. 197. LONGITUDINAL SECTION THROUGH AN ADVANCED EMBRYO OF BOM BINATOR. (After Gotte.)

m. mouth; an. anus; /. liver; ne. neurenteric canal; me. medullary canal; ch. notochord; pn. pineal gland.

ance. These conclusions have in part already been dealt with by Dohrn in his suggestive tract (No. 250). In the first place the alimentary canal must primitively have been continued to the end of the tail ; and if so, it is hardly credible that the existing anus can have been the original one. Although, therefore, it is far from easy, on the physiological principles involved in the Darwinian theory, to understand the formation of a new anus 1 ; it is nevertheless necessary to believe that the present

1 Dohrn (No. 250, p. 25) gives an explanation of the origin of the new anus which does not appear to me quite satisfactory.

21 2


324


POST-ANAL GUT.


vertebrate anus is a formation acquired within the group of the Chordata, and not inherited from some older group. This involves a series of further consequences. The opening of the urinogenital ducts into the cloaca must also be secondary, and it is probable that the segmental tubes were primitively continued along the whole post-anal region of the vertebrate tail, opening into the body cavity which embryology proves to have been originally present there. They are in fact continued in many existing forms for some distance behind the present anus. If the present anus is secondary, there must have been a primitive anus, which was probably situated behind the post-anal vesicle ; and therefore in the region of the neurenteric canal. The neurenteric canal is, however, the remnant of the blastopore (vide p. 277). It follows, therefore, that tJie vertebrate blastopore is probably almost, if not exactly identical in position with the primitive aims. This consideration may assist in explaining the remarkable phenomenon of the existence of the neurenteric canal. The attempt has already been made to shew that the central canal of the nervous system is really a groove converted into a tube and lined by the external epidermis. This tube (as may be concluded from embryological considerations) was probably at first open posteriorly, and no doubt terminated at the primitive anus. On the closure of the primitive anal opening, the terminal portions of the post-anal gut and the neural tube, may conceivably have been so placed that both of them opened into a common cavity, which previously had communication with the exterior by the anus. Such an arrangement would necessarily result in the formation of a neurenteric canal. It seems not impossible that a dilated vesicle, often present at the end of the post-anal gut (vide fig. 28*, p. 58), may have been the common cavity into which both neural and alimentary tubes opened 1 .

1 As pointed out in Vol. II. p. 255, there is a striking similarity between the history of the neurenteric canal in Vertebrates, and the history of the blastopore and ventral groove as described by Kowalevsky in the larva of Chiton. Mr A. Sedgwick has pointed out to me that the ciliated ventral groove in Protoneomenia, which contains the anus, is probably the homologue of the groove found in the larva of Chiton, and not, as usually supposed, simply the foot. Were this groove to be converted into a canal, on the sides of which were placed the nervous cords, there would be formed a precisely similar neurenteric canal to that in Vertebrata, though I do not mean to suggest that there is any homology between the two (vide Hubrecht, Zool. Anzeigcr, 1880, p. 589).


ON THE ANCESTRAL FORM OF THE CHORDATA. 325

Till further light is thrown by fresh discoveries upon the primitive condition of the posterior continuation of the vertebrate alimentary tract, it is perhaps fruitless to attempt to work out more in detail the 'above speculation.

Body cavity and mesoblastic somites. The Chordata, or at least the most primitive existing members of the group, are characterized by the fact that the body cavity arises as a pair of outgrowths of the archenteric cavity. This feature 1 in the development is a nearly certain indication that the Chordata are a very primitive stock. The most remarkable point with reference to the development of the two outgrowths is, however, the fact that the dorsal part of each outgrowth becomes separated from the ventral. Its walls become segmented and form the mesoblastic somites, which eventually, on the obliteration of their cavity, give rise to the muscle-plates and to the tissue surrounding the notochord. It is not easy to understand the full significance of the processes concerned in the formation of the mesoblastic somites (vide p. 296). The mesoblastic somites have no doubt a striking resemblance to the mesoblastic somites of the Chsetopods, and most probably the segmentation of the mesoblast in the two groups is a phenomenon of the same nature ; but the difference in origin between the two types of mesoblastic somites is so striking, and the development of the muscular system from them is so dissimilar in the two groups, as to render a direct descent of the Chordata from the Chsetopoda very improbable. The ventral parts of the original outgrowth give rise to the permanent body cavity, which appears originally to have been divided into two parts by a dorsal and a ventral mesentery.

The notochord. The most characteristic organ of the Chordata is without doubt the notochord. The ontogenetic development of this organ probably indicates that it arose as a differentiation of the dorsal wall of the archenteron ; at the same time it is not perhaps safe to lay too much stress upon its mode of development. Embryological and anatomical evidence demonstrate, however, in the clearest manner that the early Chordata were provided with this organ as their sole axial skeleton ;

1 Vide the chapter on the Germinal Layers.


326 GILL-CLEFTS.


and no invertebrate group can fairly be regarded as genetically related to the Chordata till it can be shewn to possess some organ either derived from a notochord, or capable of having become developed into a notochord. No such organ has as yet been recognized in any invertebrate group 1 .

Gill-clefts. The gill-clefts, which are essentially pouches of the throat opening externally, constitute extremely characteristic organs of the Chordata, and have always been taken into consideration in any comparison between the Chordata and the Invertebrata.

Amongst the Invertebrata organs of undoubtedly the same nature are, so far as I know, only found in Balanoglossus, where they were discovered by Kowalevsky. The resemblance in this case is very striking ; but although it is quite possible that the gill-clefts in Balanoglossus are genetically connected with those of the Chordata, yet the organization of Balanoglossus is as a whole so different from that of the Chordata that no comparison can be instituted between the two groups in the present state of our knowledge.

Other organs of the Invertebrata have some resemblance to the gill-clefts. The lateral pits of the Nemertines, which appear to grow out as a pair of oesophageal diverticula, which are eventually placed in communication with the exterior by a pair of ciliated canals (vide Vol. II. pp. 200 and 202), are such organs.

Semper (No. 256) has made the interesting discovery that in the budding of Nais and Chaetogaster two lateral masses of cells, in each of which a lumen may be formed, unite with the oral invagination and primitive alimentary canal to form the permanent cephalic gut. The lateral masses of cells are regarded by him as branchial passages homologous in some way with those in the Chordata. The somewhat scanty observations on this subject which he has recorded do not appear to me to lend much support to this interpretation.

It is probable that the part of the alimentary tract in which gill- clefts are present was originally a simple unperforated tube provided with highly vascular walls ; and that respiration was carried on in it by the alternate introduction and expulsion of sea water. A more or less similar mode of respiration has been recently shewn by Eisig 2 to take place in the fore part

1 In the Chaetopods various organs have been interpreted as rudiments of a notochord, but none of these interpretations will bear examination.

2 " Ueb. d. Vorkommen eines schwimmblasenahnlichen Organs bei Anneliden." Mittheil. a. d. zoo!. Station zu Neapel, Vol. n. 1881.



ON THE ANCESTRAL FORM OF THE CHORDATA. 327

of the alimentary tract of many Chastopods. This part of the alimentary tract was probably provided with paired cascal pouches with their blind ends in contiguity with the skin.

Perforations placing these pouches in communication with the exterior must be supposed to have been formed ; and the existence of openings into the alimentary tract at the end of the tentacles of many Actinias and of the hepatic diverticula of some nudibranchiate Molluscs (Eolis, &C. 1 ) shews that such perforations may easily be made. On the formation of such perforations the water taken in at the mouth would pass out by them ; and the respiration would be localized in the walls of the pouches leading to them, and thus the typical mode of respiration of the Chordata would be established.

Phylogeny of the Chordata. It may be convenient to shew in a definite way the bearing of the above speculations on the phylogeny of the Chordata. For this purpose, I have drawn up the subjoined table, which exhibits what I believe to be the relationships of the existing groups of the Chordata. Such a table cannot of course be constructed from embryological data alone, and it does not fall within the scope of this work to defend its parts in detail.

MAMMALIA SAUROPSIDA

L- T J

. PROTO-AMNIOTA AMPHIBIA


TELEOSTEI PROTO-PENTADACTYLOIDEI

I


GANOIDEI


-DIPNOI


PROTO-GANOIDEI

HOLOCEPHALI -ELASMOBRANCHII


PROTO-GNATHOSTOMATA


Cyclostomata PROTO-VERTEBRATA

Cephafochorda PROTOCHORDATA Uroc/iorda

In the above table the names printed in large capitals are hypothetical groups. The other groups are all in existence at the present day, hut those printed in Italics are probably degenerate.

The ancestral forms of the Chordata, which may be called the Protochordata, must be supposed to have had (i) a

1 The openings of the hepatic diverticula through the sacks lined with thread cells are described by Hancock and Embleton, Ann. and Mag. of Nat. History, Vol. xv. 1845, p. 82. Von Jhering has also recently described these openings (Zool. Anzeiger, No. 23) and apparently attributes their discovery to himself.


328 PHYLOGENY OF THE CHORDATA.

notochord as their sole axial skeleton, (2) a ventral mouth, surrounded by suctorial structures, and (3) very numerous gill-slits. Two degenerate offshoots of this stock still persist in Amphioxus (Cephalochorda), and the Ascidians (Urochorda).

The direct descendants of the ancestral Chordata, were probably a group which may be called the Proto-vertebrata, of which there is no persisting representative. In this group, imperfect neural arches were probably present ; and a ventral suctorial mouth without a mandible and maxillae was still persistent. The branchial clefts had, however, become reduced in number, and were provided with gill-folds ; and a secondary head (vide p. 313), with brain and organs of sense like those of the higher Vertebrata, had become formed.

The Cyclostomata are probably a degenerate offshoot of this group.

With the development of the branchial bars, and the conversion of the mandibular bar into the skeleton of the jaws, we come to the Proto-gnathostomata. The nearest living representatives of this group are the Elasmobranchii, which still retain in the adult state the ventrally placed mouth. Owing to the development of food-yolk in the Elasmobranch ovum the early stages of development are to some extent abbreviated, and almost all trace of a stage with a suctorial mouth has become lost.

We next come to an hypothetical group which we may call the Proto-ganoidei. Bridge, in his memoir on Polyodon 1 , which contains some very interesting speculations on the affinities of the Ganoids, has called this group the Pneumatoccela, from the fact that we find for the first time a full development of the air-bladder, though it is possible that a rudiment of this organ, in the form of a pouch opening on the dorsal side of the stomachic extremity of the oesophagus, was present in the earlier type.

Existing Ganoids are descendants of the Proto-ganoidei. Some of them at all events retain in larval life the suctorial mouth of the Proto-vertebrata ; and the mode of formation of their germinal layers, resembling as it does that in the Lamprey

1 Phil. Trans. 1878. Part II.


ON THE ANCESTRAL FORM OF THE CHORDATA. 329

and the Amphibia, probably indicates that they are not descended from forms with a large food-yolk like that of Elasmobranchii, and that the latter group is therefore a lateral offshoot from the main line of descent.

Of the two groups into which the Ganoidei may be divided it is clear that certain members of the one (Teleostoidei), viz. Lepidosteus and Amia, shew approximations to the Teleostei, which no doubt originated from the Ganoids ; while the other (Selachoidei or Sturiones) is more nearly related to the Dipnoi. Polypterus has also marked affinities in this direction, e.g. the external gills of the larva (vide p. 1 18).

The Teleostei, which have in common a meroblastic segmentation, had probably a Ganoid ancestor, the ova of which were provided with a large amount of food-yolk. In most existing Teleostei, the ovum has become again reduced in size, but the meroblastic segmentation has been preserved. It is quite possible that Amia may also be a descendant of the Ganoid ancestor of the Teleostei ; but Lepidosteus, as shewn by its complete segmentation, is clearly not so.

The Dipnoi as well as all the higher Vertebrata are descendants of the Proto-ganoidei.

The character of the limbs of higher Vertebrata indicates that there was an ancestral group, which may be called the Proto-pentadactyloidei, in which the pentadactyle limb became established ; and that to this group the common ancestor of the Amphibia and Amniota belonged.

It is possible that the Plesiosauri and Ichthyosauri of Mesozoic times may have been more nearly related to this group than either to the Amniota or the Amphibia. The Proto-pentadactyloidei were probably much more closely related to the Amphibia than to the Amniota. They certainly must have been capable of living in water as well as on land, and had of course persistent branchial clefts. It is also fairly certain that they were not provided with large-yolked ova, otherwise the mode of formation of the layers in Amphibia could not be easily explained.

The Mammalia and Sauropsida are probably independent offshoots from a common stem which may be called the Protoamniota.


330 BIBLIOGRAPHY.


BIBLIOGRAPHY.

(249) F. M. Balfour. A Monograph on the development of Elasmobranch Fishes, London, 1878.

(250) A. Dohrn. Der (Jrsprung d. Wirbelthiere und d. Princip. d. Functionswechsel. Leipzig, 1875.

(251) E. Haeckel. Sch'dpfungsgeschichte. Leipzig. Vide also Translation. The History of Creation. King and Co. , London. 1876.

(252) E. Haeckel. Anthropogenie. Leipzig. Vide also Translation. Anthropogeny. Kegan Paul and Co., London, 1878.

(253) A. Kowalevsky. " Entwicklungsgeschichte d. Amphioxus lanceolatus." Mem. Acad. d. Scien. St Petersbourg, Ser. VII. Tom. XI. 1867, and Archivf. mikr. Anat., Vol. xin. 1877.

(254) A. Kowalevsky. "Weitere Stud. lib. d. Entwick. d. einfachen Ascidien." Archivf. mikr. Anat., Vol. VII. 1871.

(255) C. Semper. "Die Stammesverwandschaft d. Wirbelthiere u. Wirbellosen." Arbeit, a. d. zool.-zoot. Instit. Wurzburg, Vol. II. 1875.

(256) C. Semper. "Die Verwandschaftbeziehungen d. gegliederten Thiere." Arbeit, a. d. zool.-zoot. Instit. Wurzburg, Vol. III. 1876 1877.


CHAPTER XIII.


GENERAL CONCLUSIONS.


I. THE MODE OF ORIGIN AND HOMOLOGIES OF THE GERMINAL LAYERS.

IT has already been shewn in the earlier chapters of the work that during the first phases of development the history of all the Metazoa is the same. They all originate from the coalescence of two cells, the ovum and spermatozoon. The coalesced product of these cells the fertilized ovum then undergoes a process known as the segmentation, in the course of which it becomes divided in typical cases into a number of uniform cells. An attempt was made from the point of view of evolution to explain these processes. The ovum and spermatozoon were regarded as representing phylogenetically two physiologically differentiated forms of a Protozoon ; their coalescence was equivalent to conjugation : the subsequent segmentation of the fertilized ovum was the multiplication by division of the organism resulting from the conjugation ; the resulting organisms, remaining, however, united to form a fresh organism in a higher state of aggregation.

In the systematic section of this work the embryological history of the Metazoa has been treated. The present chapter contains a review of the cardinal features of the various histories, together with an attempt to determine how far there are any points common to the whole of these histories ; and the phylogenetic interpretation to be given to such points.

Some years ago it appeared probable that a definite answer


332 INVAGINATION.


would be given to the questions which must necessarily be raised in the present chapter ; but the results of the extended investigations made during the last few years have shewn that these expectations were premature, and in spite of the numerous recent valuable contributions to this branch of Embryology, amongst which special attention may be called to those of Kowalevsky (No. 277), Lankester (Nos. 278 and 279), and Haeckel (No. 266), there are few embryologists who would venture to assert that any answers which can be given are more than tentative gropings towards the truth.

In the following pages I aim more at summarising the facts, and critically examining the different theories which can be held, than at dogmatically supporting any definite views of my own.

In all the Metazoa, the development of which has been investigated, the first process of differentiation, which follows upon the segmentation, consists in the cells of the organism becoming divided into two groups or layers, known respectively as epiblast and hypoblast.

These two layers were first discovered in the young embryos of vertebrated animals by Pander and Von Baer, and have been since known as the germinal layers, though their cellular nature was not at first recognised. They were shewn, together with a third layer, or mesoblast, which subsequently appears between them, to bear throughout the Vertebrata constant relations to the organs which became developed from them. A very great step was subsequently made by Remak (No. 287), who successfully worked out the problem of vertebrate embryology on the cellular theory.

Rathke in his memoir on the development of Astacus (No. 286) attempted at a very early period to extend the doctrine of the derivation of the organs from the germinal layers to the Invertebrata. In 1859 Huxley made an important step towards the explanation of the nature of these layers by comparing them with the ectoderm and endoderm of the Hydrozoa ; while the brilliant researches of Kowalevsky on the development of a great variety of invertebrate forms formed the starting point of the current views on this subject.

The differentiation of the epiblast and hypoblast may commence during the later phases of the segmentation, but is generally not completed till after its termination. Not only do the cells of the blastoderm become differentiated


ORIGIN OF THE GERMINAL LAYERS.


333


into two layers, but these very large number of


two layers, in the case of a ova with but little food-yolk, con


(fig. 198) the require further



FIG. 198. DIAGRAM OF A GASTRULA.

(From Gegenbaur.)

a. mouth ; b. archenteron ; c. hypoblast ; d. epiblast.


stitute a double-walled sack the gastrula characters of which are too well known to description. Following the lines of phylogenetic speculation above indicated, it may be concluded that the two-layered condition of the organism represents in a general way the passage from the protozoon to the metazoon condition. It is probable that we may safely go further, and assert that the gastrula reproduces, with more or less fidelity, a stage in the evolution of the Metazoa, permanent in the simpler Hydrozoa, during which the organism was provided with (i) a fully developed digestive cavity (fig. 198 b) lined by the hypoblast with digestive and assimilative functions, (2) an oral opening (a), and (3) a superficial epiblast (d}. These generalisations, which are now widely accepted, are no doubt very valuable, but they leave unanswered the following important questions :

(1) By what steps did the compound Protozoon become differentiated into a Metazoon ?

(2) Are there any grounds for thinking that there is more than one line along which the Metazoa have become independently evolved from the Protozoa ?

(3) To what extent is there a complete homology between the two primary germinal layers throughout the Metazoa ?

Ontogenetically there is a great variety of processes by which the passage from the segmented ovum to the two-layered or diploblastic condition is arrived at.

These processes may be grouped under the following heads : 1. Invagination. Under this term a considerable number of closely connected processes are included. When the segmentation results in the formation of a blastosphere, one half of the blastosphere may be pushed in towards the opposite half, and a gastrula be thus produced (fig. 199, A and B). This process is known as embolic invagination. Another process, known as epibolic invagination, consists in epiblast cells growing round and en


334


INVAGINATION.


closing the hypoblast (fig. 200). This process replaces the former process when the hypoblast cells are so bulky from being distended by food-yolk that their invagination is mechanically impossible.



FlG. 199. TWO STAGES IN THE DEVELOPMENT OF HOLOTHURIA TUBULOSA,

VIEWED IN OPTICAL SECTION. (After Selenka.) A. Stage at the close of segmentation. B. Gastrula stage.

mr. micropyle ; fl. chorion ; s.c. segmentation cavity; bl. blastoderm; ep. epiblast; hy. hypoblast ; ms. amoeboid cells derived from hypoblast ; a.e. archenteron.

There are various peculiar modifications of invagination which cannot be dealt with in detail.

Invagination in one form or other occurs in some or all the members of the following groups :

The Dicyemidae, Calcispongiae (after the amphiblastula stage) and Silicispongiae, Coelenterata, Turbellaria, Nemertea, Rotifera, Mollusca, Polyzoa, Brachiopoda, Chaetopoda, Discophora, Gephyrea, Chaetognatha, Nematelminthes, Crustacea, Echinodermata, and Chordata.

The gastrula of the Crustacea is peculiar, as is also that of many of the Chordata (Reptilia, Aves, Mammalia), but there is every reason to suppose



FIG. 200. TRANSVERSE SECTION THROUGH THE OVUM OF EUAXES DURING AN EARLY STAGE OF DEVELOPMENT, TO SHEW THE NATURE OF EPiiiOLic INVAGINATION. (After Kowalevsky. )

ep. epiblast ; ms. mesoblastic band ; hy. hypoblast.


ORIGIN OF THE GERMINAL LAYERS.


335


that the gastrulae of these groups are simply modifications of the normal type.

2. Delamination. Three types of delamination may be distinguished :

a. Delamination where the cells of a solid morula become divided into a superficial epiblast, and a central solid mass in which the digestive cavity is subsequently hollowed out (fig. 201).



FlG. 201. TWO STAGES IN THE DEVELOPMENT OF STEPHANOMIA PICTUM, TO ILLUSTRATE THE FORMATION OF THE LAYERS BY DELAMINATION. (After

Metschnikoff.)

A. Stage after the delamination; ep. epiblastic invagination to form pneumatocyst.

B. Later stage after the formation of the gastric cavity in the solid hypoblast. po. polypite ; /. tentacle ; pp. pneumatocyst ; ep. epiblast of pneumatocyst ; hy. hypoblast surrounding pneumatocyst.

b. Delamination where the segmented ovum has the form of a blastosphere, the cells of which give rise by budding to scattered cells in the interior of the vesicle, which, though they may at first form a solid mass, finally arrange themselves in the form of a definite layer around a central digestive cavity (fig. 202).

c. Delamination where the segmented ovum has the form of a blastosphere in the cells of which the protoplasm is differentiated into an inner and an outer part. By a subsequent


336


DELAMINATION.


process the inner parts of the cells become separated from the outer, and the walls of the blastosphere are so divided into two distinct layers (fig. 205).

Although the third of these processes is usually regarded as the type of delamination, it does not, so far as I know, occur in nature, but is most nearly approached in Geryonia (fig. 203).

The first type of delamination is found in the Ceratospongiae, some Silicispongiae (?), and in many Hydrozoa and Actinozoa, and in Nemertea and Nematelminthes (Gordioidea ?). The second type occurs in many Porifera \Calcispongi(e (A see t fa), Myxospongice], and in some Coelenterata, and Brachiopoda ( Thecidium).

Delamination and invagination are undoubtedly the two most frequent modes in which the layers are differentiated, but

C



FIG. 202. THREE LARVAL STAGES OF EUCOPE POLYSTYLA. (After Kowalevsky.) A. Blastosphere stage with hypoblast spheres becoming budded off into central cavity. B. Planula stage with solid hypoblast. C. Planula stage with a gastric cavity, ep. epiblast ; hy. hypoblast ; al. gastric cavity.

there are in addition several others. In the first place the whole of the Tracheata (with the apparent exception of the Scorpion) develop, so far as is known, on a plan peculiar to them, which approaches delamination. This consists in the appearance of a superficial layer of cells enclosing a central yolk mass, which corresponds to the hypoblast (figs. 204 and 214). This mode of development might be classed under delamination, were it not for the fact that the early development


ORIGIN OF THE GERMINAL LAYERS.


337


of many Crustacea is almost the same, but is subsequently followed by an invagination (fig. 208), which apparently corre



FIG. 203. DIAGRAMMATIC FIGURES SHEWING THE DELAMINATION OF THE

EMBRYO OF GERYONIA. (After Fol.)

A. Stage at the commencement of the delamination ; the dotted lines x shew

the course of the next planes of division. B. Stage at the close of the delamination.

cs. segmentation cavity ; a. endoplasm ; b. ectoplasm ; ep. epiblast ; hy. hypoblast.

spends to the normal invagination of other types. There are strong grounds for thinking that the tracheate type of forma


FIG. 204. SEGMENTATION AND FORMATION OF THE BLASTODERM IN CHELIFER.

(After Metschnikoff. )

In A the ovum is divided into a number of separate segments. In B a number of small cells have appeared (bl) which form a blastoderm enveloping the large yolkspheres. In C the blastoderm has become divided into two layers.

B. III. 22


338 ORIGIN OF THE GASTRULA.

tion of the epiblast and hypoblast is a secondary modification of an invaginate type (vide Vol. II. p. 457).

The type of some Turbellaria (Stylochopsis ponticus) and that of Nephelis amongst the Discophora is not capable of being reduced to the invaginate type.

The development of almost all the parasitic groups, i.e. the Trematoda, the Cestoda, the Acanthocephala, and the Linguatulida, and also of the Tardigrada, Pycnogonida, and other minor groups, is too imperfectly known to be classed with either the delaminate or invaginate types.

It will, I think, be conceded on all sides that, if any of the ontogenetic processes by which a gastrula form is reached are repetitions of the process by which a simple two-layered gastrula was actually evolved from a compound Protozoon, these processes are most probably of the nature either of invagination or of delamination.

The much disputed questions which have been raised about the gastrula and planula theories, originally put forward by Haeckel and Lankester, resolve themselves then into the simple question, whether any, and if so which, of the ontogenetic processes by which the gastrula is formed are repetitions of the phylogenetic origin of the gastrula.

It is very difficult to bring forward arguments of a conclusive kind in favour of either of these processes. The fact that delaminate and invaginate gastrulse are in several instances found coexisting in the same group renders it certain that there are not two independent phyla 'of the Metazoa, derived respectively from an invaginate and a delaminate gastrula 1 .

1 It is not difficult to picture a possible derivation of delamination from invagination ; while a comparison of the formation of the inner layers (mesoblast and hypoblast) in Ascetta (amongst the Sponges), and in the Echinodermata, shews a very simple way in which it is possible to conceive of a passage of delamination into invagination. In Ascetta the cells, which give rise to the mesoblast and hypoblast, are budded off from the inner wall of the blastosphere, especially at one point ; while in Echinodermata (fig. 199) there is a small invaginated sack which gives rise to the hypoblast, while from the walls of this sack amoeboid cells are budded off which give rise to a large part of the mesoblast. If we suppose the hypoblast cells budded off at one point in Ascetta gradually to form an invaginated sack, while the mesoblast cells continued to be budded off as before, we should pass from the delaminate type of tta t<> the invaginate type of an Echinoderm.


ORIGIN OF THE GERMINAL LAYERS. 339

The four most important cases in which the two processes coexist are the Porifera, the Coelenterata, the Nemertea, and the Brachiopoda. In the cases of the Porifera and Ccelenterata, there do not appear to me to be any means of deciding which of these processes is derived from the other ; but in the Nemertea and the Brachiopoda the case is different. In all the types of Nemertea in which the development is relatively not abbreviated there is an invaginate gastrula, while in the types with a greatly abbreviated development there is a delaminate gastrula. It would seem to follow from this that a delaminate gastrula has here been a secondary result of an abbreviation in the development. In the Brachiopoda, again, the majority of types develop by a process of invagination, while Thecidium appears to develop by delamination ; here also the delaminate type would appear to be secondarily derived from the invaginate.

If these considerations are justified, delamination must be in some instances secondarily derived from invagination ; and this fact is so far an argument in favour of the more primitive nature of invagination ; though it by no means follows that in the invaginate process the steps by which the Metazoa were derived from the Protozoa are preserved.

It does not, therefore, seem possible to decide conclusively in favour of either of these processes by a comparison of the cases where they occur in the same groups.

The relative frequency of the two processes supplies us with another possible means for deciding between them ; and there is no doubt that here again the scale inclines towards invagination. It must, however, be borne in mind that the frequency of the process of invagination admits of another possible explanation. There is a continual tendency for the processes of development to be abbreviated and simplified, and it is quite possible that the frequent occurrence of invagination is due to the fact of its being, in most cases, the simplest means by which the twolayered condition can be reached. But this argument can have but little weight until it can be shewn in each case that invagination is a simpler process than delamination ; and it is rendered improbable by the cases already mentioned in which delamination has been secondarily derived from invagination.

If it were the case that the blastopore had ih all types the

22 2


340


BLASTOPORE.


same relation to the adult mouth, there would be strong grounds for regarding the invaginate gastrula as an ancestral form ; but the fact that this is by no means so is an argument of great weight in favour of some other explanation of the frequency of invagination.

The force of this consideration can best be displayed by a short summary of the fate of the blastopore in different forms.

The fate of the blastopore is so variable that it is difficult even to classify the cases which have been described.

(1) It becomes the permanent mouth in the following forms 1 : Ccelenterata. Pelagia, Cereanthus.

Turbellaria. Leptoplana (?), Thysanozoon.

Nemertea. Pilidium, larvae of the type of Desor.

Mollusca. In numerous examples of most Molluscan groups, except the

Cephalopoda.

Chcetopoda. Most Oligochaeta, and probably many Polychseta. Gephyrea. Phascolosoma, Phoronis. Nematelminthes. Cucullanus.

(2) It closes in the position where the mouth is subsequently formed. Ccelenterata. Ctenophora (?).

Mollusca. In numerous examples of most Molluscan groups, except the

Cephalopoda. Crustacea. Cirripedia (?), some Cladocera (Moina) (?).

(3) It becomes the permanent anus. Mollusca. Paludina.

Chatopoda. Serpula and some other types. Echinodermata.Mmosl universally, except amongst the Crinoidea.

(4) It closes in the position where the anus is subsequently formed. Echinodermata. Crinoidea.

(5) It closes in a position which does not correspond or is not known to correspond 2 either with the future mouth or anus. Porifera Sycandra. Ccelenterata Chrysaora*, Aurelia*. Nemertea* Some larvae which develop without a metamorphosis. Rolifera*. Mollusca Cephalopoda. Polyzoa*. Brachiopoda Argiope, Terebratula, Terebratulina. Ch(Etopoda Euaxes. Discophora Clepsine. Gephyrea Bonellia*. Chatognatha. Crustacea Decapoda. Chordata.

The forms which have been classed together under the last heading vary considerably in the character of the blastopore. In some cases the fact of its not coinciding either with the mouth

1 The above list is somewhat tentative ; and future investigations will probably shew that many of the statements at present current about the position of the blastopore are inaccurate.

2 The forms in which the position of the blastopore in relation to the mouth or anus is not known <ire marked with an asterisk.


ORIGIN OF THE GERMINAL LAYERS. 341

or anus appears to be due simply to the presence of a large amount of food-yolk. The cases of the Cephalopoda, of Euaxes, and perhaps of Clepsine and Bonellia, are to be explained in this way : in the case of all these forms, except Bonellia, the blastopore has the form of an elongated slit along the ventral surface. This type of blastopore is characteristic of the Mollusca generally, of the Polyzoa, of the Nematelminthes, and very possibly of the Chaetopoda and Discophora. In the Chaetognatha (fig. 209 B) the blastopore is situated, so far as can be determined, behind the future anus. In many Decapoda the blastopore is placed behind, but not far from, the anus. In the Chordata it is also placed posteriorly to the anus, and, remarkably enough, remains, in a large number of forms, for some time in connection with the neural tube by a neurenteric canal.

The great variations in the character of the gastrula, indicated in the above summary, go far to shew that if the gastrulae, as we find them in most types, have any ancestral characters, these characters can only be of the most general kind. This may best be shewn by the consideration of a few striking instances. The blastopore in Mollusca has an elongated slit-like form, extending along the ventral surface from the mouth to the anus. In Echinodermata it is a narrow pore, remaining as the anus. In most Chsetopoda it is a pore remaining as the mouth, but in some as the anus. In Chordata it is a posteriorlyplaced pore, opening into both the archenteron and the neural canal.

It is clearly out of the question to explain all these differences as having connection with the characters of ancestral forms. Many of them can only be accounted for as secondary adaptations for the convenience of development.

The epibolic gastrula of Mammalia (vide pp. 215 and 291) is a still more striking case of a secondary embryonic process, and is not directly derived from the gastrula of the lower Chordata. It probably originated in connection with the loss of food-yolk which took place on the establishment of a placental nutrition for the foetus. The epibolic gastrula of the Scorpion, of Isopods, and of other Arthropoda, seems also to be a derived gastrula. These instances of secondary gastrulse are very probably by no


342 BLASTOPORE.


means isolated, and should serve as a warning against laying too much stress upon the frequency of the occurrence of invagination. The great influence of the food-yolk upon the early development might be illustrated by numerous examples, especially amongst the Chordata (vide Chapter XL).

If the descendants of a form with a large amount of food-yolk in its ova were to produce ova with but little food-yolk, the type of formation of the germinal layers which would thereby result would be by no means the same as that of the ancestors of the forms with much food-yolk, but would probably be something very different, as in the case of Mammalia. Yet amongst the countless generations of ancestors of most existing forms, such oscillations in the amount of the food-yolk must have occurred in a large number of instances.

The whole of the above considerations point towards the view that the formation of the hypoblast by invagination, as it occurs in most forms at the present day, can have in many instances no special phylogenetic significance, and that the argument from frequency, in favour of invagination as opposed to delamination, is not of prime importance.

A third possible method of deciding between delamination and invagination is to be found in the consideration as to which of these processes occurs in the most primitive forms. If there were any agreement amongst primitive forms as to the type of their development this argument might have some weight. On the whole, delamination is, no doubt, characteristic of many primitive types, but the not infrequent occurrence of invagination in both the Ccelenterata and the Porifera the two groups which would on all hands be admitted to be amongst the most primitive deprives this argument of much of the value it might otherwise have.

To sum up considering the almost indisputable fact that both the processes above dealt with have in many instances had a purely secondary origin, no valid arguments can be produced to shew that either of them reproduces the mode of passage between the Protozoa and the ancestral two-layered Metazoa. These conclusions do not, however, throw any doubt upon the fact that the gastrula, however evolved, was a primitive form of the Metazoa ; since this conclusion is founded upon the actual




ORIGIN OF TIIH GERMINAL LAYERS.


343


existence of adult gastrula forms independently of their occurrence in development.

Though embryology does not at present furnish us with a definite answer to the question how the Metazoa became developed from the Protozoa, it is nevertheless worth while reviewing some of the processes by which this can be conceived to have occurred.

On purely a priori grounds there is in my opinion more to be said for invagination than for any other view.

On this view we may suppose that the colony of Protozoa in the course of conversion into Metazoa had the form of a blastosphere ; and that at one pole of this a depression appeared. The cells lining this depression we



F


FIG. 205. DIAGRAM SHEWING THE FORMATION OF A GASTRULA IJY DELAMINATION. (From Lankester.)

Fig. i, ovum; fig. 2, stage in segmentation; fig. 3, commencement of delamination after the appearance of a central cavity ; fig. 4, delamination completed, mouth forming at M. In figs, i, 2, and 3, EC, is ectoplasm, and En. is endoplasm. In fig. 4, EC. is epiblast, and En. hypoblast. E. and F. food particles.

may suppose to have been amoeboid, and to have carried on the work of digestion ; while the remaining cells were probably ciliated. The digestion may be supposed to have been at first carried on in the interior of the cells, as in the Protozoa; but, as the depression became deeper (in order to increase the area of nutritive cells and to retain the food) a digestive secretion probably became poured out from the cells lining it, and the mode of digestion generally characteristic of the Metazoa was thereby inaugurated. It may be noted that an intracellular protozoon type of digestion persists in the Porifera, and appears also to occur in many Ccelenterata, Turbellaria,


344 PASSAGE FROM THE PROTOZOA TO THE METAZOA.

&c., though in most of these cases both kinds of digestion probably go on simultaneously 1 .

Another hypothetical mode of passage, which fits in with delamination, has been put forward by Lankester, and is illustrated by fig. 205. He supposes that at the blastosphere stage the fluid in the centre of the colony acquired special digestive properties ; the inner ends of the cells having at this stage somewhat different properties from the outer, and the food being still incepted by the surface of the cells (fig. 205, 3). In a later stage of the process the inner portions of the cells became separated off as the hypoblast ; while the food, though still ingested in the form of solid particles by the superficial cells, was carried through the protoplasm into the central digestive cavity. Later (fig. 205, 4), the point where the food entered became localised, and eventually a mouth became formed at this point.

The main objection which can be raised against Lankester's view is that it presupposes a type of delamination which does not occur in nature except in Geryonia.

Metschnikoff has propounded a third view with reference to delamination. He starts as before with a ciliated blastosphere. He next supposes the cells from the walls of this to become budded off into the central cavity, as in Eucope (fig. 202), and to lose their cilia. These cells give rise to an internal parenchyma, which carries on an intracellular digestion. At a later stage a central digestive cavity is supposed to be formed. This view of the passage from the protozoon to the metazoon state, though to my mind improbable in itself, fits in very well with the ontogeny of the lower Hydrozoa.

Another view has been put forward by myself in the chapter on the Porifera*, to the effect that the amphiblastula larva of Calcispongias may be a transitional form between the Protozoa and the Metazoa, composed of a hemisphere of nutritive amoeboid cells, and a hemisphere of ciliated cells. The absence of such a larval form in the Ccelenterata and higher Metazoa is opposed, however, to this larva being regarded as a transitional form, except for the Porifera.

It is obvious that so long as there is complete uncertainty as to the value to be attached to the early developmental processes, it is not possible to decide from these processes whether there is only a single metazoon phylum or whether there may not be two or more such phyla. At the same time there appear to be strong

1 J. Parker, "On the Histology of Hydra fusca," Quart. Journ. Micr. Science, vol. xx. 1880; and El. Metschnikoff, " Ueb. die intracellulare Verdauung bei Ccelenteraten," Zoologischer Anzeiger, No. 56, vol. in. 1880 and Lankester, " On the intracellular digestion and endoderm of Limnocodium, " Quart. Journ. Micr. Science, vol. xxi. 1881.

! Vol. n. p. 149.


ORIGIN OF THE GERMINAL LAYERS. 345

arguments for regarding the Porifera as a phylum of the Metazoa derived independently from the Protozoa. This seems to me to be shewn (i) by the striking larval peculiarities of the Porifera ; (2) by the early development of the mesoblast in the Porifera, which stands in strong contrast to the absence of this layer in the embryos of most Ccelenterata ; and above all, (3) by the remarkable characters of the system of digestive channels. A further argument in the same direction is supplied by the fact that the germinal layers of the Sponges very probably do not correspond physiologically to the germinal layers of other types. The embryological evidence is insufficient to decide whether the amphiblastula larva is, as suggested above, to be regarded as the larval ancestor of the Porifera.

Homologies of the germinal layers. The question as to how far there is a complete homology between the two primary germinal layers throughout the Metazoa was the third of the questions proposed to be discussed here.

Since there are some Metazoa with only two germinal layers, and other Metazoa with three, and since, as is shewn in the following section, the third layer or mesoblast can only be regarded as a derivative of one or both the primary layers, it is clear that a complete homology between the two primary germinal layers does not exist.

That there is a general homology appears on the other hand hardly open to doubt.

The primary layers are usually continuous with each other, near one or both (when both are present) the openings of the alimentary tract.

As a rule an oral and anal section of the alimentary tract the stomodaeum and proctodaeum are derived from the epiblast ; but the limits of both these sections are so variable, sometimes even in closely allied forms, that it is difficult to avoid the conclusion that there is a border-land between the epiblast and hypoblast, which appears by its development to belong in some forms to the epiblast and in other forms to the hypoblast. If this is not the case it is necessary to admit that there are instances in which a very large portion of the alimentary canal is phylogenetically an epiblastic structure. In some of the Isopods, for example, the stomodaeum and proctodaeum give


346 ORIGIN OF THE MESOBLAST.

rise to almost the whole of the alimentary canal with its appendages, except the liver.

The origin of the Mesoblast. A diploblastic condition of the organism preceded, as we have seen, the triploblastic. The epiblast during the diploblastic condition was, as appears from such forms as Hydra, especially the sensory and protective layer, while the hypoblast was the secretory and assimilating layer; both layers giving rise to muscular elements. It must not, however, be supposed that in the early diploblastic ancestors there was a complete differentiation of function, but there is reason to think that both the primary layers retained an indefinite capacity for developing into any form of tissue 1 . The fact of the triploblastic condition being later than the diploblastic proves in a conclusive way that the mesoblast is a derivative of one or both the primary layers. In the Ccelenterata we can study the actual origin from the two primary layers of various forms of tissue which in the higher types are derived from the mesoblast 2 . This fact, as well as general a priori considerations, conclusively prove that the mesoblast did not at first originate as a mass of independent cells between the two primary layers, but that in the first instance it gradually arose as differentiations of the two layers, and that its condition in the embryo as an independent layer of undifferentiated cells is a secondary condition, brought about by the general tendency

1 The Hertwigs (No. 270) have for instance shewn that nervous structures are developed in the hypoblast in the Actinozoa and other Coelenterata.

2 There is considerable confusion in the use of the names for the embryonic layers. In some cases various tissues formed by differentiations of the primary layers have been called mesoblast. Schultze, and more recently the Hertwigs, have pointed out the inconvenience of this nomenclature. In the case of the Coelenterata it is difficult to decide in certain instances (e.g. Sympodium) whether the cells which give rise to a particular tissue of the adult are to be regarded as forming a mesoblast, i.e. a middle undifferentiated layer of cells, or whether they arise as already histologically differentiated elements from one of the primary layers. The attempt to distinguish by a special nomenclature the epiblast and hypoblast after and before the separation of the mesoblast, which has been made by Allen Thomson (No. 1), appears incapable of being consistently applied, though it is convenient to distinguish a primary and a secondary hypoblast. A proposal of the Hertwigs to adopt special names for the outer and inner limiting membranes of the adult, and for the interposed mass of organs, appears to me unnecessary.


ORIGIN OF THE GERMINAL LAYERS. 347

towards a simplification of development, and a retardation of histological differentiation 1 .

The Hertwigs have recently attempted (No. 271) to distinguish two types of differentiation of the mesoblast, viz. (i) a direct differentiation from the primitive epithelial cells ; (2) a differentiation from primitively indifferent cells budded off into the gelatinous matter between the two primary layers.

It is quite possible that this distinction may be well founded, but no conclusive evidence of the occurrence of the second process has yet been adduced. The Ctenophora are the type upon which special stress is laid, but the early passage of amoeboid cells into the gelatinous tissue, which subsequently become muscular, is very probably an embryonic abbreviation ; and it is quite possible that these cells may phylogenetically have originated from epithelial cells provided with contractile processes passing through the gelatinous tissue.

The conversion of non-embryonic connective-tissue cells into muscle cells in the higher types has been described, but very much more evidence is required before it can be accepted as a common occurrence.

In addition to the probably degraded Dicyemida:: and Orthonectidae, the Ccelenterata are the only group in which a true mesoblast is not always present. In other words, the Ccelenterata are the only group in which there is not found in the embryo an undifferentiated group of cells from which the majority of the organs situated between the epidermis and the alimentary epithelium are developed.

The organs invariably derived, in the triploblastic forms, from the mesoblast, are the vascular and lymphatic systems, the muscular system, and the greater part of the connective tissue and the excretory and generative (?) systems. On the other hand, the nervous systems (with a few possible exceptions) and organs of sense, the epithelium of most glands, and a few exceptional connective-tissue organs, as for example the notochord, are developed from the two primary layers.

The fact of the first-named set of organs being invariably derived from the mesoblast points to the establishment of the two following propositions: (i) That with the differenti 1 The causes which give rise to a retardation of histological differentiation will be dealt with in the second part of this chapter which deals with larval characters and larval forms.


348 ORIGIN OF THE MESOBLAST.

ation of the mesoblast as a distinct layer by the process already explained, the two primary layers lost for the most part the capacity they primitively possessed of giving rise to muscular and connective-tissue differentiations 1 , to the epithelium of the excretory organs, and to generative cells. (2) That the mesoblast throughout the triploblastic Metazoa, in so far as these forms have sprung from a common triploblastic ancestor, is an homologous structure.

The second proposition follows from the first. The mesoblast can only have ceased to be homologous throughout the triploblastica by additions from the two primary layers, and the existence of such additions is negatived by the first proposition.

These two propositions, which hang together, are possibly only approximately true, since it is quite possible that future investigations may shew that differentiations of the two primary layers are not so rare as has been hitherto imagined.

Ranvier 2 finds that the muscles of the sweat-glands are developed from the inner part of the layer of epiblast cells, invaginated to form these glands.

Gotte 3 describes the epiblast cells of the larva of Comatula as being at a certain stage contractile and compares them with the epithelio-muscular cells of Hydra. These cells would appear subsequently to be converted into a simple cuticular structure.

It is moreover quite possible that fresh differentiations from the two primary layers may have arisen after the triploblastic condition had been established, and by the process of simplification of development and precocious segregation, as Lankester calls it, have become indistinguishable from the normal mesoblast. In spite of these exceptions it is probable that the major part of the muscular system of all existing triploblastic forms has been differentiated from the muscular system of the ancestor or ancestors (if there is more than one phylum) of the triplo 1 The connective-tissue test of the Tunicata, though derived from the epiblast, is not really an example of such a differentiation.

1 M. L. Ranvier. " Sur la stricture des glandes sudoripares." Comptes Rendus, Dec. 29, 1879.

1 A. Gotte, "Vergleich. Entwick. d. Comatula mediterranea." Archiv f. mikr. Anat. vol. XI I. p. 597.


ORIGIN OF THE GERMINAL LAYERS.


349


blastica. In the case of other tissues there are a few instances which might be regarded as examples of an organ primitively developed in one of the two primary layers having become secondarily carried into the mesoblast. The notochord has sometimes been cited as such an organ, but, as indicated in a previous chapter, it is probable that its hypoblastic origin can always be demonstrated.

A



FIG. 206. EPIBOLIC GASTRULA OF BONELLIA. (After Spengel.)

A. Stage when the four hypoblast cells are nearly enclosed.

B. Stage after the formation of the mesoblast has commenced by an infolding of the lips of the blastopore.

ep. epiblast; me. mesoblast; bl. blastopore.

The nervous system, although imbedded in mesoblastic derivates in the adults of all the higher triploblastica, retains with marvellous constancy its epiblastic origin (though it is usually separated from the epiblast prior to its histogenic differentiation) ; yet in the Cephalopoda, and some other Mollusca, the evidence is in favour of its developing in the mesoblast. Should future investigations confirm these conclusions, a good example will be afforded of an organ changing the layer from which it usually develops 1 . The explanation of such a change would be precisely the same as that already given for the mesoblast as a whole.

The actual mode of origin of various tissues, which in the true triploblastic forms arise in mesoblast, can be traced in the

1 The Hertvvigs hold that there is a distinct part of the nervous system which was at first differentiated in the mesoblast in many types, amongst others the Mollusca. The evidence in favour of this view is extremely scanty and the view itself appears to me highly improbable.


350 ORIGIN OF THE MESOBLAST.

Ccelenterata 1 . In this group the epiblast and hypoblast both give rise to muscular and connective-tissue elements ; and although the main part of the nervous system is formed in the epiblast, it seems certain that in some types nerves may be derived from the hypoblast' 2 . These facts are extremely interest


FlG. 207. TWO TRANSVERSE SECTIONS THROUGH EMBRYOS OF HYDROPHILUS

PICEUS. (After Kowalevsky.)

A. Section through an embryo at the point where the two germinal folds most approximate.

B. Section through an embryo, in the anterior region where the folds of the amnion have not united.

gg. germinal groove; me. mesoblast; am. amnion; yk. yolk.

ing, but it is by no means certain that any conclusions can be directly drawn from them as to the actual origin of the mesoblast in the triploblastic forms, till we know from what diploblastic forms the triploblastica originated. All that they shew is that any of the constituents of the mesoblast may have originated from either of the primitive layers.

1 The reader is referred for this subject to the valuable memoirs which have been recently published by the Hertwigs, especially to No. 270. He will find a general account of the subject written before the appearance of the Hertwigs' memoir in pp. 180-182 of Volume II. of this treatise.

- It would be interesting to know the history of the various nervous structures found in the walls of the alimentary tract in the higher forms. I have shewn (Development of Elasmobranch Fishes, p. 172) that the central part of the sympathetic system is derived from the epiblast. It would however be well to work over the development of Auerbach's plexus.


ORIGIN OF THE GERMINAL LAYERS.


351


For further light as to the origin of the mesoblast, it is necessary to turn to its actual development.

The following summary illustrates the more important modes in which the mesoblast originates. B



FIG. 208. FIGURES ILLUSTRATING THE DEVELOPMENT OF ASTACUS. (From Parker; after Reichenbach. )

A. Section through part of the ovum during segmentation, n. nuclei ; w.y. white yolk ; y.p. yolk pyramids ; c. central yolk mass.

B. and C. Longitudinal sections of the gastrula stage, a. archenteron ; b. blastopore; ms. mesoblast; ec. epiblast; en. hypoblast, distinguished from epiblast by shading.

D. Highly magnified view of anterior lip of blastopore, to shew the origin of the primary mesoblast from the wall of the archenteron. /. ms. primary mesoblast ; ec. epiblast ; en. hypoblast.

E. Two hypoblast cells to shew the amoeba-like absorption of yolk spheres. y. yolk ; n. nucleus ; p. pseudopodial process.

F. Hypoblast cells giving rise endogenously to the secondary mesoblast (s.tns.) ; n. nucleus.

I. It grows inwards from the lips of the blastopore as a pair of bands. In these cases it may originate (a) from cells which are clearly hypoblastic, (b} from cells which are clearly epiblastic, (c) from cells which cannot be regarded as belonging to either layer.

Mollusca. Gasteropoda, Cephalopoda, and Lamellibranchiata. In Gasteropoda and Lamellibranchiata the mesoblast sometimes originates


352


DEVELOPMENT OF THE MESOBLAST.


from a pair of cells at the lips of the blastopore, though very probably some of the elements subsequently come from the epiblast ; and in Cephalopoda it begins as a ring of cells round the edge of the blastoderm.

Polyzoa Entoprocta. It originates from a pair of cells at the lips of the blastopore.

Chaetopoda. Euaxes. It arises as a ridge of cells at the lips of the blastopore (fig. 200).

Gephyrea. Bonellia. It arises (fig. 206) as an infolding of the epiblastic lips of the blastopore.

Nematelminthes. Cucullanus. It grows backwards from the hypoblast cells at the persistent oral opening of the blastopore.

Tracheata. Insecta. It grows inwards from the lips of the germinal groove (fig. 207), which probably represent the remains of a blastopore. Part of the mesoblast is probably also derived from the yolk-cells. A similar though more modified development of the mesoblast occurs in the Araneina (fig. 214).

Crustacea. Decapoda. It partly grows in from the hypoblastic lips of the blastopore, and is partly derived from the yolk-cells (fig. 208).



FIG. tog. THREE STAGES IN THE DEVELOPMENT OF SAGITTA. (A. and C.

after Biitschli, and B. after Kowalevsky.) The three embryos are represented in the same positions.

A. Represents the gastrula stage.

B. Represents a succeeding stage, in which the primitive archenteron is commencing to be divided into three.

C. Represents a later stage, in which the mouth involution (m) has become continuous with the alimentary tract, and the blastopore has become closed.

m. mouth; al. alimentary canal; ae. archenteron; bl.p. blastopore; pv. perivisceral cavity; sp. splanchnic mesoblast; so. somatic mesoblast; ge. generative organs.

2. The mesoblast is developed from the walls of hollow outgrowths of the archenteron, the cavities of which become the body cavity.




ORIGIN OF THE GERMINAL LAYERS.


353


Brachiopoda. The walls of a pair of outgrowths form the whole of the mesoblast.

Chaetognatha. The mesoblast arises in the same manner as in the Brachiopoda (fig. 209).

Echinodermata. The lining of the peritoneal cavity is developed from the walls of outgrowths of the archenteron, but the greater part of the mesoblast is derived from the amoeboid cells budded off from the walls of the archenteron (fig. 210).



ME


Mp. Pld.

FIG. 210. LONGITUDINAL SECTION THROUGH AN EMBRYO OF CUCUMARIA DOL1OLUM AT THE -END OF THE FOURTH DAY.

Vpv. vaso-peritoneal vesicle; ME. mesenteron; Sip., Ptd. blastopore, proctodjeum.

Enteropneusta (Balanoglossus). The body cavity is derived from two pairs of alimentary diverticula, the walls of which give rise to the greater part of the mesoblast.

Chordata. Paired archenteric outgrowths give rise to the whole mesoblast in Amphioxus (fig. 211), and the mode of formation of the mesoblast in other Chordata is probably secondarily derived from this.

3. The cells which will form the mesoblast become marked out very early, and cannot be regarded as definitely springing from either of the primary layers.

Turbellaria. Leptoplana (fig. 212), Planaria polychroa (?).

Chsetopoda. Lumbricus, &c.

Discophora.

It is very possible that the cases quoted under this head ought more properly to belong to group i.

4. The mesoblast cells are split off from the epiblast.

Nemertea. Larva of Desor. The mesoblast is stated to be split off from the four invaginated discs.

B. III. 23


354


DEVELOPMENT OF THE MESOBLAST.


5. The mcsoblast is split off from the hypoblast.

Nemertea. Some of the types without a metamorphosis.

Mollusca. Scaphopoda. It is derived from the lateral and ventral cells of the hypoblast.

Oephyrea. Phascolosoma.

Vertebrata. In most of the Ichthyopsida the mesoblast is derived from the hypoblast (fig. 213). In some types (i.e. most of the Amniota) the mesoblast might be described as originating at the lips of the blastopore (primitive streak).

6. The mesoblast is derived from both germinal layers.

Tracheata. Araneina (fig. 214). It is derived partly from cells split off from the epiblast and partly from the yolk-cells ; but it is probable that the statement that the mesoblast is derived from both the germinal layers is only formally accurate ; and that the derivation of part of the mesoblast from the yolk-cells is not to be interpreted as a derivation from the hypoblast.

Amniota. The derivation of the mesoblast of the Amniota from both the primary germinal layers is without doubt a secondary process.

The conclusions to be drawn from the above summary are by no means such as might have been anticipated. The analogy of the Ccelenterata would lead us to expect that the mesoblast



FIG. 211.


A. B.


SECTIONS OF AN AMPH'IOXUS EMBRYO AT TIIRKE STAGES.

(After Kowalevsky.) Section at gastrula stage. Section of a somewhat older embryo. C. Section through the anterior part of still older embryo. np. neural plate; nc. neural canal; mcs. archenteron in A, and mesenteron in B and C ; ch. notochord ; so. mesoblastic somite.

would be derived partly from the epiblast and partly from the hypoblast. Such, however, is not for the most part the case, though more complete investigations may shew that there are a greater number of instances in which the mesoblast has a mixed origin than might be supposed from the above summary.



ORIGIN OF THE GERMINAL LAYERS. 355

I have attempted to reduce the types of development of the mesoblast to six ; but owing to the nature of the case it is not always easy to distinguish the first of these from the last fourOf the six types the second will on most hands be admitted to be the most remarkable. The formation of hollow outgrowths of the archenteron, the cavities of which give rise to the body cavity, can only be explained on the supposition that the body cavity of the types in which such outgrowths occur is derived from diverticula cut off from the alimentary tract. The lining epithelium of the diverticula the peritoneal epithelium is clearly part of the primitive hypoblast, and this part of the mesoblast is clearly hypoblastic in origin.



FIG. 112. SECTIONS THROUGH THE OVUM OF LEPTOPLANA TREMELLARIS IN

THREE STAGES OF DEVELOPMENT. (After Hallez.) cp. epiblast ; ;;/. mesoblast; hy. yolk-cells (hypoblast); bl. blastopore.

In the case of the Chaetognatha (Sagitta), Brachiopoda, and Amphioxus, the whole of the mesoblast originates from the walls of the diverticula ; while in the Echinodermata the walls of the diverticula only give rise to the vaso-peritoneal epithelium, the remainder of the mesoblast being derived from amoeboid cells which spring from the walls of the archenteron before the origin of the vaso-peritoneal outgrowths (figs. 199 and 210).

Reserving for the moment the question as to what conclusions can be deduced from the above facts as to the origin of the mesoblast, it is important to determine how far the facts of embryology warrant us in supposing that in the whole of the triploblastic forms the body cavity originated from the alimentary diverticula. There can be but little doubt that the mode of origin of the mesoblast in many Vertebrata, as two solid plates split off from the hypoblast, in which a cavity is secondarily developed, is an abbreviation of the process observable in Amphioxus ; but this process approaches in some forms of

232


356


ORIGIN OF THE MESOBLAST.



Vertebrata to the ingrowth of the mesoblast from the lips of the blastopore.

It is, therefore, highly _ en A.

probable that the paired ingrowths of the mesoblast from the lips of the blastopore may have been in the first instance derived from a pair of archenteric diverticula. This process of formation of the mesoblast is, as may be seen by reference to the summary, the most frequent, including as it does the Chaetopoda,

the Mollusca, the Arthro- FIG. 213. Two SECTIONS OF A YOUNG 101 ELASMOBRANCH EMBRYO, TO SHEW THE

pOda, &C. MESOBLAST SPLIT OFF AS TWO LATERAL

MASSES FROM THE HYPOBLAST.

While there is no difficulty in the view that the body cavity may have originated from a pair of enteric diverticula in the case of the forms where a body cavity is present, there is a considerable difficulty in holding this view, for forms in which there is no body cavity distinct from the alimentary diverticula.

Of these types the Platyelminthes are the most striking. It is, no doubt, possible that a body cavity may have existed in the Platyelminthes, and become lost ; and the case of the Discophora, which in their muscular and connective tissue systems as well as in the absence of a body cavity resemble the Platyelminthes, may be cited in favour of this view, in that, being closely related to the Chaetopoda, they are almost certainly descended from ancestors with a true body cavity. The usual view of the primitive character of the


nig. medullary groove ; ep. epiblast ; ;;/. mesoblast ; hy. hypoblast ; n.al. cells formed around the nuclei of the yolk which have entered the hypoblast.


1 The wide occurrence of this process was first pointed out by Rabl. He holds, however, a peculiar modification of the gastrsea theory, for which I must refer the reader to his paper (No. 284) ; according to this theory the mesoblast has sprung from a zone of cells of the blastosphere, at the junction between the cells which will be invaginated and the epiblast cells. In the bilateral blastosphere, from which he holds that all the higher forms (Bilateralia) have originated, these cells had a bilateral arrangement, and thus the bilateral origin of the mesoblast is explained. The origin of the mesoblast from the lips of the blastopore is explained by the position of its mother-cells in the blastosphere. It need scarcely be said that the views already put forward as to the probable mode of origin of the mesoblast, founded on the analogy of the Ccelenterata, are quite incompatible with Rabl's theories.


ORIGIN OF THE GERMINAL LAYERS. 357

Platyelminthes, which has much to support it, is, however, opposed to the idea that the body cavity has disappeared.

If Kowalevsky 1 is right in stating that he has found a form intermediate between the Ccelenterata and the Platyelminthes, there will be strong grounds for holding that the Platyelminthes are, like the Ccelenterata, forms the ancestors of which were not provided with a body cavity.

Perhaps the triploblastica are composed of two groups, viz. (i) a more ancestral group (the Platyelminthes), in which there is no body cavity as dis


FIG. 214. SECTION THROUGH AN EMBRYO OK AGEI.ENA LABYRINTHICA. The section is represented with the ventral plate upwards. In the ventral plate is seen a keel-like thickening, which gives rise to the main mass of the mesoblast. yk. yolk divided into large polygonal cells, in several of which are nuclei.

tinct from the alimentary, and (2) a group descended from these, in which two of the alimentary diverticula have become separated from the alimentary tract to form a body cavity (remaining triploblastica). However this may be, the above considerations are sufficient to shew how much there is that is still obscure with reference even to the body cavity.

If embryology gives no certain sound as to the questions just raised with reference to the body cavity, still less is it to be hoped that the remaining questions with reference to the origin of the mesoblast can be satisfactorily answered. It is clear, in the first place, from an inspection of the summary given above, that the process of development of the mesoblast is, in all the higher forms, very much abbreviated and modified. Not only is its differentiation relatively deferred, but it does not in most cases originate, as it must have done to start with, as a more or

1 Zoologischer Anzeiger, No. 52, p. 140. This form has been named by Kowalevsky Cceloplana Metschnikowii. Kowalevsky's description appears, however, to be quite compatible with the view that this form is a creeping Ctenophor, in no way related to the Turbellarians.


358 EVOLUTION OK THE MESOBLAST.


less continuous sheet, split off from parts of one or both the primary layers. It originates in most cases from the hypoblast, and although the considerations already urged preclude us from laying very great stress on this mode of origin, yet the derivation of the mesoblast from the walls of archenteric outgrowths suggests the view that the whole, or at any rate the greater part, of the mesoblast primitively arose by a process of histogenic differentiation from the walls of the archenteron or rather from diverticula of these walls. This view, which was originally put forward by myself (No. 260), appears at first sight very improbable, but if the statement of the Hertwigs (No. 270), that there is a large development of a hypoblastic muscular system in the Actinozoa, is well founded, it cannot be rejected as impossible. Lankester (No. 279), on the other hand, has urged that the mode of origin of the mesoblast in the Echinodermata is more primitive ; and that the amoeboid cells which here give rise to the muscular and connective tissues represent cells which originally arose from the whole inner surface of the epiblast. It is, however, to be noted that even in the Echinodermata the amoeboid cells actually arise from the hypoblast, and their mode of origin may, therefore, be used to support the view that the main part of the muscular system of higher types is derived from the primitive hypoblast.

The great changes which have taken place in the development of the mesoblast would be more intelligible on this view than on the view that the major part of the mesoblast primitively originated from the epiblast. The presence of food-yolk is much more frequent in the hypoblast than in the epiblast ; and it is well known that a large number of the changes in early development are caused by food-yolk. If, therefore, the mesoblast has been derived from the hypoblast, many more changes might be expected to have been introduced into its early development than if it had been derived from the epiblast. At the same time the hypoblastic origin of the mesoblast would assist in explaining how it has come about that the development of the nervous system is almost always much less modified than that of the mesoblast, and that the nervous system is not, as might, on the grounds of analogy, have been anticipated, as a rule secondarily developed in the mesoblast.




ORIGIN OF THE GERMINAL LAYERS. 359

The Hertwigs have recently suggested in their very interesting memoir (No. 271) that the Triploblastica are to be divided into two phyla, (i) the Enteroccela, and (2) the Pseudocoela ; the former group containing the Chaetopoda, Gephyrea, Brachiopoda, Nematoda, Arthropoda, Echinodermata, Enteropneusta and Chordata ; and the latter the Mollusca, Polyzoa, the Rotifera, and Platyelminthes.

The Enteroccela are forms in which the primitive alimentary diverticula have given origin to the body cavity, while the major part of the muscular system has originated from the epithelial walls of these diverticula, part however being in many cases also derived from the amoeboid cells, called by them mesenchyme, by the second process of mesoblastic differentiation mentioned on p. 347.

In the Pseudoccela the muscular system has become differentiated from mesenchyme cells ; while the body cavity, where it exists, is merely a split in the mesenchyme.

It is impossible for me to attempt in this place to state fully, or do justice to, the original and suggestive views contained in this paper. The general conclusion I cannot however accept. The views of the Hertwigs depend to a large extent upon the supposition that it is possible to distinguish histologically muscle cells derived from epithelial cells, from those derived from mesenchyme cells. That in many cases, and strikingly so in the Chordata, the muscle cells retain clear indications of their primitive origin from epithelial cells, I freely admit ; but I do not believe either that its histological character can ever be conclusive as to the non-epithelial origin of a muscle cell, or that its derivation in the embryo from an indifferent amoeboid cell is any proof that it did not, to start with, originate from an epithelial cell.

I hold, as is clear from the preceding statements, that such immense secondary modifications have taken place in the development of the mesoblast, that no such definite conclusions can be deduced from its mode of development as the Hertwigs suppose.

In support of the view that the early character of embryonic cells is no safe index as to their phylogenetic origin, I would point to the few following facts.

(1) In the Porifera and many of the Ccelenterata (Eucope polystyla, Geryonia, &c.) the hypoblast (endoderm) originates from cells, which according to the Hertwigs' views ought to be classed as mesenchyme.

(2) In numerous instances muscles which have, phylogenetically, an undoubted epithelial origin, are ontogenetically derived from cells which ought to be classed as mesenchyme. The muscles of the head in all the higher Vertebrata, in which the head cavities have disappeared, are examples of this kind ; the muscles of many of the Tracheata, notably the Araneina, must also be placed in the same category.

(3) The Mollusca are considered by the Hertwigs to be typical Pseudocoela. A critical examination of the early development of the mesoblast in these forms demonstrates however that with reference to the mesoblast they


360 FCETAL AND LARVAL DEVELOPMENT.

must be classed in the same group as the Cluetopoda. The mesoblast (Vol. II. p. 227) clearly originates as two bands of cells which grow inwards from the blastopore, and in some forms (Paludina, Vol. II. fig. 107) become divided into a splanchnic and somatic layer, with a body cavity between them. All these processes are such as are, in other instances, admitted to indicate Enteroccclous affinities.

The subsequent conversion of the mesoblast elements into amoeboid cells, out of which branched muscles are formed, is in my opinion simply due to the envelopment of the soft Molluscan body within a hard shell.

In addition to these instances I may point out that the distinction between the Pseudocoela and Enteroccela utterly breaks down in the case of the Discophora, and the Hertwigs have made no serious attempt to discuss the characters of this group in the light of their theory, and that the derivation of the Echinoderm muscles from mesenchyme cells is a difficulty which is very slightly treated.


II. LARVAL FORMS: THEIR NATURE, ORIGIN AND AFFINITIES.

Preliminary considerations. In a general way two types of development may be distinguished, viz. a foetal type and a larval type. In the foetal type animals undergo the whole or nearly the whole of their development within the egg or within the body of the parent, and are hatched in a condition closely resembling the adult ; and in the larval type they are born at an earlier stage of development, in a condition differing to a greater or less extent from the adult, and reach the adult state either by a series of small steps, or by a more or less considerable metamorphosis.

The satisfactory application of embryological data to morphology depends upon a knowledge of the extent to which the record of ancestral history has been preserved in development. Unless secondary changes intervened this record would be complete ; it becomes therefore of the first importance to the cmbryologist to study the nature and extent of the secondary changes likely to occur in the fcetal or the larval state.

The principles which govern the perpetuation of variations which occur in either the larval or the fcetal state are the same as those for the adult condition. Variations favourable to the survival of the species are equally likely to be perpetuated, at whatever period of life they occur, prior to the loss of the reproductive powers. The possible nature and extent of the


LARVAL FORMS. 361


secondary changes which may have occurred in the developmental history of forms, which have either a long larval existence, or which are born in a nearly complete condition, is primarily determined by the nature of the favourable variations which can occur in each case.

Where the development is a fcetal one, the favourable variations which can most easily occur are (i) abbreviations, (2) an increase in the amount of food-yolk stored up for the use of the developing embryo. Abbreviations take place because direct development is always simpler, and therefore more advantageous; and, owing to the fact of the foetus not being required to lead an independent existence till birth, and of its being in the meantime nourished by food-yolk, or directly by the parent, there are no physiological causes to prevent the characters of any stage of the development, which are of functional importance during a free but not during a fcetal existence, from, disappearing from the developmental history. All organs of locomotion and nutrition not required by the adult will, for this reason, obviously have a tendency to disappear or to be reduced in foetal developments; and a little consideration will shew that the ancestral stages in the development of the nervous and muscular systems, organs of sense, and digestive system will be liable to drop out or be modified, when a simplification can thereby be effected. The circulatory and excretory systems will not be modified to the same extent, because both of them are usually functional during fcetal life.

The mechanical effects of food-yolk are very considerable, and numerous instances of its influence will be found in the earlier chapters of this work 1 . It mainly affects the early stages of development, i.e. the form of the gastrula, &c.

The favourable variations which may occur in the free larva are much less limited than those which can occur in the fcetus. Secondary characters are therefore very numerous in larvae, and there may even be larvae with secondary characters only, as, for instance, the larvae of Insects.

In spite of the liability of larvae to acquire secondary characters, there is a powerful counterbalancing influence tending

1 For numerous instances of this kind, vide Chapter XI. of Vol. in.


362 METAL AND LARVAL DEVELOPMENT.

towards the preservation of ancestral characters, in that larvae are necessarily compelled at all stages of their growth to retain in a functional state such systems of organs, at any rate, as are essential for a free and independent existence. It thus comes about that, in spite of the many causes tending to produce secondary changes in larvae, there is always a better chance of larvae repeating, in an unabbreviated form, their ancestral history, than is the case with embryos, which undergo their development within the egg.

It may be further noted as a fact which favours the relative retention by larvae of ancestral characters, that a secondary larval stage is less likely to be repeated in development than an ancestral stage, because there is always a strong tendency for the former, which is a secondarily intercalated link in the chain of development, to drop out by the occurrence of a reversion to the original type of development.

The relative chances of the ancestral history being preserved in the foetus or the larva may be summed up in the following way : There is a greater chance of the ancestral history being lost in forms which develop in the egg ; and of its being masked in those which are hatched as larvae.

The evidence from existing forms undoubtedly confirms the a priori considerations just urged 1 . This is well shewn by a study of the development of Echinodermata, Nemertea, Mollusca, Crustacea, and Tunicata. The free larvae of the four first groups are more similar amongst themselves than the embryos which develop directly, and since this similarity cannot be supposed to be due to the larvae having been modified by living under precisely similar conditions, it must be due to their retaining common ancestral characters. In the case of the Tunicata the free larvae retain much more completely than the embryos certain characters such as the notochord, the cerebrospinal canal, etc., which are known to be ancestral.

1 It has long been known that land and freshwater forms develop without a metamorphosis much more frequently than marine forms. This is probably to be explained by the fact that there is not the same possibility of a land or freshwater species extending itself over a wide area by the agency of free larvre, and there k, therefore, much less advantage in the existence of such larva:; while the fact of such larviu being more liable to be preyed upon than eggs, which are either concealed, or carried about by the parent, might render a larval stage absolutely disadvantageous.


LARVAL FORMS. 363


Types of Larvae. Although there is no reason to suppose that all larval forms are ancestral, yet it seems reasonable to anticipate that a certain number of the known types of larvae would retain the characters of the ancestors of the more important phyla of the animal kingdom.

Before examining in detail the claims of various larvae to such a character, it is necessary to consider somewhat more at length the kind of variations which are most likely to occur in larval forms.

It is probable a priori that there are two kinds of larvae, which may be distinguished as primary and secondary larvae. Primary larvae are more or less modified ancestral forms, which have continued uninterruptedly to develop as free larvae from the time when they constituted the adult form of the species. Secondary larvae are those which have become introduced into the ontogeny of species, the young of which were originally hatched with all the characters of the adult; such secondary larvae may have originated from a diminution of food-yolk in the egg and a consequently earlier commencement of a free existence, or from a simple adaptive modification in the just hatched young. Secondary larval forms may resemble the primary larval forms in cases where the ancestral characters were retained by the embryo in its development within the egg; but in other instances their characters are probably entirely adaptive.

Causes tending to produce secondary changes in larv<z. The modes of action of natural selection on larvae may probably be divided more or less artificially into two classes.

1. The changes in development directly produced by the existence of a larval stage.

2. The adaptive changes in a larva acquired in the ordinary course of the struggle for existence.

The changes which come under the first head consist essentially in a displacement in the order of development of certain organs. There is always a tendency in development to throw back the differentiation of the embryonic cells into definite tissues to as late a date as possible. This takes place in order to enable the changes of form, which every organ undergoes, in repeating even in an abbreviated way its phylogenetic history, to be effected with the least expenditure of energy. Owing to


364 CHANGES IN LARWE.

this tendency it comes about that when an organism is hatched as a larva many of the organs are still in an undifferentiated state, although the ancestral form which this larva represents had all its organs fully differentiated. In order, however, that the larva may be enabled to exist as an independent organism, certain sets of organs, e.g. the muscular, nervous, and digestive systems, have to be histologically differentiated. If the period of foetal life is shortened, an earlier differentiation of certain organs is a necessary consequence ; and in almost all cases the existence of a larval stage causes a displacement in order of development of organs, the complete differentiation of many organs being retarded relatively to the muscular, nervous, and digestive systems.

The possible changes under the second head appear to be unlimited. There is, so far as I see, no possible reason why an indefinite number of organs should not be developed in larvae to protect them from their enemies, and to enable them to compete with larvae of other species, and so on. The only limit to such development appears to be the shortness of larval life, which is not likely to be prolonged, since, ceteris paribus, the more quickly maturity is reached the better it is for the species.

A very superficial examination of marine larvae shews that there are certain peculiarities common to most of them, and it is important to determine how far such peculiarities are to be regarded as adaptive. Almost all marine larvae are provided with well-developed organs of locomotion, and transparent bodies. These two features are precisely those which it is most essential for such larvae to have. Organs of locomotion are important, in order that larvae may be scattered as widely as possible, and so disseminate the species ; and transparency is very important in rendering larvae invisible, and so less liable to be preyed upon by their numerous enemies 1 .

These considerations, coupled with the fact that almost all free-swimming animals, which have not other special means of protection, are transparent, seem to shew that the transparency

1 The phosphorescence of many larvze is very peculiar. I should have anticipated that phosphorescence would have rendered them much more liable to be captured by the forms which feed upon them; and it is difficult to see of what advantage it can be to them.


LARVAL FORMS. 365


of larvae at all events is adaptive ; and it is probable that organs of locomotion are in many cases specially developed, and not ancestral.

Various spinous processes on the larvae of Crustacea and Teleostei are also examples of secondarily acquired protective organs.

These general considerations are sufficient to form a basis for the discussion of the characters of the known types of larvae.

The following table contains a list of the more important of such larval forms :

DICYEMID^. The Infusoriform larva (vol. n. fig. 62).

PORIFERA. (a) The Amphiblastula larva (fig. 215), with one-half of the body ciliated, and the other half without cilia; (b) an oval uniformly ciliated larva, which may be either solid or have the form of a vesicle.

CCELENTERATA. The planula (fig. 216).

TURBELLARIA. (a) The eight-lobed larva of Miiller (fig. 222); (b) the larvae of Gotte and Metschnikoff, with some Pilidium characters.

NEMERTEA. The Pilidium (fig. 221).

TREMATODA. The Cercaria.

ROTIFERA. The Trochosphere-like larvae of Brachionus (fig. 217) and Lacinularia.

MOLLUSCA. The Trochosphere larva (fig. 218), and the subsequent Veliger larva (fig. 219).

BRACHIOPODA. The three-lobed larva, with a postoral ring of cilia (fig. 220).

POLYZOA. A larval form with a single ciliated ring surrounding the mouth, and an aboral ciliated ring or disc (fig. 228).

CH/ETOPODA. Various larval forms with many characters like those of the molluscan Trochosphere, frequently with distinct transverse bands of cilia. They are classified as Atrochoe, Mesotrochse, Telotrochse (fig. 225 A and fig. 226), Polytrochae, and Monotrochae (fig. 225 B).

GEPHYREA NUDA. Larval forms like those of preceding groups. A specially characteristic larva is that of Echiurus (fig. 227).

GEPHYREA TUBICOLA. Actinotrocha (fig. 230), with a postoral ciliated ring of arms.

MYRIAPODA. A functionally hexapodous larval form is common to all the Chilognatha (vol. n. fig. 174).

INSECTA. Various secondary larval forms.

CRUSTACEA. The Nauplius (vol. n. fig. 208) and the Zosea (vol. II. fig. 210).

ECHINODERMATA. The Auricularia (fig. 223 A), the Bipinnaria (fig. 223 B), and the Pluteus (fig. 224), and the transversely-ringed larvae of Crinoidea (vol. II. fig. 268). The three first of which can be reduced to a common type (fig. 231 c).

ENTEROPNEUSTA. Tornaria (fig. 229).

UROCHORDA (TUNICATA). The tadpole-like larva (vol. in. fig. 8).

GANOIDEI. A larva with a disc with adhesive papillae in front of the mouth (vol. in. fig. 67).

ANUROUS AMPHIBIA. The tadpole (vol. in. fig. 80).


366


TYPES OF LARVAE.


Of the larval forms included in the above list a certain



en


e.g.


FlG. 21=1. TWO FREE STAGES IN THE DEVELOPMENT OF SYCANDRA RAPHANUS.

(After Schultze. )

A. Amphiblastula stage.

B. Stage after the ciliated cells have commenced to be invaginated.

c.s. segmentation cavity; ec. granular epiblast cells; en. ciliated hypoblast cells.

number are probably without affinities outside the group to which they belong. This is the case with the larvae of the

C



FIG. 216. THREE LARVAL STAGES OF EUCOPE POLYSTYI.A. (After Kowalevsky.)

A. Blastosphere stage with hypoblast spheres becoming budded into the central cavity.

B. Planula stage with solid hypoblast.

C. I'lanula stage with a gastric cavity.

</>. epiblast: hy. hypoblast; al. gastric cavity.


LARVAL FORMS.


367


Myriapoda, the Crustacean lame, and with the larval forms of the Chordata. I shall leave these forms out of consideration.

There are, again, some larval forms which may possibly turn out hereafter to be of importance, but from which, in the present state of our knowledge, we cannot draw any conclusions. The infusoriform larva of the Dicyemidse, and the Cercaria of the Trematodes, are such forms.

Excluding these and certain other forms, we have finally left for consideration the larvae of the Ccelenterata, the Turbellaria, the Rotifera, the Nemertea, the Mollusca, the Polyzoa, the Brachiopoda, the Chaetopoda, the Gephyrea, the Echinodermata, and the Enteropneusta.

The larvae of these forms can be divided into two groups. The one group contains the larva of the Ccelenterata or Planula, the other group the larvae of all the other forms.

The Planula (fig. 216) is characterised by its extreme simplicity. It is a two-layered organism, with a form varying from cylindrical to oval, and usually a radial symmetry. So long as it remains free it is not usually provided with a mouth, and it is as yet uncertain whether or no the absence of a mouth is to be regarded as an ancestral character. The Planula is very probably the ancestral form of the Ccelenterata.

The larvae of almost all the other groups, although they may be subdivided into a series of very distinct types, yet agree in the possession of certain common characters 1 . There is a more or less dome-shaped dorsal surface, and a flattened or concave ventral surface, containing the open 1 The larva of the Brachiopoda does not possess most of the characters mentioned below. It is probably, all the same, a highly differentiated larval form belonging to this group.



Id


ov


FIG. 217. EMBRYO OF BRACHIONUS URCEOLARIS, SHORTLY BEFORE IT is HATCHED. (After Salensky.)

m. mouth ; ms. masticatory apparatus ; me. mesenteron ; an. anus ; Id. lateral gland ; ov. ovary ; t. tail (foot) ; tr. trochal disc ; sg. supraoesophageal ganglion.


368 LARWE OF THE TRIPLOBLASTICA.

ing of the mouth, and usually extending posteriorly to the opening of the anus, when such is present.

The dorsal dome is continued in front of the mouth to form a large prceoral lobe.

There is usually present at first an uniform covering of cilia ; but in the later larval stages there are almost always formed definite bands or rings of long cilia, by which locomotion is effected. These bands are often produced into arm-like processes.

The alimentary canal has, typically, the form of a bent tube with a ventral concavity, constituted (when an anus is present)



FIG. 218. DIAGRAM OF AN EMBRYO OF PLEUROBRANCHIDIUM.

(From Lankester.)

/. foot; ol. otocyst; m. mouth; v. velum; ng. nerve ganglion; ry. residual yolk spheres; sAs. shell-gland; i. intestine.

of three sections, viz. an oesophagus, a stomach, and a rectum. The oesophagus and sometimes the rectum are epiblastic in origin, while the stomach always and the rectum usually are derived from the hypoblast 1 .

To the above characters may be added a glass-like transparency ; and the presence of a widish space possibly filled with gelatinous tissue, and often traversed by contractile cells, between the alimentary tract and the body wall.

1 There is some uncertainty as to the development of the oesophagus in the Echinodermata, but recent researches appear to indicate that it is developed from the hypoblast.


LARVAL FORMS.


369


Considering the very profound differences which exist between many of these larvae, it may seem that the characters just enumerated are hardly sufficient to justify my grouping them together. It is, however, to be borne in mind that my grounds for doing so depend quite as much upon the fact that A B



FIG. 219. LARVAE OF CEPHALOPHOROUS MOLLUSCA IN THE VELIGER STAGE. (From Gegenbaur.)

A. and B. Earlier and later stage of Gasteropod. C. Pteropod (Cymbulia). v. velum; c. shell; /. foot; op. operculum ; t. tentacle.

they constitute a series without any great breaks in it, as upon the existence of characters common to the whole of them. It is also worth noting that most of the characters which have been enumerated as common to the whole of these larvae are not such secondary characters as (in accordance with the considerations used above) might be expected to arise from the fact of their being subjected to nearly similar conditions of life. Their transparency is, no doubt, such a secondary character, and it is not impossible that the existence of ciliated bands may be so also ; but it is quite possible that if, as I suppose, these larvae reproduce the characters of some ancestral form, this form may have existed at a time when all marine animals were free-swimming, and that it may, therefore, have been provided with at least one ciliated band.



FIG. 220. LARVA OF ARGIOPE. (From Gegenbaur ; after Kowalevsky.)

m. mantle ; b. setre ; d. archenteron.


B. III.


2 4


370 THE ECHINODERM GROUP.

The detailed consideration of the characters of these larvae, given below, supports this view.

This great class of larvae may, as already stated, be divided into a series of minor subdivisions. These subdivisions are the following :

1. The Pilidium Group. This group is characterised by the mouth being situated nearly in the centre of the ventral surface, and by the absence of an anus. It includes the Pilidium



FlG. 221. TWO STAGES IN THE DEVELOPMENT OF PlLIDIUM.

(After Metschnikoff.)

ae. archenteron; oe. oesophagus; st. stomach; am. amnion; pr.d. prostomial disc ; pod. metastomial disc ; c.s. cephalic sack (lateral pit).

of the Nemertines (fig. 221), and the various larvae of marine Dendrocoela (fig. 222). At the apex of the praeoral lobe a thickening of epiblast may be present, from which (fig. 232) a contractile cord sometimes passes to the oesophagus.

2. The Echinoderm Group. This group (figs. 223, 224 and 231 C) is characterised by the presence of a longitudinal pastoral band of cilia, by the absence of special sense organs in the praeoral region, and by the development of the body cavity as an outgrowth of the alimentary tract. The three typical divisions of the alimentary tract are present, and there is a more or less developed praeoral lobe. This group only includes the larvae of the Echinodermata.


LARVAL FORMS. 371


3. The Trochosphere Group. This group (figs. 225, 226) is characterised by the presence of a praeoral ring of long cilia, the region in front of which forms a great part of the praeoral lobe. The mouth opens immediately behind the praeoral ring of cilia, and there is very often a second ring of short cilia parallel to the main ring, immediately behind the mouth. The

B.



FIG. 222. A. LARVA OF EURYLEPTA AURICULATA IMMEDIATELY AFTER HATCHING. VIEWED FROM THE SIDE. (After Hallez.) m. mouth.

B. MULLER'S TURBELLARIAN LARVA (PROBABLY THYSANOZOON). VIEWED FROM THE VENTRAL SURFACE. (After Muller.) The ciliated band is represented by the black line. m. mouth ; u.l. upper lip.

function of the ring of short cilia is nutritive, in that its cilia are employed in bringing food to the mouth ; while the function of the main ring is locomotive. A perianal patch or ring of cilia is often present (fig. 225 A), and in many forms intermediate rings are developed between the praeoral and perianal rings.

The praeoral lobe is usually the seat of a special thickening of epiblast, which gives rise to the supra-cesophageal ganglion of the adult. On this lobe optic organs are very often developed in connection with the supra-oesophageal ganglion, and a contractile band frequently passes from this region to the oesophagus.

The alimentary tract is formed of the three typical divisions.

The body cavity is not developed directly as an outgrowth of the alimentary tract, though the process by which it originates is very probably secondarily modified from a pair of alimentary outgrowths.

24 2


372


TORNARIA.


Paired excretory organs, opening to the exterior and into the body cavity, are often present (fig. 226 nph}.

This type of larva is found in the Rotifera (fig. 217) (in which it is preserved in the adult state), the Chaetopoda (figs. 225 and 226), the Mollusca (fig. 218), the Gephyrea nuda (fig. 227), and the Polyzoa (fig. 228)'.



FIG. 223. A. THE LARVA OF A HOLOTHUROID. B. THE LARVA OF AN ASTEROID.

m. mouth; si. stomach; a. anus; I.e. primitive longitudinal ciliated band; pr.c. pneoral ciliated band.

4. Tornaria. This larva (fig. 229) is intermediate in most of its characters between the larvae of the Echinodermata (more especially the Bipinnaria) and the Trochosphere. It resembles Echinoderm larvae in the possession of a longitudinal ciliated band (divided into a praeoral and a postoral ring), and in the derivation of the body cavity and water-vascular vesicle from alimentary diverticula ; and it resembles the Trochosphere in the presence of sense organs on the praeoral lobe, in the existence of a perianal ring of cilia, and in the possession of a contractile band passing from the praeoral lobe to the oesophagus.



FIG. 224. LOCENTRUS.

m. mouth : d. stomach ;


A LARVA OF STROXGY(From Agassiz.)

a. anus ; o. oesophagus ; c. intestine ; v ' . and v.


ciliated ridges ; w. water- vascular tube ; r. calcareous rods.


1 For a discussion as to the structure of the Polyzoon larva, vide Vol. II. p. 305.


LARVAL FORMS. 373


5. Actinotrocha. The remarkable larva of Phoronis (fig. 230), known as Actinotrocha, is characterised by the presence of (i) a postoral and somewhat longitudinal ciliated ring produced into tentacles, and (2) a perianal ring. It is provided with a prseoral lobe, and a terminal or somewhat dorsal anus.

6. The larva of the Brachiopoda articulata (fig. 220). The relationships of the six types of larval forms thus briefly

characterised have been the subject of a considerable amount of controversy, and the following suggestions on their affinities must be viewed as somewhat speculative. The Pilidium type of larva is in some important respects less highly differentiated



FIG. 225. Two CH^TOPOD LARWE. (From Gegenhaur.)

o. mouth ; i. intestine ; a. anus ; v. praeoral ciliated band ; w. perianal ciliated band.

than the larvae of the five other groups. It is, in the first place, without an anus ; and there are no grounds for supposing that the anus has become lost by retrogressive changes. If for the moment it is granted that the Pilidium larva represents more nearly than the larvae of the other groups the ancestral type of larva, what characters are we led to assign to the ancestral form which this larva repeats ?

In the first place, this ancestral form, of which fig. 231 A is an ideal representation, would appear to have had a dome-shaped body, with a flattened oral surface and a rounded aboral surface. Its symmetry was radial, and in the centre of the flattened oral surface was placed the mouth, and round its edge was a ring of cilia. The passage of a Pilidium-like larva into the vermiform bilateral Platyelminth form, and therefore it may be presumed of the ancestral form which this larva repeats, is effected by the



374 ORIGIN OF PILIDIUM LARVA.

larva becoming more elongated, and by the region between the mouth and one end of the body becoming the pneoral region, and by an outgrowth between the mouth and the opposite end developing into the trunk, an anus becoming placed at its extremity in the higher forms.

If what has been so far postulated is correct, it is clear that this primitive larval form bears a very close resemblance to a simplified free-swimming Ccelenterate (Medusa), and that the conversion of such a radiate form into

..... , , , , . , , i FlG. 226. POLYGORDIUS

the bilateral took place, not by the LARVA- ( After Hatschek.) elongation of the aboral surface, and ;;/ mouth; ^ ^.^

the formation of an anus there, but by phageal ganglion ; nph. nephri, , , . r . 1 i r dion ; me.p. mesoblastic band :

the unequal elongation of the oral face, aw< anus f oL stomach .

an anterior part, together with the dome

above it, forming a praeoral lobe, and a posterior outgrowth the

trunk (figs. 226 and 233) ; while the aboral surface became the

dorsal surface.

This view fits in very well with the anatomical resemblances between the Coelenterata and the Turbellaria 1 , and shews, if true, that the ventral and median position of the mouth in many Turbellaria is the primitive one.

The above suggestion as to the mode of passage from the radial into the bilateral form differs largely from that usually held. Lankester 2 , for instance, gives the following account of this passage :

" It has been recognised by various writers, but notably by Gegenbaur and Haeckel, that a condition of radiate symmetry must have preceded the condition of bilateral symmetry in animal evolution. The Diblastula may be conceived to have been at first absolutely spherical with spherical symmetry. The establishment of a mouth led necessarily to the establishment of a structural axis passing through the mouth, around which axis the body was arranged with radial symmetry. This condition is more or less perfectly maintained by many Ccelenterates, and is reassumed by degrada 1 Vide Vol. II. pp. 179 and 191. In this connection attention may be called to Cceloplana Mdschnikowii, a form described by Kowalevsky, Zoologischer Anzeiger, No. 52, p. 140, as being intermediate between the Ctenophora and the Turbellaria. As already mentioned, there does not appear to me to be sufficient evidence to prove that this form is not merely a creeping Ctenophor.

Qiiart. Journ. of Micr. Science, Vol. XVH. pp. 422-3.


LARVAL FORMS.


375


tion of higher forms (Echinoderms, some Cirrhipedes, some Tunicates). The next step is the differentiation of an upper and a lower surface in



FIG. 227. LARVA OF ECHIURUS. (After Salensky.)

  1. . mouth ; an. anus ; sg. supra-oesophageal ganglion (?).

relation to the horizontal position, with mouth placed anteriorly, assumed by the organism in locomotion. With the differentiation of a superior and inferior surface, a right and a left side, complementary one to the other, are necessarily also differentiated. Thus the organism becomes bilaterally symmetrical. The Ccelentera are not wanting in indications of this bilateral symmetry, but for all other higher groups of animals it is a fundamental character. Probably the development of a region in front of, and dorsal to the mouth, forming the Prattomium, was accomplished pari passu with the development of bilateral symmetry. In the radially symmetrical Ccelentera we find very commonly a series of lobes of the bodywall or tentacles produced equally with radial symmetry, that is to say all round the mouth, the mouth terminating the main axis of the body that is to say, the organism being ' telostomiate.' The later fundamental form, common to all animals above the Ccelentera, is attained by shifting what was the main axis of the body so that it may be described now as the ' enteric ' axis ; whilst the new main axis, that parallel with the plane of progression, passes through the dorsal region of the body running obliquely in relation to the enteric axis. Only one lobe or outgrowth of those radially disposed in the telostomiate organisms now persists. This lobe lies dorsally to the mouth, and through it runs the new main axis. This lobe is the Prostomium, and all the organisms which thus develop a new main axis, oblique to the old main axis, may be called prostomiate."


FIG. 228. DIAGRAM OF A LARVA OF THE

POLYZOA.

m. mouth ; an. anus ; st. stomach; s. ciliated disc.


376


COMPARISON -BETWEEN TYPES OF LARVAE.


It will be seen from this quotation that the aboral part of the body is supposed to elongate to form the trunk, while the prasoral region is derived from one of the tentacles.

Before proceeding to further considerations as to the origin of the Bilateralia, suggested by the Pilidium type of larva, it is necessary to enter into a more detailed comparison between our larval forms.

A very superficial consideration of the characters of these forms brings to light two important features in which they differ, viz. :

(l) In the presence or absence of sense organs on the prasoral lobe.



FlG. 229. TWO STAGES IN THE DEVELOPMENT OF TORNARIA.

(After Metschnikoff.)

The black lines represent the ciliated bands.

in. mouth; an. anus; br. branchial cleft; ht. heart; c. body cavity between splanchnic and somatic mesoblast layers ; w. so-called water-vascular vesicle ; v. circular blood-vessel.

(2) In the presence or absence of outgrowths from the alimentary tract to form the body cavity.

The larvae of the Echinodermata and Actinotrocha (?) are without sense organs on the praeoral lobe, while the other types


LARVAL FORMS.


377


of larvae are provided with them. Alimentary diverticula are characteristic of the larvae of the Echinodermata and of Tornaria.

If the conclusion already arrived at to the effect that the prototype of the six larval groups was descended from a radiate ancestor is correct, it appears to follow that the nervous system, in so far as it was differentiated, had primitively a radiate form ; and it is also probably true that there were alimentary diverticula in the form of radial pouches, two of which may have given origin to the paired diverticula which become the body cavity in such types as the Echinodermata, Sagitta, etc. If these two points are granted, the further conclusions seem to follow (i) that the ganglion and sense organs of the praeoral lobe were secondary structures, which arose (perhaps as differentiations of an original circular nerve ring) after the assumption of a bilateral form; and (2) that the absence of these organs in the larvae of the Echinodermata and Actinotrocha (?) implies that these larvae retain, so far, more primitive characters than the Pilidium. The same may be said of the alimentary diverticula. There are thus indications that in two important points the Echinoderm larvae are more primitive than the Pilidium.

The above conclusions with reference to the Pilidium and Echinoderm larvae involve some not inconsiderable difficulties, and suggest certain points for further discussion.

In the first place it is to be noted that the above speculations render it probable that the type of nervous system from which that found in the adults of the Echinodermata, Platyelminthes, Chsetopoda, Mollusca, etc., is derived, was a circumoral ring, like that of Medusae, with which radially arranged sense organs may have been connected ; and that in the Echinodermata this form of nervous system has been retained, while in the other types it has been modified. Its anterior part may have given rise to supra-cesophageal ganglia and organs of vision ; these being



FIG. 230. ACTINOTROCHA. (After Metschnikoff.)

/. mouth ; an. anus.


378


PRIMITIVE TYPE OF NERVOUS SYSTEM.


developed on the assumption of a bilaterally symmetrical form, and the consequent necessity arising for the sense organs to be situated at the anterior end of the body. If this view is correct, the question presents itself as to how far the posterior part of the nervous system of the Bilateralia can be regarded as derived from the primitive radiate ring.



FIG. 231. THREE DIAGRAMS REPRESENTING THE IDEAL EVOLUTION OF VARIOUS

LARVAL FORMS.

A. Ideal ancestral larval form.

B. Larval form from which the Trochosphere larva may have been derived.

C. Larval form from which the typical Echinoderm larva may have been derived.

m. mouth ; an. anus ; st. stomach ; s.g. supra-cesophageal ganglion. The black lines represent the ciliated bands.

A circumoral nerve-ring, if longitudinally extended, might give rise to a pair of nerve-cords united in front and behind exactly such a nervous system, in fact, as is present in many Nemertines 1 (the Enopla and Pelagonemertes), in Peripatus 2 , and in primitive molluscan types (Chiton, Fissurella, etc.). From the lateral parts of this ring it would be easy to derive the ventral cord of the Chaetopoda and Arthropoda. It is especially deserving of notice in connection with the nervous system of the

1 Vute Hubrecht, "Zur Anat. und Phys. d. Nerven-System. d. Nemertinen," Kbn. Akad. Wiss., Amsterdam ; and " Researches on the Nervous System of Nemertines," Quart. Journ. of Micr. Science, 1880.

  • Vide F. M. Balfour, " On some points in the Anat. of Peripatus capensis," Quart.

Jourt:. of Micr. Science, Vol. xix. 1879.


LARVAL FORMS. 379


above-mentioned Nemertines and Peripatus, that the commissure connecting the two nerve-cords behind is placed on the dorsal side of the intestine. As is at once obvious, by referring to the diagram (fig. 231 B), this is the position this commissure ought, undoubtedly, to occupy if derived from part of a nerve-ring which originally followed more or less closely the ciliated edge of the body of the supposed radiate ancestor.

The fact of this arrangement of the nervous system being found in so primitive a type as the Nemertines tends to establish the views for which I am arguing ; the absence or imperfect development of the two longitudinal cords in Turbellarians may very probably be due to the posterior part of the nerve-ring having atrophied in this group.

It is by no means certain that this arrangement of the nervous system in some Mollusca and in Peripatus is primitive, though it may be so.

In the larvae of the Turbellaria the development of sense organs in the praeoral region is very clear (fig. 222 B) ; but this is by no means so obvious in the case of the true Pilidium. There is in Pilidium (fig. 232 A) a thickening of epiblast at the summit of the dorsal dome, which might seem, from the analogy of Mitraria, etc. (fig. 233), to correspond to the thickening of the praaoral lobe, which gives rise to the supra-cesophageal ganglion ; but, as a matter of fact, this part of the larva does not apparently enter into the formation of the young Nemertine (fig. 232). The peculiar metamorphosis, which takes place in the development of the Nemertine out of the Pilidium 1 , may, perhaps, eventually supply an explanation of this fact ; but at present it remains as a still unsolved difficulty.

The position of the flagellum in Pilidium, and of the supra-cesophageal ganglion in Mitraria, suggests a different view of the origin of the supraoesophageal ganglion from that adopted above. The position of the ganglion in Mitraria corresponds closely with that of the auditory organ in Ctenophora ; and it is not impossible that the two structures may have had a common origin. If this view is correct, we must suppose that the apex of the aboral lobe has become the centre of the praeoral field of the Pilidium and Trochosphere larval forms 2 a view which fits in very well with their structure (figs. 226 and 233). The whole of the questions concerning the nervous system are still very obscure, and until further facts are brought to light no definite conclusions can be arrived at.

1 Vide Vol. ii. p. 204.

2 The independent development of the supra-cesophageal ganglion and ventral nerve-cord in Chaetopoda (vide Kleinenberg, Development of Lumbricus trapezoides) agrees very satisfactorily with this view.


380 PRIMITIVE RADIAL SYMMETRY OF ECHINODERMATA.


The absence of sense organs on the praeoral lobe of larval Echinodermata, coupled with the structure of the nervous system of the adult, points to the conclusion that the adult Echinoder


FlG. 232. A. PlLIDIUM WITH AN ADVANCED NEMERTINE WORM. B. RlPE EMBRYO OF NEMERTES IN THE POSITION IT OCCUPIES IN PlLIDIUM. (Both after Biitschli.)

ft. oesophagus ; st. stomach ; i. intestine ; fr. proboscis ; lp. lateral pit (cephalic sack) ; a. amnion ; n. nervous system.

mata have retained, and not, as is now usually held, secondarily acquired, their radial symmetry; and if this is admitted it follows that the obvious bilateral symmetry of Echinoderm larvae is a secondary character.

The bilateral symmetry of many Ccelenterate larvae (the larva of ,/Eginopsis, of many Acraspeda, of Actinia, &c.), coupled with the fact that a bilateral symmetry is obviously advanta


LARVAL FORMS. 381


geous to a free-swimming form, is sufficient to shew that this supposition is by no means extravagant ; while the presence of only two alimentary diverticula in Echinoderm larvae is quite in accord with the presence of a single pair of perigastric chambers in the early larva of Actinia, though it must be admitted that the derivation of the water-vascular system from the left diverticulum is not easy to understand on this view.

A difficulty in the above speculation is presented by the fact of the anus of the Echinodermata being the permanent blastopore, and arising prior to the mouth. If this fact has any special significance, it becomes difficult to regard the larva of Echinoderms and that of the other types as in any way related ; but if the views already urged, in a previous section on the germinal layers, as to the unimportance of the blastopore, are admitted, the fact of the anus coinciding with the blastopore ceases to be a difficulty. As may be seen, by referring to fig. 231 C, the anus is placed on the dorsal side of the ciliated band. This position for the anus adapts itself to the view that the Echinoderm larva had originally a radial symmetry, with the anus placed at the aboral apex, and that, with the elongation of the larva on the attainment of a bilateral symmetry, the aboral apex became shifted to the present position of the anus.

It may be noticed that the obscure points connected with the absence of a body cavity in most adult Platyelminthes, which have already been dealt with in the section of this chapter devoted to the germinal layers, present themselves again here ; and that it is necessary to assume either that alimentary diverticula, like those in the Echinodermata, were primitively present in the Platyelminthes, but have now disappeared from the ontogeny of this group, or that the alimentary diverticula have not become separated from the alimentary tract.

So far the conclusion has been reached that the archetype of the six types of larvae had a radiate form, and that amongst existing larvae it is most nearly approached in general shape and in the form of the alimentary canal by the Pilidium group, and in certain other particulars by the Echinoderm larvae.

The edge of the oral disc of the larval archetype was probably armed with a ciliated ring, from which the ciliated ring of the Pilidium type and of the Echinodermata was most likely derived. The ciliated ring of the Pilidium varies greatly in its characters,


382 PRIMITIVE RADIAL SYMMETRY OF ECHINODERMATA.


and has not always the form of a complete ring. In Pilidium proper (fig. 232 A) it is a simple ring surrounding the edge of the oral disc. In Muller's larva of Thysanozoon (fig. 222 B) it is



FlG. 233. TWO STAGES IN THE DEVELOPMENT OF MlTRARIA. (After Metschnikoff.) m. mouth; an. anus; sg. supra-cesophageal ganglion; br. and b. provisional bristles ; pr.b. prasoral ciliated band.

inclined at an axis to the oral disc, and might be called praeoral, but such a term cannot be properly used in the absence of an anus.



FIG. 234. CYPHONAUTES (LARVA OF MEMBRANIPORA). (After Hatschek.)

m. mouth ; a '. anus ; f.g. foot gland ; x. problematical body (probably a bud).

The aboral apex is turned downwards.


LARVAL FORMS. 383


The Echinoderm ring is oblique to the axis of the body, and, owing to the fact of its passing ventrally in front of the anus, must be called postoral.

The next point to be considered is that of the affinities of the other larval types to these two types.

The most important of all the larval types is the Trochosphere, and this type is undoubtedly more closely related to the Pilidium than to the Echinoderm larva. Mitraria amongst the Chaetopods (fig. 233) has, indeed, nearly the form of a Pilidium, and mainly differs from a Pilidium in the possession of an anus and of provisional bristles ; the same may be said of Cyphonautes (fig. 234) amongst the Polyzoa.

The existence of these two forms appears to shew that the praeoral ciliated ring of the Trochosphere may very probably be derived directly from the circumoral ciliated ring of the Pilidium; the other ciliated rings or patches of the Trochosphere having a secondary origin.

The larva of the Brachiopoda (fig. 220), in spite of its peculiar characters, is, in all probability, more closely related to the Chaetopod Trochosphere than to any other larval type. The most conspicuous point of agreement between them is, however, the possession in common of provisional setae.

Echinoderm larvae differ from the Trochosphere, not only in the points already alluded to, but in the character of the ciliated band. The Echinoderm band is longitudinal and postoral. As just stated, there is reason to think that the praeoral band of the Trochosphere and the postoral band of the Echinoderm larva are both derived from a ciliated ring surrounding the oral disc of the prototype of these larvae (vide fig. 231). In the case of the Echinodermata the anus must have been formed on the dorsal side of this ring, and in the case of the Trochosphere on the ventral side ; and so the difference in position between the two rings was brought about. Another view with reference to these rings has been put forward by Gegenbaur and Lankester, to the effect that the praeoral ring of the Trochosphere is derived from the breaking up of the single band of most Echinoderm larvae into the two bands found in Bipinnaria (vide fig. 223) and the atrophy of the posterior band. There is no doubt a good deal to be said for this origin of the praeoral ring, and it is


384 PHYLOGENETIC CONCLUSIONS.

strengthened by the case of Tornaria ; but the view adopted above appears to me more probable.

Actinotrocha (fig. 230) undoubtedly resembles more closely Echinoderm larvae than the Trochosphere. Its ciliated ring has Echinoderm characters, and the growth along the line of the ciliated ring of a series of arms is very similar to what takes place in many Echinoderms. It also agrees with the Echinoderm larvae in the absence of sense organs on the praeoral lobe.

Tornaria (fig. 229) cannot be definitely united either with the Trochosphere or with the Echinoderm larval type. It has important characters in common with both of these groups, and the mixture of these characters renders it a very striking and well-defined larval form.

Phylogenetic conclusions. The phylogenetic conclusions which follow from the above views remain to be dealt with. The fact that all the larvae of the groups above the Ccelenterata can be reduced to a common type seems to indicate that all the higher groups are descended from a single stem.

Considering that the larvae of comparatively few groups have persisted, no conclusions as to affinities can be drawn from the absence of a larva in any group; and the presence in two groups of a common larval form may be taken as proving a common descent, but does not necessarily shew any close affinity.

There is every reason to believe that the types with a Trochosphere larva, viz. the Rotifera, the Mollusca, the Chaetopoda, the Gephyrea, and the Polyzoa, are descended from a common ancestral form ; and it is also fairly certain there was a remote ancestor common to these forms and to the Platyelminthes. A general affinity of the Brachiopoda with the Chaetopoda is more than probable. All these types, together with various other types which are nearly related to them, but have not preserved an early larval form, are descended from a bilateral ancestor. The Echinodermata, on the other hand, are probably directly descended from a radial ancestor, and have more or less completely retained their radial symmetry. How far Actinotrocha 1 is related to the Echinoderm larvae cannot be settled. Its characters may possibly be secondary, like those of the

1 It is quite possible that Phoronis is in no way related to the other Gephyrea.


LARVAL FORMS. 385


mesotrochal larvae of Chaetopods, or they may be due to its having branched off very early from the stock common to the whole of the forms above the Ccelenterata. The position of Tornaria is still more obscure. It is difficult, in the face of the peculiar water-vascular vesicle with a dorsal pore, to avoid the conclusion that it has some affinities with the Echinoderm larvae. Such affinities would seem, on the lines of speculation adopted in this section, to prove that its affinities to the Trochosphere, striking as they appear to be, are secondary and adaptive. From this conclusion, if justified, it would follow that the Echinodermata and Enteropneusta have a remote ancestor in common, but not that the two groups are in any other way related.

General conclusions and summary. Starting from the demonstrated fact that the larval forms of a number of widely separated types above the Ccelenterata have certain characters in common, it has \&&\ provisionally assumed that the characters have been inherited from a common ancestor ; and an attempt has been made to determine (i) the characters of the prototype of all these larvae, and (2) the mutual relations of the larval forms in question. This attempt started with certain more or less plausible suggestions, the truth of which can only be tested by the coherence of the results which follow from them, and their capacity to explain all the facts.

The results arrived at may be summarised as follows :

1. The larval forms above the Ccelenterata may be divided into six groups enumerated on pages 370 to 373.

2. The prototype of all these groups was an organism something like a Medusa, with a radial symmetry. The mouth was placed in the centre of a flattened ventral surface. The aboral surface was dome-shaped. Round the edge of the oral surface was a ciliated ring, and probably a nervous ring provided with sense organs. The alimentary canal was prolonged into two or more diverticula, and there was no anus.

3. The bilaterally symmetrical types were derived from this larval form by the larva becoming oval, and the region in front of the mouth forming a praeoral lobe, and that behind the mouth growing out to form the trunk. The aboral dome became the dorsal surface.

On the establishment of a bilateral symmetry the anterior

15. in. 25


386 GENERAL CONCLUSIONS.

part of the nervous ring gave rise (?) to the supra-cesophageal ganglia, and the optic organs connected with them ; while the posterior part of the nerve-ring formed (?) the ventral nerve-cords. The body cavity was developed from two of the primitive alimentary diverticula.

The usual view that radiate forms have become bilateral by the elongation of the aboral dome into the trunk is probably erroneous.

4. Pilidium is the larval form which most nearly reproduces the characters of the larval prototype in the course of its conversion into a bilateral form.

5. The Trochosphere is a completely differentiated bilateral form, in which an anus has become developed. The praeoral ciliated ring of the Trochosphere is probably directly derived from the ciliated ring of Pilidium, which is itself the original ring of the prototype of all these larval forms.

6. Echinoderm larvae, in the absence of a nerve-ganglion or special organs of sense on the prseoral lobe, and in the presence of alimentary diverticula, which give rise to the body cavity, retain some characters of the prototype larva which have been lost in Pilidium. The ciliated ring of Echinoderm larvae is probably derived directly from that of the prototype by the formation of an anus on the dorsal side of the ring. The anus was very probably originally situated at the aboral apex.

Adult Echinoderms have probably retained the radial symmetry of the forms from which they are descended, their nervous ring being directly derived from the circular nervous ring of their ancestors. They have not, as is usually supposed, secondarily acquired their radial symmetry. The bilateral symmetry of the larva is, on this view, secondary, like that of so many Coelenterate larvae.

7. The points of similarity between Tornaria and (i) the Trochosphere and (2) the Echinoderm larvae are probably adaptive in the one case or the other ; and, while there is no difficulty in believing that those to the Trochosphere are adaptive, the presence of a water- vascular vesicle with a dorsal pore renders probable a real affinity with Echinoderm larvae.

8. It is not possible in the present state of our knowledge to decide how far the resemblances between Actinotrocha and Echinoderm larvae are adaptive or primary.


LARVAL FORMS. 387


BIBLIOGRAPHY.

(257) Allen Thomson. British Association Address, 1877.

(258) A. Agassiz. " Embryology of the Ctenophorae." Mem. Amer. Acad. of Arts and Sciences, Vol. X. 1874.

(259) K. E. von Baer. Ueb. Entivicklungsgeschichte d. Thiere. Konigsberg, 18281837.

(260) F. M. Balfour. "A Comparison of the Early Stages in the Development of Vertebrates." Quart. Joum. of Micr. Set., Vol. XV. 1875.

(261) C. Glaus. Die Typenlehre u. E. HaeckeFs sg. Gastraa-tlieorie. Wien, 1874.

'(262) C. Glaus. Grundziige d. Zoologie. Marburg und Leipzig, 1879.

(263) A. Dohrn. Der Ursprung d. Wirbelthiere u. d. Princip des Functionsivechsels. Leipzig, 1875.

(264) C. Gegenbaur. Grttndriss d. vergleichenden Anatomic. Leipzig, 1878. Vide also Translation. Elements of Comparative Anatomy. Macmillan & Co. 1878.

(265) A. Gotte. Entwicklungsgeschichte d. Unke. Leipzig, 1874.

(266) E. Haeckel. Studien z. Gastraa-theorie, Jena, 1877; and also jtenaisc/ic Zeitschrift, Vols. vin. and IX. 1874-5.

(267) E. Haeckel. Schopfungsgeschichte. Leipzig. Vide also Translation, The History of Creation. King & Co., London, 1878.

(268) E. Haeckel. Anthropogenic. Leipzig. Vide also Translation, Anthropogeny. Kegan Paul & Co., London, 1878.

(269) B. Hatschek. "Studien lib. Entwicklungsgeschichte d. Anneliden." Arbeit, a. d. zool. Instit. d. Univer. Wien. 1878.

(270) O. and R. Hertwig. "Die Actinien." Jenaische Zeitschrift, Vols. xm. and xiv. 1879.

(271) O. and R. Hertwig. Die Ccelomtheorie. Jena, 1881'.

(272) O. Hertwig. Die Chatognathen. Jena, 1880.

(273) R. Hertwig. Ueb. d. Bau d. Ctenophoren. Jena, 1880.

(274) T. H. Huxley. The Anatomy of Invertebrated Animals. Churchill, 1877.

(274*) T. H. Huxley. "On the Classification of the Animal Kingdom." Quart. J. of Micr. Science, Vol. xv. 1875.

(275) N. Kleinenberg. Hydra, eine anatomisch-cntwickhingsgeschichtiiche Untersuchung. Leipzig, 1872.

(276) A. Kolliker. Entwicklungsgeschichte d. Menschen it, d. hoh. Thiere. Leipzig, 1879.

(277) A. Kowale vsky. " Embryologische Studien an Wiirmern u. Arthropoden." Mem. Acad. Petersbourg, Series vil. Vol. xvi. 1871.

(278) E. R. Lankester. "On the Germinal Layers of the Embryo as the Basis of the Genealogical Classification of Animals." Ann. and Mag. of Nat. Hist. 1873 1 This important memoir only came into my hands after this chapter was already in type.

25 2


388 BIBLIOGRAPHY.


(279) E. R. Lankester. "Notes on Embryology and Classification." Quart. Jonrn. of Micr. Set., Vol. XVII. 1877.

(280) E. Metschnikoff. "Zur Entwicklungsgeschichte d. Kalkschwamme." Zeit.f. wiss. Zool., Vol. xxiv. 1874.

(281) E. Metschnikoff. " Spongiologische Stuclien." Zeit.f, wiss. Zool., Vol. xxxn. 1879.

(282) A. S. P. Packard. Life Histories of Animals, including Man, or Outlines of Comparative Embryology. Holt and Co., New York, 1876.

(283) C. Rabl. " Ueb. d. Entwick. d. Malermuschel. " Jenaische Zeitsch., Vol. x. 1876.

(284) C. Rabl. "Ueb. d. Entwicklung. d. Tellerschnecke (Planorbis)." Morph. Jahrbuch, Vol. v. 1879.

(285) H. Rathke. Abhandlungen 2. Bildung und Entwicklungsgesch. d. Menschen . d. Thiere. Leipzig, 1833.

(286) H. Rathke. Ueber die Bildung u. Entwicklungs. d. Flusskrebses. Leipzig, 1829.

(287) R. Remak. Untersuch. iib. d. Entwick. d. Wirbelthiere. Berlin, 1855.

(288) Salensky. " Bemerkungen iib. Haeckels Gastrsea-theorie." Archiv f. Na turgesch ich te, 1874.

(289) E. Schafer. "Some Teachings of Development." Quart. Jonnt. of Micr. Science, Vol. xx. 1880.

(290) C. Semper. "Die Verwandtschaftbeziehungen d. gegliederten Thiere. Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. III. 1876-7.


PART II.

ORGANOGENY.


PART II. ORGANOGENV.

INTRODUCTION.

OUR knowledge of the development of the organs in most of the Invertebrate groups is so meagre that it would not be profitable to attempt to treat systematically the organogeny of the whole animal kingdom.

For this reason the plan adopted in this section of the work has been to treat somewhat fully the organogeny of the Chordata, which is comparatively well known ; and merely to indicate a few salient facts with reference to the organogeny of other groups. In the case of the nervous system, and of some other organs which especially lend themselves to this treatment, such as the organs of special sense and the excretory system, a wider view of the subject has been taken ; and certain general principles underlying the development of other organs have also been noticed.

The classification of the organs is a matter of some difficulty. Considering the character of this treatise it seemed desirable to arrange the organs according to the layers from which they are developed. The compound nature of many organs, e.g. the eye and ear, renders it, however, impossible to carry out consistently such a mode of treatment. I have accordingly adopted a rough classification of the organs according to the layers, dropping the principle where convenient, as, for instance, in the case of the stomodaeum and proctodseum.

The organs which may be regarded as mainly derived from


392 INTRODUCTION.


the epiblast are (i) the skin; (2) the nervous system; (3) the organs of special sense.

Those from the mesoblast are (i) the general connective tissue and skeleton ; (2) the vascular system and body cavity ; (3) the muscular system ; (4) the urinogenital system.

Those from the hypoblast are the alimentary tract and its derivates ; with which the stomodaeum and proctodaeum and their respective derivates are also dealt with.

BIBLIOGRAPHY.

General works dealing with the development of the organs of the

Chordata.

(291) K. E. von Baer. Ueber Entwicklungsgeschichte d. Thiere. Konigsberg, 18281837.

(292) F. M. Balfour. A Monograph on tlic development of Elasmobrancli Fishes. London, 1878.

(293) Th. C. W. Bischoff. Entwicklungsgesch. d. Sdtigethiere ti. d. Menschen. Leipzig, 1842.

(294) C. Gegenbaur. Gnindriss d. vergleichenden Anatomic. Leipzig, 1878. Vide also English translation, Elements of Comp. Anatomy. London, 1878.

(295) M. Foster and F. M. Balfour. The Elements of Embryology. Part I. London, 1874.

(296) Alex. Gotte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.

(297) W. His. Untersitch. iib. d. erste Anlage d. Wirbelthierleibcs . Leipzig, 1868.

(298) A. Ko Hiker. Entwicklungsgeschichte d. Menschen u. der hoheren Thiere. Leipzig, 1879.

(299) H. Rathke. Abhandlungen it. Bildung mid Entwicklungsgeschichle d. Menschen it. d. Thiere. Leipzig, 1838.

(300) H. Rathke. Entwicklungs. d. Natter. Kbnigsberg, 1839.

(301) H. Rathke. Entwicklungs. d. Wirbelthiere. Leipzig, 1861.

(302) R. Remak. Untersuchnngen iib. d. Entwicklung d. Wirbelthiere. Berlin, 18501855.

(303) S. L. Schenk. Lehrbuch d. vei'gleich. Embryologie d. Wirbeltliicre. Wien, 1874.


.

CHAPTER XIV. THE EPIDERMIS AND ITS DERIVATIVES.


IN many of the Ccelenterata the outermost layer of the blastoderm is converted as a whole into the skin or ectoderm. The cells composing it become no doubt in part differentiated into muscular elements and in part into nervous elements, &c. ; but still it may remain through life as a simple external membrane. This membrane contains in itself indefinite potentialities for developing into various organs, and in all the true Triploblastica these potentialities are more or less realized. The embryonic epiblast ceases in fact, in the higher forms, to become converted as a whole into the epidermis, but first gives rise to parts of the nervous system, organs of special sense, and other parts.

After the formation of these parts the remnant of the epiblast gives rise to the epidermis, and often unites more or less intimately with a subjacent layer of mesoblast, known as the dermis, to form with it the skin.

Various differentiations may arise in the epidermis forming protective or skeletal structures, terminal sense organs, or glands. The structure of the epidermis itself varies greatly, and for Vertebrates its general modifications have been already sufficiently dealt with in chapter XII. Of its special differentiations those of a protective or skeletal nature and those of a glandular nature may be considered in this place.

Protective epidermal structures. These structures constitute a general cuticle or an exoskeleton of scales, hairs, feathers, nails, hoofs, &c. They may be entirely formed from


394 TH E EXOSKELETON.


the epidermis either as (i) a cuticular deposit, or as (2) a chitinization, a cornification, or calcification of its constituent cells. These two processes run into each other, and are in many cases not easily distinguished. The protective structures of the epidermis may be divided into two groups according as they are formed on the outer or the inner side of the epidermis. Dermal skeletal structures are in many cases added to them. Amongst the Invertebrata the most widely distributed type of exoskeleton is a cuticle formed on the outer surface of the epidermis, which reaches its highest development in the Arthropoda. In the same class with this cuticle must be placed the molluscan and brachiopod shells, which are developed as cuticular plates on special regions of the epidermis. They differ, however, from the more usual form of cuticle in their slighter adhesion to the subjacent epidermis, and in their more complicated structure. The test of Ascidians is an abnormal form of exoskeleton belonging to this type. It is originally formed (Hertvvig and Semper) as a cuticle on the surface of the epidermis ; but subsequently epidermic cells migrate into it, and it then constitutes a tissue similar to connective tissue, but differing from ordinary epidermic cuticles in that the cells which deposit it do so over their whole surface, instead of one surface, as is usually the case with epithelial cells.

In the Vertebrata the two types of exoskeleton mentioned above are both found, but that developed on the inner surface of the epidermis is always associated with a dermal skeleton, and that on the outer side frequently so. The type of exoskeleton developed on the inner side of the general epidermis is confined to the Pisces, where it appears as the scales; but a primitive form of these structures persists as the teeth in the Amphibia and Amniota. The type developed on the outer side of the epidermis is almost entirely 1 confined to the Amphibia and Amniota, where it appears as scales, feathers, hairs, claws, nails, &c. For the histological details as to the formation of these various organs I must refer the reader to treatises on histology, confining my attention here to the general embryological processes which take place in their development.

1 The horny teeth of the Cyclostomala are structures belonging to this group.


THE EPIDERMIS AND ITS DERIVATIVES.


395


The most primitive form of the first type of dermal structures is that of the placoid scales of Elasmobranchii 1 . These consist, when fully formed, of a plate bearing a spinous projection. They are constituted of an outer enamel layer on the projecting part, developed as a cuticular deposit of the epidermis (epiblast), and an underlying basis of dentine (the lower part of which may be osseous) with a vascular pulp in its axis. The development (fig. 235) is as follows (Hertwig, No. 306). A papilla of the dermis makes its appearance, the outer layer of which gradually calcifies to form the dentine and osseous tissue. This papilla is covered by the columnar mucous layer of the epidermis (e), from which it is separated by a basement membrane, itself a product of the epidermis. This membrane gradually thickens and calcifies, and so gives rise to the enamel cap (o). The spinous point gradually forces its way through the epidermis, so as to project freely at the surface.

The scales of other forms of fishes are to be derived from those of Elasmobranchii. The great dermal plates of many fishes have been formed by the concrescence of groups of such scales. The dentine in many cases partially or completely atrophies, leaving the major part of the scale formed of osseous tissue ; such plates often become parts of the internal skeleton.



d


5\



FIG. 235. VERTICAL SECTION THROUGH THE SKIN OF AN EMBRYONIC SHARK, TO SHEW A DEVELOPING PLACOID SCALE. (From Gegenbaur ; after O. Hertwig.)

E. epidermis ; C. layers of dermis ; d. uppermost layer of dermis ; p. papilla of dermis ; e. mucous layer of epidermis ; o. enamel layer.

1 For the most important contributions on this subject from which the facts and views here expressed are largely derived, vide O. Hertwig, Nos. 306 808.


396 THK KXOSKELETON.


The teeth, as will be more particularly described in the section on the alimentary tract, are formed by a modification of the same process as the placoid scales, in which a ridge of the epithelium grows inwards to meet a connective tissue papilla, so that the development of the teeth takes place entirely below the superficial layer of epidermis.

In most Teleostei the enamel and dentine layers have disappeared, and the scales are entirely formed of a peculiar calcified tissue developed in the dermis.

The cuticle covering the scales of Reptiles is the simplest type of protective structure formed on the outer surface of the epidermis. The scales consist of papillae of the dermis and epidermis ; and are covered by a thickened portion of a twolayered cuticle, formed over the whole surface of the body from a cornification of the superficial part of the epidermis. Dermal osseous plates may be formed in connection with these scales, but are never of course united with the superficial cuticle.

Feathers are probably special modifications of such scales. They arise rom an induration of the epidermis of papillae containing a vascular core. The provisional down, usually present at the time of hatching, is formed by the cornification of longitudinal ridges of the mucous layer of the epidermis of the papillee ; each cornified ridge giving rise to a barb of the feather. The horny layer of the epidermis forms a provisional sheath for the developing feather below. When the barbs are fully formed this sheath is thrown- off, the vascular core dries up, and the barbs become free except at their base.

Without entering into the somewhat complicated details of the formation of the permanent feathers, it may be mentioned that the calamus or quill is formed by a cornification in the form of a tube of both layers of the epidermis at the base of the papilla. The quill is open at both ends, and to it is attached the vexillum or plume of the feather. In a typical feather this is formed at the apex of the papilla from ridge-like thickenings of the mucous layer of the epidermis, arranged in the form of a longitudinal axis, continuous with the cornified mucous layer of the quill, and from lateral ridges. These subsequently become converted into the axis and barbs of the plume. The external epidermic layer becomes converted into a provisional horny sheath for the true feather beneath.

On the completion of the plume of the feather the external sheath is thrown off, leaving it quite free, and the vascular core belonging to it shrivels up. The papilla in which the feather is formed becomes at a very early period secondarily enveloped in a pit or follicle which gradually deepens as the development of the feather is continued.

Hairs (Kolliker, No. 298) are formed in solid processes of the mucous layer of the epidermis, which project into the


THE p;PIDERMIS AND ITS DERIVATIVES. 397

subjacent dermis. The hair itself arises from a cornification of the cells of the axis of one of the above processes ; and is invested by a sheath similarly formed from the more superficial epidermic cells. A small papilla of the dermis grows into the inner end of the epidermic process when the hair is first formed. The first trace of the hair appears close to this papilla, but soon increases in length, and when the end of the hair projects from the surface, the original solid process of the epidermis becomes converted into an open pit, the lumen of which is filled by the root of the hair. Hairs differ in their mode of formation from scales in a manner analogous to that in which the teeth differ from ordinary placoid scales ; i.e. they are formed in inwardly directed projections of the epidermis instead of upon free papillae at the surface.

Nails (Kolliker, No. 298) are developed on special regions of the epidermis, known as the primitive nail beds. They are formed by the cornification of a layer of cells which makes its appearance between the horny and mucous layers of the epidermis. The distal border of the nail soon becomes free, and the further growth is effected by additions to the under side and attached extremity of the nail.

Although the nail at first arises in the interior of the epidermis, yet its position on the outer side of the mucous layer clearly indicates with which group of epidermic structures it should be classified.

Dermal skeletal structures. We have seen that in the Chordata skeletal structures, which were primitively formed of both an epidermic and dermic element, may lose the former element and be entirely developed in the dermis. Amongst the Invertebrata there are certain dermal skeletal structures which are evolved wholly independently of the epidermis. The most important of these structures are the skeletal plates of the Echinodermata.

Glands. The secretory part of the various glandular structures belonging to the skin is invariably formed from the epidermis. In Mammalia it appears that these glands are always formed as solid ingrowths of the mucous layer (Kolliker, No. 298). The ends of these ingrowths dilate to form the true glandular part of the organs, while the stalks connecting the glandular portions with the surface form the ducts. In the case of the sweat-glands the lumen of the duct becomes first established. Its formation is inaugurated by the appearance of


398 THE EXOSKELETON.


the cuticle, and appears first at the inner end of the duct and thence extends outwards (Ranvier, No. 311). In the sebaceous glands the first secretion is formed by a fatty modification of the whole of the central cells of the gland.

The muscular layer of the secreting part of the sweat-glands is formed, according to Ranvier (No. 311), from a modification of the deeper layer of the epidermic cells.

The Mammary Glands arise in essentially the same manner as the other glands of the skin 1 . The glands of each side are formed as a solid bud of the mucous layer of the epidermis. From this bud processes sprout out, each of which gives rise to one of the numerous glands of which the whole organ is formed. Two very distinct types in the relation of the ducts of the glands to the nipple are found (Gegenbaur, No. 313).

BIBLIOGRAPHY OF EPIDERMIS. General.

(304) T. H. Huxley. " Tegumentary organs." Tocld's Cyclopaedia of Anat. and Physiol.

(305) P. Z. Unna. " Histol. u. Entwick. d. Oberhaut." Archiv f. mikr. Anat. Vol. xv. 1876. FzV&also Kolliker (No. 298).

Scales of tJic Pisces.

(306) O. Her twig. " Ueber Bau u. Entwicklung d. Placoidschuppen u. d. Zahne d. Selachier." Jenaische Zeitschrift, Vol. vin. 1874.

(307) O. Hertwig. " Ueber d. Hautskelet d. Fische." Morphol. Jahrln<ch, Vol. n. 1876. (Siluroiden u. Acipenseridre.)

(308) O. Hertwig. "Ueber d. Hautskelet d. Fische (Lepidosteus u. Polypterus)." Alorph. Jahrbuch, Vol. v. 1879.

FeatJiers.

(309) Th. Studer. Die Entwick. d. Federn. Inaug. Diss. Bern, 1873.

(310) Th. Studer. "Beitrage z. Entwick. d. Feder." Zeit. f. wiss. Zool., Vol. xxx. 1878.

Sweat-glands.

(311) M. S. Ranvier. " Sur la structure des glandes sudoripares." Comptes A'f/iiiits, Dec. 29, 1879.

1 For a very different view on this subject vide Creighton (No. 312).


BIBLIOGRAPHY OF EPIDERMIS. 399


Mammary glands.

(312) C. Creighton. "On the development of the Mamma and the Mammary function." Jour, of Anat. and Phys. , Vol. XI. 1877.

(313) C. Gegenbaur. " Bemerkungen iib. d. Milchdriisen-Papillen d. Saugethiere." Jenaische Zeit., Vol. vn. 1873.

(314) M. Huss. "Beitr. z. Entwick. d. Milchdriisen b. Menschen u. b. Wiederkauern." Jenaische Zeit., Vol. vil. 1873.

(315) C. Langer. " Ueber d. Ban u. d. Entwicklung d. Milchdriisen." Denk. d. k. Akad. Wiss. Wien, Vol. III. 1851.


CHAPTER XV.


NERVOUS SYSTEM.


Origin of the Nervous System.

ONE of the most important recent embryological discoveries is the fact that the central nervous system, in all the Metazoa in which it is fully established, is (with a few doubtful exceptions) derived from the primitive epiblast 1 . As we have already seen that the epiblast represents to a large extent the primitive epidermis, the fact of the nervous system being derived from the epiblast implies that the functions of the central nervous system, which were originally taken by the whole skin, became gradually concentrated in a special part of the skin which was step by step removed from the surface, and has finally become in the higher types a well-defined organ imbedded in the subdermal tissues.

Before considering in detail the comparative development of the nervous system, it will be convenient shortly to review the present state of our knowledge on the general process of its evolution.

This process may be studied either embryologically, or by a comparison of the various stages in its evolution preserved in living forms. Both the methods have led to important results.

1 Whether there is any part of it in many types not so derived requires further investigation, now that it has been shewn by the Hertwigs that part of the system develops from the endoderm in some Coelenterata. O. Hertwig holds that part of it has a mesoblastic origin in Sagitta, but his observations on this point appear to me very inconclusive. It would be very advantageous to investigate the origin of . \ucrl >ach's plexus in Mammalia.


NERVOUS SYSTEM. 401


The embryological evidence shews that the ganglion-cells of the central part of the nervous system are originally derived from the simple undifferentiated epithelial cells of the surface of the body, while the central nervous system itself has arisen from the concentration of such cells in special tracts. In the Chordata at any rate the nerves arise as outgrowths of the central organ.

Another important fact shewn by embryology is that the central nervous system, and percipient portions of the organs of special sense, especially of optic organs, are often formed from the same part of the primitive epidermis. Thus the retina of the Vertebrate eye is formed from the two lateral lobes of the primitive fore-brain.

The same is true for the compound eyes of some Crustacea. The supracesophageal ganglia of these animals are formed in the embryo from two thickened patches of the epiblast of the procephalic lobes. These thickened patches become gradually detached from the surface, remaining covered by a layer of epidermis. They then constitute the supraoesophageal ganglia ; but they form not only the ganglia, but also the retinulae of the eye the parts in fact which correspond to the rods and cones in our own retina. The accessory parts of these organs of special sense, viz. the crystalline lens of the Vertebrate eye, and the corneal lenses and crystalline cones of the Crustacean eye, are independently formed from the epiblast after the separation of the part which becomes the central nervous system.

In the Acraspedote Medusae the rudimentary central nervous system has the form of isolated rings, composed of sense-cells prolonged into nervous fibres, surrounding the stalks of tentaclelike organs, at the ends of which are placed the sense-organs.

This close connection between certain organs of special sense and ganglia is probably to be explained by supposing that the two sets of structures actually originated part passu.

We may picture the process as being somewhat as. follows :

It is probable that in simple ancestral organisms the whole body was sensitive to light, but that with the appearance of pigment-cells in certain parts of the body, the sensitiveness to light became localised to the areas where the pigment-cells were present. Since, however, it was necessary that stimuli received by such organs should be communicated to other parts

B. III. 26


402 EVOLUTION OF THE NERVOUS SYSTEM.

of the body, some of the epidermic cells in the neighbourhood of the pigment-spots, which were at first only sensitive in the same manner as other cells of the epidermis, became gradually differentiated into special nerve-cells. As to the details of this differentiation embryology does not as yet throw any great light ; but from the study of comparative anatomy there are grounds for thinking that it was somewhat as follows: Cells placed on the surface sent protoplasmic processes of a nervous nature inwards, which came into connection with nervous processes from similar cells placed in other parts of the body. The cells with such processes then became removed from the surface, forming a deeper layer of the epidermis below the sensitive cells of the organ of vision. With the latter cells they remained connected by protoplasmic filaments, and thus they came to form a thickening of the epidermis underneath the organ of vision, the cells of which received their stimuli from those of the organ of vision, and transmitted the stimuli so received to other parts of the body. Such a thickening would obviously be the rudiment of a central nervous system, and is in fact very similar to the rudimentary ganglia of the Acraspeda mentioned above. It is easy to see by what steps it might become larger and more important, and might gradually travel inwards, remaining connected with the senseorgan at the surface by protoplasmic filaments, which would then constitute nerves. The rudimentary eye would at first merely consist of cells sensitive to light, and of ganglion-cells connected with them ; while at a later period optical structures, constituting a lens capable of throwing an image of external objects upon it, would be developed, and so convert the whole structure into a true organ of vision. It has thus come about that, in the development of the individual, the retina is often first formed in connection with the central nervous system, while the lenses of the eye are independently evolved from the epidermis at a later period.

A series of forms of the Ccelenterata and Platyelminthes affords us examples of various stages in the differentiation of a central nervous system 1 .

In sea-anemones (Hertwigs, No. 321) there are, for instance, no organs of special sense, and no definite central nervous system. There are, however, scattered throughout the skin, and also throughout the lining of the digestive tract, a number of specially modified epithelial cells, which are no doubt delicate organs of sense. They are provided at their free extremity with a long hair, and are prolonged on their inner side into fine processes which penetrate into the deeper part of the epithelial layer of the skin or digestive wall. They eventually join a fine network of protoplasmic fibres which forms a special layer immediately within the epithelium. The fibres of this network are no doubt essentially nervous. In addition to fibres there are,

1 Our knowledge on this subject is especially due to the brothers Hertwig (Nos. 320 and 321), Eimer (No. 318), Claus (No. 317), Schafer (No. 326), and Hubrecht (No. 323).


NERVOUS SYSTEM.


403



FIG. 236. NEUROEPITHELIALSENSECELLS OFAURELIA

AURITA. (From

Lankester ; after Schafer.)


moreover, present in the network cells of the same character as the multipolar ganglion-cells in the nervous system of Vertebrates, and some of these cells are characterised by sending a process into the superjacent epithelium. Such cells are obviously intermediate between neuroepithelial cells and ganglion-cells ; and it is probable that the nerve-cells are, in fact, sense-cells which have travelled inwards and lost their epithelial character.

In the Craspedote Medusae (Hertwigs, No. 320) the differentiation of the nervous system is carried somewhat further. There is here a definite double ring, placed at the insertion of the velum, and usually connected with sense-organs. The two parts of the ring belong respectively to the epithelial layers on the upper and lower surfaces of the velum, and are not separated from these layers ; they are formed of fine nerve-fibres and ganglion-cells. The epithelium above the nerve rings contains sense-cells (fig. 237) with a stiff hair at their free extremity, and a nervous prolongation at the opposite end, which joins the nervefibres of the ring. Between such cells and true ganglioncells an intermediate type of cell has been found (fig. 237 B) which sends a process upwards amongst the epithelial cells, but does not reach the surface. Such cells, as the Hertwigs have pointed out, are clearly sense-cells partially transformed into ganglioncells.

A still higher type of nervous system has been met with amongst some primitive Nemertines (Hubrecht, No. 323), consisting of a pair of large cephalic ganglia, and two well-developed lateral ganglionic cords placed close beneath the epidermis. These cords, instead of giving off definite nerves, as in animals with a fully differentiated nervous system, are connected with a continuous subdermal nervous plexus.

The features of the embryology and the anatomy of the nervous system, to which attention has just been called, point to the following general conclusions as to the evolution of the nervous system.

(1) The nervous system of the higher Metazoa appears to have been evolved in the course of a long series of generations from a differentiation of some of the superficial epithelial cells of the body, though it is possible that some parts of the system may have been formed by a differentiation of the alimentary epithelium.

(2) An early feature in the differentiation consisted in the growth of a series of delicate processes of the inner ends of

26 2


404


EVOLUTION OF THE NERVOUS SYSTEM.


certain epithelial cells, which became at the'same time especially differentiated as sense-cells (figs. 236 and 237).



FIG. 237. ISOLATED CELLS BELONGING TO THE UPPER NERVE-RING OF CARMARINA HASTATA. (After O. and R. Hertwig.)

A. Neuro-epithelial sense-cell, c. sense-hair.

B. Transitional cell between a neuro-epithelial cell and a ganglion -cell.

(3) These processes gave rise to a subepithelial nervous plexus, in which ganglion-cells, formed from sense-cells which travelled inwards and lost their epithelial character (fig. 237 B), soon formed an important part.

(4) Local differentiations of the nervous network, which was no doubt distributed over the whole body, took place partly in the formation of organs of special sense, and partly in other ways, and such differentiations gave rise to a central nervous system. The central nervous system was at first continuous with the epidermis, but became separated from it and travelled inwards.

(5) Nerves, such as we find them in the higher types, originated from special differentiations of the nervous network, radiating from the parts of the central nervous system.

The following points amongst others are still very obscure :

(1) The steps by which the protoplasmic processes from the primitive epidermic cells became united together so as to form a network of nervefibres, placing the various parts of the body in nervous communication.

(2) The process by which nerves became connected with muscles, so that a stimulus received by a nerve-cell could be communicated to and cause a contraction in a muscle.

It is probable, as stated in the above summary, that the nervous net


NERVOUS SYSTEM. 405



work took its origin from processes of the sense-cells. The processes of the different cells probably first met and then fused together, and, becoming more arborescent, finally gave rise to a complicated network.

The primitive relations between the nervous network and the muscular system are matters of pure speculation. The primitive muscular cells consist of epithelial cells with muscular processes (fig. 238), but the branches of the nervous network have not been traced into connection with FIG. 238. MYO-EPITHELIAL

the muscles in any Ccelenterata except CELLS OF HYDRA. (From Gegenthe Ctenophora. In the higher types a baur 5 after Kleinenberg.) continuity between nerves and muscles ' contractile fibres; processes

in the form of motorial end plates has

been widely observed. Even in the case of the Ccelenterata it is quite clear from Romanes' experiments that stimuli received by the nerves are capable of being transmitted to the muscles, and that there must therefore be some connection between nerves and muscles. How did this connection originate?

Epithelial cells with muscular processes (fig. 238) were discovered by Kleinenberg (No. 324) in Hydra before epithelial cells with nervous processes were known, and Kleinenberg pointed out that Hydra shewed the possibility of nervous and muscular tissues existing without a central nervous system, and suggested that the epithelial part of the myo-epithelial cells was a sense-organ, and that the connecting part between this and the contractile processes was a rudimentary nerve. He further supposed that in the subsequent evolution of these elements the epithelial part of the cell became a ganglion-cell, while the part connecting this with the muscular tail became prolonged so as to form a true nerve. The discovery of neuro-epithelial cells existing side by side with myo-epithelial cells demonstrates that this theory must in part be abandoned, and that some other explanation must be given of the continuity between nerves and muscles. The hypothetical explanation which most obviously suggests itself is that of fusion.

It seems quite possible that many of the epithelial cells of the epidermis and walls of the alimentary tract were originally provided with processes, the protoplasm of which, like that of the Protozoa, carried on the functions of nerves and muscles at the same time, and that these processes united amongst themselves into a network. Such cells would be very similar to Kleinenberg's neuro-muscular cells. By a subsequent differentiation some of the cells forming this network may have become specially contractile, the epithelial parts of the cells ceasing to have a nervous function, and other cells may have lost their contractility and become solely nervous. In this way we should get neuro-epithelial cells and myo-epithelial cells both differentiated from the primitive network, and the connection between the two would also be explained. This hypothesis fits in moreover very well with the condition of the neuro-muscular system as we find it in the Coelenterata.


406 INVERTEBRATA.


BIBLIOGRAPHY. Origin of the Nervous System,

(316) F. M. Balfour. " Address to the Department of Anat. and Physiol. of the British Association." 1880.

(317) C. Claus. "Studien lib. Polypen u. Quallen d. Adria. I. Acalephen, Discomedusen." Denk. d. math.-naturwiss. Classe d. k. Akad. Wiss. Wien, Vol. xxxvin. 1877.

(318) Th. Eimer. Zoologische Studien a, Capri. I. Ueber Beroe ovatus, Ein Beitrag 2. Anat. d. Rippenquallen. Leipzig, 1873.

(319) V. Hen sen. " Zur Entwicklung d. Nervensystems. " Virchmifs Archiv, Vol. xxx. 1864.

(320) O. and R. Hertwig. Das Nerveiisystem u. d. Sinnesorgane d. Medusen. Leipzig, 1878.

(321) O. and R. Hertwig. "Die Actinien anat. u. histol. mit besond. Beriicksichtigung d. Nervenmuskelsystem untersucht." Jenaische Zeit., Vol. xin. 1879.

(322) R. Hertwig. "Ueb. d. Bau d. Ctenophoren." Jenaische Zeitschrift, Vol. xiv. 1880.

(323) A. W. Hubrecht. "The Peripheral Nervous System in Palaeo- and Schizonemertini, one of the layers of the body- wall." Quart. J. of After. Science, Vol. xx. 1880.

(324) N. Kleinenberg. Hydra, eine anatomisch-entwicklungsgeschichtliche Untersuchung. Leipzig, 1872.

(325) A. Kowalevsky. " Embryologische Studien an Wurmern u. Arthropoden." Mem. Acad. Petersbourg, Series VII., Vol. XVI. 1871.

(326) E. A. Schafer. "Observations on the nervous system of Aurelia aurita." Phil. Trans. 1878.

Nervous system of the Invertebrata. Our knowledge of the development of the central nervous system is still very imperfect in the case of many Invertebrate groups. In the Echinodermata and some of the Ghaetopoda it is never detached from the epidermis, and in such cases its origin is clear without embryological evidence.

In the majority of groups the central nervous system may be reduced to the type of a pair of cephalic ganglia, continued posteriorly into two cords provided with nerve-cells, which may coalesce ventrally or be' more or less widely separated, and be unsegmented or segmented. Various additional visceral ganglia may be added, and in different instances parts of the system may be much reduced, or peculiarly modified. The nervous system of the Platyelminthes (when present), of the Rotifera, Brachiopoda, Polyzoa (?), the Mollusca, the Chaetopoda, the


NERVOUS SYSTEM. 407


Discophora, the Gephyrea, the Tracheata, and the Crustacea, the various small Arthropodan phyla (Pcecilopoda, Pycnognida, Tardigrada, &c.), the Chaetognatha (?), and the Myzostomea, probably belongs to this type.

The nervous system of the Echinodermata cannot be reduced to this form ; nor in the present state of our knowledge can that of the Nematelminthes or Enteropneusta.

It is only in the case of members of the former set of groups that any adequate observations have yet been made on the development of the nervous system, and even in the case of these groups observations which have any claim to completeness are confined to certain members of the Chaetopoda, the Arthropoda and the Mollusca. An account of imperfect observations on other forms, where such have been made, will be found in the systematic part of this work.

Chaetopoda. We are indebted to Kleinenberg (No. 329) for the most detailed account which we have of the development of the central nervous system in the Chaetopoda.

The supracesophageal ganglion with the cesophageal commissure developes independently of the ventral cord. It arises as an unpaired thickening of the epiblast, p IG- 239 . SECTION close to the dorsal side of the oesophagus THROUGH THE HEAD OF

A 'YOUNG EMBRYO OF

at the front end of the head (fig. 239), LUMBRICUS TRAPEZOIDES. which becomes separated from the epi- < After Kleinenber s-)

, e.g. cephalic ganglion ;

blast, and extends obliquely backwards CCi cephalic portion of the and downwards in a somewhat arched body cavity ;*. oesophagus. form ; its lower extremities being somewhat swollen. The inner portion of this curved rudiment becomes converted into commissural nerve-fibres, while the cells of the outer and upper portion assume the characters of ganglion-cells. The commissural fibres are continued downwards to meet the ventral chord, but their junction with the latter structure is not effected till late in embryonic life.

The ventral cord is formed by the coalescence of a pair of linear cords, the development of which takes place from before backwards, so that when their anterior part is well developed their posterior part is hardly differentiated. These cords arise, one on



408


CH^TOPODA.



FIG. 240. SECTION THROUGH PART OF THE VENTRAL WALL OF THK TRUNK OF AN EMBRYO OF LUMBRIcus TRAPEZOIDES. (After Kleinenberg.)

m. longitudinal muscles ; so. somatic mesoblast ; sp. splanchnic mesoblast; hy. hypoblast; Vg- ventral nerve-cord; w. ventral vessel.


each side of a ventral ciliated furrow, first as a single row of epiblast cells, and subsequently as several rows (fig. 240, Vg). While still united to the external epiblast, they extend themselves below the cells lining the ventral furrow, and unite into a single nervous band, which however exhibits its double origin by its bilobed section. Before the two cords unite, the groove between them becomes somewhat deep, but subsequently shallows out and disappears. The nervous band, before separating from the epiblast, exhibits, in correspondence with the mesoblastic segments, alternate swellings and constrictions. The former become the ganglia, and the latter the connecting trunks.

As soon as the cord becomes free from the epiblast, it becomes surrounded by a sheath, formed of somatic mesoblast. In each of the ganglionic enlargements there next appears on the dorsal surface a pair of areas of punctiform material, the substance of which soon differentiates itself into .nerve-fibres. These areas, by uniting from side to side, give rise to the transverse commissures, and also by a linear coalescence to the longitudinal commissures of the cord. The cellular parts of the band surrounding them become converted into a ganglionic covering of the cord.

In each ganglion the cells of this ganglionic investment penetrate as a median septum into the cord. A fissure is next formed, dividing this septum into two ; it is subsequently continued for the whole length of the cord.

Arthropoda. In the Tracheata and the Crustacea the development of the ventral cord is in the main similar to that in the Chaetopods, while that of the supracesophageal ganglia is as a rule somewhat more complicated. No such clear evidence of an independent development of these two parts, as in the case of the Chaetopods, has as yet been produced.

The most primitive type of nervous system amongst the


NERVOUS SYSTEM. 409


Tracheata is that of Peripatus, where it consists of large supraoesophageal ganglia, continuous with a pair of widely separated but large ventral cords united posteriorly above the anus. These cords have an investment of ganglion- cells for their whole length, and are imperfectly divided into ganglia corresponding in number with the feet.

The ventral cords are formed as two separate epiblastic ridges (fig. 241, v.n], continued in front into a pair of thickenings



FIG. 241. SECTION THROUGH THE TRUNK OF AN EMBRYO OF PERIPATUS. The embryo from which the section is taken was somewhat younger than that of fig. 242.

sp.m. splanchnic mesoblast ; s.m. somatic mesoblast ; me. median section of body cavity ; Ic. lateral section of body cavity ; -v. 11. ventral nerve cord ; me. mesenteron.

of the procephalic lobes, which are at first independent of each other, and from which a large part of the supracesophageal ganglia takes its origin. . After the latter have become separated from the epiblast an invagination of the epiblast covering them grows into each lobe (fig. 242), and becoming constricted from the superficial epiblast, which remains as the epidermis, forms a not unimportant part of the permanent supracesophageal ganglia.

In the Arachnida the mode of development of the nervous system is essentially the same, and the reader will find a detailed account of it for Spiders in Vol. II. pp. 447 451. The ventral cords are here formed as independent and at first widely separated strands (fig. 243, vii), which for a long time remain far apart ; they are subsequently divided into ganglia and become united by transverse commissures.

The supracesophageal ganglia are formed as two independent


4io


ARTHROPODA.


thickenings of the procephalic lobes (fig. 244), which eventually separate from the superficial skin. There is formed however in



FIG. 242. HEAD OF AN EMBRYO PERIPATUS. (From Moseley.) The figure shews the jaws (mandibles), and close to them epiblastic involutions, which grow into the supracesophageal ganglia. The antennas, oral cavity, and oral papillae are also shewn.

each of them a semicircular groove (fig. 244, gr) lined by the superficial epiblast, which becomes detached from the skin, and is involuted to form part of the ganglia.

A similar mode of formation of both the ventral cords and the supraoesophageal ganglia obtains in Insects (fig. 245). The



FIG. 243. TRANSVERSE SECTION THROUGH THE VENTRAL PLATE OF AGELENA

LABYRINTHICA.

The ventral cords have begun to be formed as thickenings of the epiblast, and the limbs are established.

me.s. mesoblastic somite; vn. ventral nerve-cord; yk. yolk.

ventral cords are however much less widely separated than in Spiders, and early unite in the median line. In the supraoesophageal ganglia the invaginated epiblast has in Lepidoptera (Hatschek) the form of a pit on the dorsal border of the antennae.


NERVOUS SYSTEM.


Hatschek states that there takes place an invagination of a median part of the skin between the two ventral cords, for the details of which I must refer the reader to Vol. II. p. 410. He has made more or less similar statements for the earthworm, but his observations in both instances are open to serious doubt.


ce.s



FIG. 244. SECTION THROUGH THE PROCEPHALIC LOBES OF AN EMBRYO OF

AGELENA LABYRINTHICA.

st. stomadaeum; gr. section through semi-circular groove in procephalic lobe; ce.s. cephalic section of body cavity.

Full details as to the development of the nervous system in the Crustacea are still wanting ; a fairly complete account of


nie.s



FlG. 245. TWO TRANSVERSE SECTIONS THROUGH THE EMBRYO OF HYDROPHILUS.

(After Kowalevsky.)

A. Transverse section through an embryo in the region of one of the stigmata.

B. Transverse section through an older embryo.

vn. ventral nerve-cord ; am. amnion and serous membrane ; me. mesoblast ; me.s. somatic mesoblast; hy. hypoblast (?) ; yk. yolk-cells (true hypoblast); st. stigma of trachea.


412 GEPHYREA.


what is known on the subject is given in Vol. n. pp. 521 2. It appears that the ventral cord may either arise as an unpaired thickening of the epiblast (Isopoda), marked however by a shallow median furrow, or from two cords which eventually coalesce 1 . It is not certain how far the supracesophageal ganglia are usually in the first instance continuous with the ventral cord. In Astacus, the early stages of which have been elaborately investigated by Reichenbach (No. 331), they are stated to be so ; the supracesophageal ganglia are moreover described by this author as having a somewhat complicated origin. Five elements enter into their composition. There is first formed a pair of pits on the procephalic lobes, which become very deep during the Nauplius stage, and are continuous with a pair of epiblastic ridges which pass round the mouth, and join the ventral cords just described. The walls of the pits are believed to form a part of the embryonic ganglia which gives rise to the retina as well as to the optic ganglia. The ridges form the remainder of the ganglia and the cesophageal commissures ; while the fifth element is supplied by a median invagination in front of the mouth, which appears at a much later date than the other parts.

In the Isopoda supracesophageal ganglia are stated to arise as thickenings of the procephalic lobes, which become eventually detached from the epidermis.

The ventral cord is at first unsegmented, but soon becomes partially divided by a series of constrictions into a number of ganglia, corresponding with the segments. The development of the commissural and ganglionic portions takes place much as in the Chaetopoda.

The Gephyrea approach closely the types so far dealt with, but the ventral cord in the Inermia is formed as an unpaired thickening of the epiblast. In Echiurus, as has been shewn by Hatschek in an interesting paper on the larva of this species, published since the appearance of the first volume, there is a pair of ventral cords 2 . In correspondence with a general segmentation of the body, which is subsequently lost, these cords become

1 Reichenbach (No. 331) holds that the walls of the groove between the two strands of the ventral cords become invaginated and assist in the formation of the ventral cord.

8 " Ueber Entwicklungsgeschichte d. Echiurus." Arbeit, a. d. zool. Instit. Wien Vol. ill. 1880.


NERVOUS SYSTEM.


4'3


segmented. The two cords unite in the median line, and Hatschek, in accordance with his general view on this subject, states that their junction is effected by means of a median cord of invaginated epiblast. The segmentation of the cords subsequently becomes lost. The supracesophageal ganglia arise as an unpaired median thickening of the procephalic lobe. No traces of segmentation in the ventral cord have been observed by Spengel in Bonellia, and the supracesophageal ganglion is formed in this genus as an unpaired band.


In all the groups above considered the nervous system clearly presents the same type of development with various modifications.

It is formed of two parts, viz. (i) the supracesophageal ganglia, and (2) the ventral cord.

In the simpler forms, Chaetopoda and Gephyrea, the supracesophageal ganglia are usually stated to be formed as an unpaired thickening at the apex of the praeoral lobe, which in most cases becomes subsequently bilobed.

In the Arthropoda the unpaired praeoral lobe of the Chaetopoda is replaced by the so-called procephalic lobes, which are themselves bilobed ; and the supracesophageal ganglia are formed of two independent halves ; further complications in development are also generally found.

There is not as yet sufficient evidence to decide whether the supracesophageal ganglia were primitively developed continuously with, or independently of, the ventral cords.

The ventral cord appears in the embryo as two independent unsegmented strands, although in a few cases (some Crustacea and Gephyrea) these cords, by an abbreviation in development, arise as an unpaired median thickening of the epiblast.

The form of nervous system of the Chaetopoda, Arthropoda, and Gephyrea is clearly therefore to be derived, as was first pointed out by Gegenbaur, from a more or less similar type to that now found in the Nemertines ; and as suggested in the chapter on larval forms (vide p. 378) may perhaps be derived from the elongation of a circular ring, of which the anterior end has become developed into the supracesophageal ganglia, the lateral parts into the two lateral strands, while the posterior part persists in some forms in the junction of the ventral cords above the anus (Enopla and Peripatus).


414 MOLLUSCA.


Mollusca. While study of the anatomy of the nervous system of the Mollusca, especially of certain primitive genera (Chiton, Haliotis, Fissurella, &c.) leaves little doubt that it is formed on the same type as that of the groups just spoken of, the development, so far as our imperfect knowledge enables us to make definite statements on the subject, is somewhat abnormal 1 .

In the Gasteropoda and Pteropoda the supracesophageal ganglia appear most probably to be developed either as paired thickenings of the epiblast of the velar area, or as invaginated pits of the velar area, which become detached from the surface, and then become solid (Hyaleacea and Limax). In either case the supracesophageal ganglia appear to be developed quite independently of the pedal ganglia. The latter, as might be anticipated, are earlier in their development and more constant than the various visceral ganglia ; and, if the views above expressed are correct, are homologous with the ventral cord of the Chaetopods and Arthropods. Their actual development is very imperfectly known.

The most precise statements on the subject, viz. those of Bobretzky and Fol, would lead us to suppose that they arise in the mesoblast, but it seems more probable that they are formed as thickenings of the sides of the foot.

In the Cephalopods all the ganglia are stated to be differentiated in the mesoblast (Lankester, Bobretzky).

Hatschek 2 has recently given a detailed description of the development of the supracesophageal and pedal ganglia of Teredo. He finds that the former ganglia arise as an unpaired thickening of the epiblast in the centre of the velar area, and the latter as an unpaired thickening of the epiblast of the ventral side of the body between the mouth and the anus. The two ganglia would thus seem to be disconnected with each other in their development.

(327) F. M. Balfour. "Notes on the development of the Araneina." Quart. J. of Micr. Science, Vol. XX. 1880.

(328) B. Hatschek. " Beitr. z. Entwicklung d. Lepidopteren." Jenaische Zeitschrift, Vol. xi. 1877.

(329) N. Kleinenberg. "The development of the Earthworm, Lumbricus Trapezoides." Quart. J. of Micr. Science, Vol. XIX. 1879.

(330) A. Kowalevsky. " Embryologische Studien an Wiirmem u. Arthropoden." Mem. Acad. Petersbourg, Series vin., Vol. XVI. 1871.

(331) H. Reichenbach. " Die Embryonalanlage u. erste Entwick. d. Flusskrebses." Zeit.f. wiss. Zool., Vol. xxix. 1877.

1 Vide Vol. ii., pp. 273, 274.

2 " Ueber Entwicklungsgeschichte von Teredo." Arbeit, a. d. zool. Instit, IVieit, Vol. in. 1880.


NERVOUS SYSTEM OF THE VERTEBRATA. 415


THE CENTRAL NERVOUS SYSTEM OF THE VERTEBRATA 1 .

The formation of the cerebro-spinal axis of the Chordata from the medullary plate has already been treated at length (pp. 301 304). Before entering into the consideration of the morphological value of the various parts of this cord, it will be convenient to describe the more important features of its ontogeny. For this purpose the two parts into which the nervous axis becomes at an early period divided, viz. the spinal cord and the brain, may be dealt with separately.

The Spinal Cord, shortly after the closure of the medullary canal, has, in all the true Vertebrata, the form of an oval tube ; the walls of which are of a fairly uniform thickness, and are composed of several rows of elongated cells. This cord, as development proceeds, usually becomes vertically prolonged in transverse section, and the central canal which it contains also becomes vertically elongated. The variations in shape of the spinal canal are very great at different periods and in different parts of the body, and an attempt to chronicle them would appear, in the present state of our knowledge, to be quite valueless' 2 . Fig. 117, in which the spinal cord of the chick of the third day is shewn in transverse section, illustrates the character of the cord at the stage just described. Up to this time the walls of the spinal canal have exhibited an uniform structure. A series of changes now however takes place, which results in the differentiation (i) of the epithelium of the central canal, (2) of the grey matter of the cord, and (3) of the external coating of white matter.

The relative time at which each of these parts becomes developed is not constant in the different forms.

The white matter is apparently the result of a differentiation of the outermost parts of the superficial cells of the cord into

1 For the development of the central nervous system in Amphioxus and the Tunicata the reader is referred to the chapters dealing with those two groups.

2 Lowe (No. 341) holds that at an early stage of development three regions can always be distinguished in any section of the central canal, viz. (i) a ventral narrow slit, (2) a median enlargement, and (3) a dorsal slit. Such a form can no doubt often be observed, but my own observations do not lead me to attach any special importance to it.


41 6 SPINAL CORD.


longitudinal nerve-fibres, which remain for a long period without a medullary sheath. These fibres appear in transverse sections as small dots. The white matter forms a transparent investment of the grey matter and would seem to contain neither nuclei nor cells 1 . The white matter may from the first form only two masses, one on each side, forming a layer on the ventral and lateral parts of the spinal cord but not extending to the dorsal surface (Elasmobranchii, fig. 185, W) ; or it may form four patches, viz. an anterior and a posterior white column on each side, which lie on a level with the origin of the anterior and



c


FIG. 246. SECTION THROUGH THE SPINAL CORD OF A SEVEN DAYS' CHICK.

pew. dorsal white column ; lew. lateral white column ; acw. ventral white column ; c. dorsal tissue filling up the part where the dorsal fissure will be formed ; pc. dorsal grey cornu ; ac. anterior grey cornu; ep. epithelial cells; age. anterior commissure; pf. dorsal part of spinal canal ; spc. ventral part of spinal canal ; af. anterior fissure.

posterior nerve-roots (the Fowl, Human embryo, etc.). In whichever of these forms the white matter appears, it is always, at first, a layer of extreme tenuity, which rapidly increases

1 This holds true at first for Elasmobranchii, but at a later stage there are present numerous nerve-cells in the white matter, so that the distinction between the white and grey matter becomes much less marked than in higher types; in this respect Elasmobranchii present an approximation to Amphioxus.


NERVOUS SYSTEM OF THE VERTEBRATA. 417

in thickness in the subsequent stages, and extends so as gradually to cover the whole cord (fig. 246).

The anterior white commissure is formed very shortly after the first appearance of the white matter. The grey matter and the central epithelium are formed by a differentiation of the main mass of the spinal cord. The outer cells lose their epithelial-like arrangement, and, becoming prolonged into fibres, give rise to the grey matter, while the innermost cells retain their primitive arrangement, and constitute the epithelium of the canal. The process of formation of the grey matter would appear to proceed from without inwards, so that some of the cells, which have, on the formation of the grey matter, an epithelial-like arrangement, subsequently become converted into true nerve-cells.

As has already been mentioned, the central epithelium of the nervous system probably corresponds with the so-called epidermic layer of the epiblast.

The grey matter soon becomes prolonged dorsally and ventrally into the posterior and anterior horns. Its fibres may especially be traced in two directions: (i) round the anterior end of the spinal canal, immediately outside its epithelium and so to the grey matter on the opposite side, forming in this way an anterior grey commissure, through which a decussation of the fibres from the opposite sides is effected : (2) dorsalwards along the outside of the lateral walls of the canal.

There is at this period no trace of the ventral or dorsal fissure, and the shape of the central canal is not very different to what it was at an earlier period. This condition of the spinal cord is especially instructive, as it is very nearly that which is permanent in Amphioxus.

The next event of importance is the formation of the ventral or anterior fissure. This owes its origin to a downgrowth of the anterior horns of the cord on each side of the middle line. The two downgrowths enclose between them a somewhat linear space the anterior fissure which increases in depth in the succeeding stages (fig. 246, af}.

The dorsal or posterior fissure is formed at a later period than the anterior, and accompanies the atrophy of the dorsal section of the embryonically large canal of the spinal cord. B. III. 2 7


41 8 SPINAL CORD.


The exact mode of its formation appears to me to be still involved in some obscurity.

In the Elements of Embryology the development of the posterior fissure was described in the following way :

" On the seventh day the most important event is the formation of the posterior fissure,

" This is brought about by the absorption of the roof of the posterior of the two parts into which the neural canal has become divided.

"Between the posterior horns of the cord, the epithelium forming the roof of the, so to speak, posterior canal is along the middle line covered neither by grey nor by white matter, and on the seventh day is partially absorbed, thus transforming the canal into a wedge-shaped fissure, whose mouth however is seen in section to be partially closed by a triangular clump of elongated cells (fig. 246, c]. Below this mass of cells the fissure is open. It is separated from the 'true spinal canal' by a very narrow space along which the side walls have coalesced. In the lumbar and sacral regions the two still communicate.

"We thus find, as was first pointed out by Lockhart Clarke, that the anterior and posterior fissures of the spinal cord are, morphologically speaking, entirely different. The anterior fissure is merely the space left between two lateral downward growths of the cord, while the posterior fissure is part of the original neural canal separated from the rest of the cavity (which goes to form the true spinal canal) by a median coalescence of the side walls."

I confess that I have some doubts as to the complete accuracy of the above statement.

Kolliker gives a full account of the gradual atrophy of the central canal ; but I do not fully understand his statements with reference to the formation of the posterior fissure, which in fact appears to be only incidentally mentioned. It would seem from his account that a shallow and somewhat wide dorsal fissure is formed to start with, in the human embryo, by two projections of the posterior white horns. On the atrophy of the central canal this furrow becomes narrowed, but Kolliker does not definitely state how it becomes deepened so as to give rise to the permanent dorsal fissure.

It seems to me probable, though further investigations on the point are still required, that the dorsal fissure is a direct result of the atrophy of the dorsal part of the central canal of the spinal cord.

The walls of the canal coalesce dorsally, and the coalescence gradually extends ventralwards, so as finally to reduce the central canal to a minute tube, formed of the ventral part of the original canal. The epithelial wall formed by the coalesced walls on the dorsal side of the canal is gradually absorbed.

The epithelium of the central canal, at the period when its


NERVOUS SYSTEM OF THE VERTEBRATA. 419

atrophy commences, is not covered dorsally either by grey or white matter, so that, with the gradual reduction of the dorsal part of the canal, and the absorption of the epithelial wall formed by the fusion of its two sides, a fissure between the two halves of the spinal cord becomes formed. This fissure is the posterior or dorsal fissure. In the process of its formation the white matter of the dorsal horns becomes prolonged so as to line its walls ; and shortly after its formation the dorsal grey commissure makes its appearance, which is not improbably derived from part of the epithelium of the original central canal.

Development of the Brain.

The brain is formed from the anterior portion of the medullary plate. When the medullary plate first becomes differentiated it is not possible to distinguish between the region of the brain and that of the spinal cord. The brain region is however usually very early indicated by a widening of the medullary plate, but does not become sharply marked off from the region of the spinal cord. In many Ichthyopsida (Elasmobranchii (fig. 28, C) and Amphibia (fig. 77, A)) the anterior dilatation gives to the medullary plate, before its sides meet to form a canal, a spatula-like form ; which is either not present or less marked in Reptilia, Aves and Mammalia.

The length of the brain as compared to the spinal cord is always very great in the embryo, and in the earliest developmental periods the disproportion in the size of the brain is specially marked, owing to the full number of the somites of the trunk not having been formed. In Elasmobranchii the brain is about one-third of the whole length of the embryo at the stage immediately following the closure of the medullary canal.

The first differentiation of the brain into distinct parts is a very early occurrence, and may take place before (Mammalia) or during the closure of the medullary folds. The brain first becomes divided into two successive lobes or vesicles by a single transverse constriction, and subsequently the posterior of these again 'becomes divided into two, so that three lobes

272


42O


THE BRAIN.


are formed known as the fore- the mid- and the hind-brain ; of these the hind-brain is usually the longest. In some instances a bilobed stage can hardly be recognised. This primitive division of the brain is shewn in many of the figures already given. The reader may perhaps best refer to fig. 108. On the closure of the medullary groove the lumen of the medullary canal is continued uninterruptedly through the brain, but dilates considerably in each of the cerebral vesicles.

The anterior lobe of the brain becomes converted into the cerebral hemispheres, the thalamencephalon, the primary optic vesicles, and the parts connected with them. The middle lobe becomes the optic lobes (corpora bigemina or corpora quadrigemina in Mammalia) and the crura cerebri ; while the posterior lobe becomes converted into the cerebellum and medulla oblongata.

Before describing in detail the changes by which the primary vesicles of the brain become converted into the above parts, it will be convenient to say a few words about the general development of the brain.

The most striking peculiarity with reference to the general development of the brain is a curvature which appears in its axis, known as the cranial flexure. The flexure takes place through the mid-brain ; and causes the fore-brain to be gradually bent downwards so that the axis of its floor forms, first, a right angle with that of the hinder part of the brain, and subsequently, as a rule, an acute angle.

During these changes the brain, in most Amniota at any rate, becomes in the first instance retort-shaped, the cerebral vesicle forming the swollen part of the retort, but subsequently the retort-shape is lost owing to the great development of the vesicle of the mid-brain, which forms the termination of the long axis of the embryo. Figs. 29, 76,



FIG. 247. LONGITUDINAL SECTION THROUGH THE BRAIN OF A YOUNG PRISTIURUS EMBRYO.

cer. commencement of the cerebral hemisphere ; pn. pineal gland ; In. infundibulum ; pt. ingrowth from mouth to form the pituitary body ; mb. mid-brain ; cb. cerebellum ; ch. notochord. ; al. alimentary tract ; laa. artery of mandibular arch.


NERVOUS SYSTEM OF THE VERTEBRATA.


421


mb


pn.



and 1 1 8, are representative figures of embryos of various vertebrate forms at a period when the mid-brain forms the termination of the long axis of the body.

It is generally stated that the cranial flexure is at its maximum at the stage represented in these figures, and there can be no doubt that viewed from the exterior the cranial flexure ceases to be so marked a feature, and finally disappears as the embryo gradually grows older ; but though the mid-brain ceases to form the termination of the long axis of the embryo, the flexure of the brain becomes in many forms absolutely more marked ; while in other forms, though stated to diminish, it does not entirely vanish.

The general nature of the changes which take place will perhaps best be understood by a comparison of figs. 247 and 248 representing longitudinal sections at two stages through the brain of an embryo Elasmobranch. The actual cranial flexure, i.e. flexure of the floor of the brain, is obviously greater in the older of the two brains, though viewed from the exterior the axis of this brain appears to be quite straight. In the younger stage, fig. 247, the midbrain (mb) forms the end of the long axis of the body, while in the older one the cerebral hemispheres (cer) have grown very greatly, especially forwards and dorsalwards. They have thus come to lie in front of the mid-brain, and to form the end of the long axis of the body, and have at the same time compressed the originally large thalamencephalon against the mid-brain. The same general features may be seen in fig. 250 representing a longitudinal section of the brain of an embryo fowl, and fig. 255 representing a longitudinal section of the brain of a Mammal.


FIG. 248. LONGITUDINAL SECTION THROUGH THE BRAIN OF SCYLLIUM CANICULA AT AN ADVANCED STAGE OF DEVELOPMENT.

cer. cerebral hemisphere ; pn. pineal gland ; op.th. optic thalamus, connected with its fellow by a commissure (the middle commissure). In front of it is seen a fold of the roof of the forebrain, which is connected with the choroid plexus of the third ventricle ; op. optic chiasma ; //. pituitary body ; in. infundibulum ; cb. cerebellum ; ati.v. passage leading from the auditory vesicle to the exterior ; mel. medulla oblongata ; c.in. internal carotid artery.


422 HISTOGENESIS OF THE BRAIN.

The infundibulum or perhaps rather the point of origin of the optic nerves is to be regarded as the anterior termination of the axis of the base of the brain.

The cranial flexure is least marked in Cyclostomata (fig. 253), Teleostei, Ganoidei, and Amphibia, while it is very pronounced in Elasmobranchii, Reptilia, Aves, and Mammalia. In Teleostei, and still more in Cyclostomata, it permanently remains slight, owing to the small development of the cerebral hemispheres.

In addition to the cranial flexures, two other flexures make their appearance in the base of the brain. A posterior at the junction of the brain and spinal cord, and an anterior at the boundary between the cerebellum and medulla oblongata, just at the point where the pons Varolii is formed in Mammalia. The anterior of these is the most marked and constant ; it is shewn in fig. 250. It arises considerably later than the main cranial flexure, and since it is turned the opposite way it assists to a considerable extent in causing the apparent straightening of the cranial axis.

Histogenetic changes 1 . The walls of the brain are at first very thin and, like those of the spinal cord, are formed of a number of ranges of spindle-shaped cells. The processes of each of these cells are stated to be continued through the whole thickness of the wall. In the floor of the hind- and mid-brain a superficial layer of delicate nerve-fibres is formed at an early period. This layer appears in the first instance on the floor and sides of the hind-brain, and very slightly, if at all, later on the floor and the sides of the mid-brain. The cells internal to the nerve-fibres become differentiated into an innermost epithelial layer lining the cavities of the ventricles, and an outer layer of grey matter.

The similarity of the primitive arrangement and histological character of the parts of the brain behind the cerebral hemispheres to that of the spinal cord is very conclusively shewn by the examination of any good series of sections. In both brain and spinal cord the white matter forms a cap on the ventral and lateral parts considerably before it extends to the dorsal surface. In the medulla the white matter does not eventually extend to the roof owing to the peculiar degeneration which that part undergoes.

1 It is not within the scope of this work to give an account of the histogenesis of the brain; in the statement in the text only a few points, of some morphological importance, are touched on.


NERVOUS SYSTEM OF THE VERTEBRATA. 423

In the case of the fore-brain the earliest histological changes, except possibly in Mammals, take place on the same general plan as those of the remainder of the central nervous system 1 ; but though the general plan is the same, yet the early histological distinction between the fore-brain, and the mid- and hindbrain is more marked than the distinction between the latter and the spinal cord.

On the floor and sides of the thalamencephalon, and apparently the whole of the hemispheres of the lower types, there is formed, somewhat later than in the remainder of the brain, a very delicate layer of white matter. The inner part of the wall, which still remains comparatively thin, is not at first clearly divided into an epithelial and nervous layer. This distinction soon however becomes more or less apparent, though it is not so marked as in most other parts of the brain ; and it appears that in the subsequent growth the greater part of the original epithelial layer becomes converted into nervous tissue.

In Mammals the same plan of differentiation would seem to be followed, though somewhat less obviously than in the lower types. The walls of the hemispheres become first divided (Kolliker) into a superficial thinner layer of rounded elements, and a deeper and thicker epithelial layer, and between these the fibres of the crura cerebri soon interpose themselves. At a slightly later period a thin superficial layer of white matter, homologous with that of the remainder of the brain, becomes established.

The inner layer, together with the fibres from the crura cerebri, gives rise to the major part of the white matter of the hemispheres and to the epithelium lining the lateral ventricles.

The outer layer of rounded cells becomes divided into (i) a superficial part with comparatively few cells, which, together with its coating of white matter, forms the cortical part of the grey matter, and (2) a deeper layer with numerous cells which forms the main mass of the grey matter of the hemispheres.

The development of the several parts of the brain will now be described.

1 I have worked out these changes in Elasmobranchii, Amphibia (Salamandra) and Aves.


424


THE HIND-BRAIN.


The hind-brain. The hind-brain is at first an elongated, funnel-shaped tube, the walls of which are of a nearly uniform thickness, though the roof and floor are somewhat thinner than the sides. It forms a direct continuation of the spinal cord, into which it passes without any sharp line of demarcation. The ventricle it contains is known as the fourth ventricle.

The sides become in the chick marked by a series of transverse constrictions, dividing it into lobes, which are somewhat indefinite in number. The first of these remains permanent, and its roof gives rise to the cerebellum. It is uncertain whether the other constrictions have any morphological significance. More or less similar constrictions are present in Teleostei. In Elasmobranchii the medulla presents on its inner face at a late period a series of lobes corresponding with the roots of the vagus and glossopharyngeal nerves, and it is possible that the earlier constrictions may potentially correspond to so many nerve-roots.

Throughout the Vertebrata an anterior lobe of the hindbrain becomes very early marked off, so that the primitive hind-brain becomes divided into two regions which may be



cc


AOA


FIG. 249. SECTION THROUGH THE HIND -BRAIN OF A CHICK AT THE END OF THE THIRD DAY OF INCUBATION.

IV. Fourth ventricle. The section shews the very thin roof and thicker sides of the ventricle. Ch. Notochord ; CV. Anterior cardinal vein; CC. Involuted auditory vesicle ; CC points to the end which will form the cochlear canal ; RL. Recessus labyrinth! (remains of passage connecting the vesicle with the exterior) ; hy. Hypoblast lining the alimentary canal; AO., AOA. Aorta, and aortic arch.


NERVOUS SYSTEM OF THE VERTEBKATA. 425

conveniently spoken of as the cerebellum (figs. 247 and 248, cb) and medulla oblongata. The floor of these regions is quite continuous and is also prolonged without any break into the floor of the mid-brain.

The posterior section of the hind-brain, which forms the medulla, undergoes changes of a somewhat complicated character. In the first place its roof becomes in front very much extended and thinned out. At the raphe, where the two lateral halves of the brain originally united, a separation, as it were, takes place, and the two sides of the brain become pushed apart, remaining united by only a very thin layer of nervous matter, consisting of a single row of flattened cells (fig. 249). As a result of this peculiar growth in the brain, the roots of the nerves of the two sides, which were originally in contact at the dorsal summit of the brain, become carried away from one another, and appear to arise at the sides of the brain.

The thin roof of the fourth ventricle is triangular, or, in Mammalia, somewhat rhomboidal in shape. The apex of the triangle is directed backwards.

At a later period the blood-vessels of the pia mater form a rich plexus over the anterior part of the thin roof of the medulla, which becomes at the same time somewhat folded. The whole structure is known as the tela vasculosa, or choroid plexus of the fourth ventricle (fig. 250, chd 4). The floor of the whole hind-brain becomes thickened, and there very soon appears on its outer surface a layer of non-medullated nervefibres, similar to those which first appear on the spinal cord. They are continuous with a similar layer of fibres on the floor of the mid-brain, where they constitute the crura cerebri. On the ventral floor of the medulla is a shallow continuation of the anterior fissure of the spinal cord.

In Elasmobranchii and many Teleostei the restiform tracts are well developed, and are anteriorly continued into the cerebellum, of which they form the peduncles. Near their junction with the cerebellum they form prominent bodies, which are regarded by Miklucho-Maclay as representing the true cerebellum of Elasmobranchii.

In Elasmobranchii a dorsal pair of ridges projects into the cavity of the fourth ventricle, corresponding apparently with the fasciculi teretes of the Mammalia.

In Mammalia there develop, subsequently to the longitudinal fibres


426 THE HIND-BRAIN.


already spoken of, first the olivary bodies of the ventral side of the medulla, and at a still later period the pyramids. The fasciculi teretes in the cavity of the fourth ventricle are developed shortly before the pyramids.

When the hind-brain becomes divided into two regions the roof of the anterior part does not become thinned out like that of the posterior, but on the contrary, becomes somewhat thickened and forms a band-like structure roofing over the anterior part of the fourth ventricle (fig. 247 and fig. 253, cb).

This is a rudiment of the cerebellum, and in all Craniate Vertebrates it at first presents this simple structure and insignificant size. In Cyclostomata, Amphibia and many Reptilia this condition is permanent. In Elasmobranchii, on the other hand, the cerebellum assumes in the course of development a greater and greater prominence (fig. 248, cb), and eventually overlaps both the optic lobes in front and the medulla behind. In the later embryonic stages it exhibits in surface-views the appearance of a median constriction, and the portion of the ventricle contained in it is prolonged into two lateral outgrowths.

Miklucho-Maclay, from his observations on the brains of adult Elasmobranchii, was led to regard what is here called the cerebellum as identical with the mid-brain, and the true mid-brain as part of the thalamencephalon. Miklucho-Maclay was no doubt misled by the large size of the cerebellum, but, as we have seen, this body does not begin to be conspicuous till late in embryonic life.

The mid-brain and thalamencephalon (according to the ordinary interpretations) have in the embryo of Elasmobranchs exactly the same relations as in the embryos of other Vertebrates ; so that the embryological evidence appears to me to be conclusive against Miklucho-Maclay's view.

In Birds the cerebellum attains a very considerable development (fig. 250, cbl\ consisting of a folded central lobe with an arbor vitae, into which the fourth ventricle is prolonged. There are two small lateral lobes, apparently equivalent to the flocculi. Anteriorly the cerebellum is connected with the roof of the midbrain by a delicate membrane, the velum medullas anterius, or valve of Vieussens (fig. 250, vtna). The pons Varolii of Mammalia is represented by a small number of transverse fibres on the floor of the hind-brain immediately below the cerebellum.

In Mammalia the cerebellum attains a still greater develop


NERVOUS SYSTEM OF THE VERTEBRATA. 427

ment The median lobe or vermiform process is first developed. In the higher Mammalia the lateral parts forming the hemi fXJ^ cmfl l,. n

vnut

cU



ats inS fo s

FIG. 250. LONGITUDINAL SECTION THROUGH THE BRAIN OF A CHICK OF TEN

DAYS. (After Mihalkovics.)

Jims, cerebral hemispheres; alf. olfactory lobe; alf^. olfactory nerve; ggt. corpus striatum ; oma. anterior commissure; chd-$. choroid plexus of the third ventricle; pin. pineal gland; cmp. posterior commissure; trm. lamina terminalis; chm. optic chiasma; inf. infundibulum; hph. pituitary body; bgm. commissure of Sylvius (roof of iter a tertio ad quartum ventriculum) ; vma. velum medullae anterius (valve of Vieussens); cbl. cerebellum; chd 4. choroid plexus of the fourth ventricle; obt 4. roof of fourth ventricle ; obi. medulla oblongata ; pns. commissural part of medulla ; inv. sheath of brain ; bis. basilar artery ; crts. internal carotid.

spheres of the cerebellum become formed as swellings at the sides at a considerably later period, and are hardly developed in the Monotremata and Marsupialia.

The cerebellum is connected with the roof of the mid-brain in front and with the choroid plexus of the fourth ventricle behind by delicate membranous structures, known as the velum medullae anterius (valve of Vieussens) and the velum medullae posterius.

The pons Varolii is formed on the ventral side of the floor of the cerebellar region as a bundle of transverse fibres at about the same time as the olivary bodies.

The mid-brain. The changes undergone by the mid-brain are simpler than those of any other part of the brain. We have already seen that the rnid-brain, on the appearance of the cranial flexure, forms an impaired vesicle with a vaulted roof and curved floor, at the front end of the long axis of the body (fig. 1 1 8, MB}. It is at this period in most Vertebrates relatively much larger than in the adult ; and it is only in the Teleostei that it more or less retains in the adult its embryonic proportions.


428 THE FORE-BRAIN.


The cavity of the mid-brain, greatly reduced in size in the higher forms, is known as the iter a tertio ad quartum ventriculum, or aqueductus Sylvii.

The roof of the mid-brain is sharply constricted off from the divisions of the brain in front of and behind it, but these constrictions do not extend to the floor.

In some Vertebrates the region of the mid-brain is stated to undergo hardly any further development. In the Axolotl it remains according to Stieda 1 as a simple tube with nearly uniformly thick walls. In the majority of forms it undergoes, however, a more complicated development.

In Elasmobranchs the sides become thickened to form the optic lobes, which are soon separated by a median longitudinal groove. The floor becomes thickened to form the crura cerebri. The primitive simple median cavity becomes imperfectly divided into a median portion below, and two lateral diverticula in the optic lobes.

In Teleostei the changes, resulting in the formation of (i) a pair of longitudinal ridges projecting from the roof into the cavity of the iter, constituting the fornix of Gottsche, and (2) of the two swellings on the floor, forming the tori semicirculares, are more complicated, but have not been satisfactorily worked out. In Bombinator and the Anura generally the changes are of the same nature as those in Elasmobranchii, except that the prolongations of the ventricle into the optic lobes are still further constricted off from the median portion, which forms the true iter.

In Reptilia and Aves the development of the mid-brain takes place on the same type as in Elasmobranchii and the Anura. In Birds the optic lobes are pushed very much aside, and the roof of the iter is greatly thinned out. In Mammalia the sides of the mid-brain give rise to two pairs of prominences the corpora quadrigemina instead of the two optic lobes of other Vertebrata. The prominences, which do not contain prolongations of the iter, become first visible on the appearance of an oblique transverse furrow, while the anterior pair alone are separated by a longitudinal furrow. In the later stages of development the longitudinal furrow is continued so as to bisect the posterior pair.

The floor, which is bounded posteriorly by the pons Varolii, becomes the crura cerebri. The corpora geniculata interna also belong to this division of the brain.

Fore-brain. In its earliest condition the fore-brain forms a single vesicle without a trace of separate divisions, but very early it buds off the optic vesicles, whose history is described with that of the eye.

1 " Ueb. d. Bau d. centralen Nervensystem d. Axolotl." Zdt.f. wlss. Zool., Vol. xxv. 1875.


NERVOUS SYSTEM OF THE VERTEBRATA.


429


The optic vesicles become gradually constricted off from the fore-brain in a direction obliquely backwards and downwards. They remain, however, attached to it at the anterior extremity of the base of the fore-brain (fig. 251, op.v.). While the above changes are taking place in the optic vesicles the anterior part


opy



FIG. 251. SECTION THROUGH THE FRONT PART OF THE HEAD OF A LEPIDOSTEUS EMBRYO ON THE SEVENTH DAY AFTER IMPREGNATION.

al. alimentary tract ; fb. thalamencephalon ; /. lens of eye ; op.v. optic vesicle. The mesoblast is not represented.


FIG. 252. LONGITUDINAL SECTION THROUGH THE BRAIN OF A YOUNG PRISTIURUS EMBRYO.

cer. commencement of cerebral hemisphere; pn. pineal gland; In. infundibulum ; pt. ingrowth of mouth to form the pituitary body ; mb. mid-brain ; cb. cerebellum ; ch. notochord; al. alimentary tract; laa. artery of mandibular arch.


of the fore-brain becomes prolonged, and at the same time somewhat dilated. At first there is no sharp boundary between the primitive fore-brain and its anterior prolongation, but there shortly appears a constriction which passes from above obliquely forwards and downwards. This constriction is shallow at first, but soon becomes much deeper, leaving however the cavities of the two divisions of the fore-brain united ventrally by a somewhat wide canal (fig. 252).

Of these two divisions the posterior becomes the thalamencephalon, while the anterior and larger division (cer) forms the rudiment of the cerebral hemispheres and olfactory lobes. For a considerable period this rudiment remains perfectly simple, and exhibits no signs, either externally or internally, of a longitudinal constriction dividing it into two lobes.

From the above description it may be concluded that the


430 THE THALAMENCEPHALON.

rudiment of the cerebral hemispheres is contained in the original fore-brain. In spite however of their great importance in all the Craniata, it is probable that the hemispheres were either not present as distinct structures, or only imperfectly separated from the thalamencephalon, in the primitive vertebrate stock.

The thalamencephalon. The thalamencephalon varies so slightly in structure throughout the Vertebrate series that a general description will suffice for all the types.

It forms at first a simple vesicle, the walls of which are of a nearly uniform thickness and formed of the usual spindleshaped cells.


md.



FIG. 253. DIAGRAMMATIC VERTICAL SECTION THROUGH THE HEAD OF A LARVA OF PETROMYZON.

The larva had been hatched three days, and was 4*8 mm. in length. The optic and auditory vesicles are supposed to be seen through the tissues.

c.h. cerebral hemisphere ; th. optic thalamus; in. infundibulum ; pn. pineal gland ; mb. mid-brain ; cb. cerebellum ; md. medulla oblongata ; au.v. auditory vesicle ; op. optic vesicle; ol. olfactory pit; m. mouth; br.c. branchial pouches; th. thyroid involution; v.ao. ventral aorta; ht. ventricle of heart ; ch. notochord.

The cavity it contains is known as the third ventricle. Anteriorly it opens widely into the cerebral rudiment, and posteriorly into the ventricle of the mid-brain. The opening into the cerebral rudiment becomes the foramen of Munro.

For convenience of description I shall divide it into three regions, viz. (i) the floor, (2) the sides, and (3) the roof.

The floor becomes divided into two parts, an anterior part, giving origin to the optic nerves, in which is formed the optic chiasma ; and a posterior part, which becomes produced into an


NERVOUS SYSTEM OF THE VERTEBRATA.


431


at first inconspicuous prominence the rudiment of the infundibulum (fig. 252, In}. This comes in contact with an involution from the mouth, which gives rise to the pituitary body (fig. 252, //), the development of which will be dealt with separately.

In the later stages of development the infundibulum becomes gradually prolonged, and forms an elongated diverticulum of the third ventricle, the apex of which is in contact with the pituitary body (figs. 252, 254, in, and figs. 250 and 255, inf}.

Along the sides of the infundibulum run the commissural fibres connecting the floor of the mid-brain with the cerebrum.

In its later stages the infundibular region presents considerable variations in the different vertebrate types. In Fishes it generally remains very large, and permanently forms a marked diverticulum of the floor of the thalamencephalon. In Elasmobranchii the distal end becomes divided into three lobes a median and two lateral. The lateral lobes appear to become the sacci vasculosi of the adult.

In Teleostei peculiar bodies known as the lobi inferiores (hypoaria) make their appearance at the sides of the a2r ,. y

infundibulum. They appear to correspond in position with the tuber cinereum of Mammalia 1 . In Birds, Reptiles, and Amphibia the lower part of the embryonic infundibulum becomes atrophied and reduced to a mere fingerlike process the processus infundibuli.

In Mammalia the posterior part of the primitive infundibulum becomes the corpus albicans, which is double in Man and the higher Apes ; the ventral part of the posterior wall forms the tuber cinereum. Laterally, at the junction of the optic thalami and infundibulum, there are placed the fibres of the crura cerebri, which are probably derived from the walls of the infundibulum. A special process grows out from the base of the infundibulum, which undergoes peculiar changes, and becomes intimately united with the pituitary body ; in which connection it will be more fully described.


rncl



c.in 'Pt


FIG. 254. LONGITUDINAL SECTION THROUGH THE BRAIN OF SCYLLIUM CANICULA AT AN ADVANCED STAGE OF DEVELOPMENT.

cer. cerebral hemisphere ; pn. pineal gland ; op. th. optic thalamus, connected with its fellow by a commissure (the middle commissure). In front of it is seen a fold of the roof of the forebrain, which is the choroid plexus of the third ventricle ; op. optic chiasma ; ft. pituitary body ; in. infundibulum ; cb. cerebellum ; au.v. passage leading from the auditory vesicle to the exterior ; mel. medulla oblongata ; c . in. internal carotid artery.


1 For the relations of these bodies, vide L. Stieda, "Stud. lib. d. centrale Nervensystem d. Knochenfische." Zeit. f. wiss. Zool. Vol. xvni. 1868.


432 THE PINEAL GLAND.


The sides of the thalamencephalon become very early thickened to form the optic thalami, which constitute the most important section of the thalamencephalon. They are separated, in Mammalia at all events, on their inner aspect from the infundibular region by a somewhat S-shaped groove, known as the sulcus of Munro, which ends in the foramen of Munro. They also become in Mammalia secondarily united by a transverse commissure, the grey or middle commissure, which passes across the cavity of the third ventricle. This commissure is probably homologous with, and derived from, a commissural band in the roof of the thalamencephalon, placed immediately in front of the pineal gland which is well developed in Elasmobranchii (fig. 254).

The roof undergoes more complicated changes. It becomes divided, on the appearance of the pineal gland as a small papilliform outgrowth (the development of which is dealt with separately), into two regions a longer anterior in front of the pineal gland and a shorter posterior. The anterior region becomes at an early period excessively thin, and at a later period, when the roof of the thalamencephalon is shortened by the approach of the cerebral hemispheres to the mid-brain, it becomes (vide figs. 250 and 255, chd 3, and 254) considerably folded, while at the same time a vascular plexus is formed in the pia mater above it. On the accomplishment of these changes it is known as the tela choroidea of the third ventricle.

In the roof of the third ventricle behind the pineal gland there appear in Elasmobranchii, the Sauropsida and Mammalia transverse commissural fibres, forming a structure known as the posterior commissure, which connects together the two optic thalami.

The most remarkable organ in the roof of the thalamencephalon is the pineal gland, which is developed in most Vertebrates as a simple papilliform outgrowth of the roof, and is at first composed of cells similar to those of the other parts of the central nervous system (figs. 250, 252, 254 and 255, pn or pin}. In the lower Vertebrata it is directed forwards, but in Mammalia, and to some extent in Aves, it is directed backwards.

In Amphibia it is described by Gotte (No. 296) as being a product of the point where the roof of the brain remains latest attached to the external skin.


NERVOUS SYSTEM OF THE VERTEBRATA. 433

The figure which Gotte gives to prove this does not appear to me fully to bear out his conclusion ; which if true is very important. Although I directed my attention specially to this point, I could find no indication in Elasmobranchii of a process similar to that described by Gotte, and his observations have not as yet been confirmed for other Vertebrates. Gotte compares the pineal gland to the long-persis.ting pore which leads into the cavity of the brain in the embryo of Amphioxus, and we might add the Ascidians, and, should his facts be confirmed, the conclusion he draws from them would appear to be well founded.

The later stages in the development of the pineal gland in different Vertebrates have not in all cases been fully worked out 1 .

In Elasmobranchii the pineal gland becomes in time very long, and extends far forwards over the roof of the cerebral



FIG. -255. LONGITUDINAL VERTICAL SECTION THROUGH THE ANTERIOR PART OF THE BRAIN OF AN EMBRYO RABBIT OF FOUR CENTIMETRES. (After Mihalkovics.)

The section passes through the median line so that the cerebral hemispheres are not cut ; their position is however indicated in outline.

spt. septum lucidum formed by the coalescence of the inner walls of part of the cerebral hemispheres; cna. anterior commissure; frx. vertical pillars of the fornix; cal, genu of corpus callosum; trm. lamina terminalis; hms. cerebral hemispheres; olf. olfactory lobes; acl. artery of corpus callosum; fmr. position of foramen of Munro; chdi,. choroid plexus of third ventricle ; pin. pineal gland; cmp. posterior commissure; bgm. lamina uniting the lobes of the mid-brain; chm, optic chiasma ; hph. pituitary body; inf. infundibulum ; pns. pons Varolii; pde. cerebral peduncles; agd. iter.

1 For a full account of this subject vide Ehlers (No. 337). B. Ill, 28


434 THE PINEAL GLAND.

hemispheres (fig. 254/w). Its distal extremity dilates somewhat, and in the adult the whole organ forms (Ehlers, No. 337) an elongated tube, enlarged at its free extremity, and opening at its base into the brain. The enlarged extremity may either be lodged in a cavity in the cartilage of the cranium (Acanthias), or be placed outside the cranium (Raja).

In Petromyzon its form is very different. It arises (fig. 2 53 P n ) as a sack-like diverticulum of the thalamencephalon extending at first both backwardsand forwards. In the Ammoccete the walls of this sack are deeply infolded.

The embryonic form of the pineal gland in Amphibia is very much like that which remains permanent in Elasmobranchii ; the stalk connecting the enlarged terminal portion with the brain soon however becomes solid and very thin except at its proximal extremity. The enlarged portion also becomes solid, and is placed in the adult externally to the skull, where it forms a mass originally described by Stieda as the cerebral gland.

In Birds the primitive outgrowth to form the pineal gland becomes, according to Mihalkovics, deeply indented by vascular connective tissue ingrowths, so that it assumes a dendritic structure (fig. 250 pin).

The proximal extremity attached to the roof of the thalamencephalon forms a special section, known as the infra -pineal process. The central lumen of the free part of the gland finally atrophies, but the branches still remain hollow. The infra-pineal process becomes reduced to a narrow stalk, connecting the branched portion of the body with the brain. The branched terminal portion and the stalk obviously correspond with the vesicle and distal part of the stalk of the types already described. In Mammalia the development of the pineal gland is, according to Mihalkovics, generally similar to that of Birds. The original outgrowth becomes branched, but the follicles or lobes to which the branching gives rise eventually become solid (fig. 255 pin). An infra-pineal process is developed comparatively late, and is not sharply separated from the roof of the brain.

No satisfactory suggestions have yet been offered as to the nature of the pineal gland, unless the view of Gotte be regarded as such. It appears to possess in all forms an epithelial structure, but, except at the base of the stalk (infra-pineal process) in


NERVOUS SYSTEM OF THE VERTEBRATA. 435

Mammalia, in the wall of which there are nerve-fibres, no nervous structures are present in it in the adult state.

The pituitary body. Although the pituitary body is not properly a nervous structure, yet from its intimate connection with the brain it will be convenient to describe its development here. The pituitary body is in fact an organ derived from the epiblast of the stomodaeum. This fact has been demonstrated for Mammalia, Aves, Amphibia and Elasmobranchii, and may be accepted as holding good for all the Craniata 1 . The epiblast in the angle formed by the cranial flexure becomes involuted to form the cavity of the mouth. This cavity is bordered on its posterior surface by the front wall of the alimentary tract, and on its anterior by the base of the fore-brain. Its uppermost end does not at first become markedly constricted off from the remainder, but is nevertheless the rudiment of the pituitary body.

Fig. 256 represents a transverse section through the head of an Elasmobranch embryo, in which, owing to the cranial flexure, the fore part of the head is cut longitudinally and horizontally, and the section passes through both the fore-brain (fb) and the hind-brain. Close to the base of the fore-brain are seen the mouth (in), and the pituitary involution from this (pf). In contact with the pituitary involution is the blind anterior termination of the throat (/) which a little way back opens to the exterior by the first visceral cleft (l. v.c.}. This figure alone suffices to demonstrate the correctness of the above account of the pituitary body; but its truth is still further confirmed by fig. 252; in which the mouth involution (pt) is in contact with, but still separated from, the front end of the alimentary tract. Very shortly after the septum between the mouth and throat becomes pierced, and the two are placed in communication, the pituitary involution becomes very partially constricted off from the mouth involution, though still in direct communication with it. In later stages the pituitary involution becomes longer and

1 Scott states that in the larva of Petromyzon the pituitary body is derived from the walls of the nasal pit; Quart, jf. of Micr. Science^ Vol. xxi. p. 750. I have not myself completely followed its development in Petromyzon, but I have observed a slight diverticulum of the stomodaeum which I believe gives origin to it. Fuller details are in any case required before we can admit so great a divergence from the normal development as is indicated by Scott's statements.

283


436


PITUITARY BODY.


Ky


is dilated terminally ; while the passage connecting it with the mouth becomes narrower and narrower, and is finally reduced to a solid cord, which in its turn disappears.

Before the connection between the pituitary vesicle and the mouth is obliterated the cartilaginous cranium becomes developed, and it may then be seen that the infundibulum projects through the pituitary space to come into close juxtaposition with the pituitary body.

After the pituitary vesicle has lost its connection with the mouth it lies just in front of the infundibulum (figs. 250 and 255 hph and fig. 254 pf) ; and soon becomes surrounded by vascular mesoblast, which grows in and divides it into a number of branching tubes. In many forms the cavity of the vesicle completely disappears, and the branches become for the most part solid [Cyclostomata and some Mammalia (the rabbit), Elasmobranchii, Teleostei and Amphibia]. In Reptilia, Aves and most Mammalia the lumen of the organ is more or less retained (W. Miiller, No. 344).

Although in the majority of the Vertebrata there is a close connection between the pituitary body and the infundibulum, there is no actual fusion between the two. In Mammalia the case is different. The part of the infundibulum which lies at the hinder end of the pituitary body is at first a simple finger-like process of the brain (fig. 255 inf), but its end becomes swollen, and the lumen in this part becomes obliterated. Its cells, originally similar to those of the other parts of the nervous system and even (Kolliker) containing differentiated nerve-fibres, partly atrophy, and partly assume an indifferent form, while at the same time



FIG. 256. TRANSVERSE SECTION THROUGH THE FRONT PART OF THE HEAD OF A YOUNG PR1STIURUS EMBRYO.

The section, owing to the cranial flexure, cuts both the fore- and the hind-brain. It shews the premandibular and mandibular head cavities \pp and 2//, etc. The section is moreover somewhat oblique from side to side.

fb. fore-brain; /. lens of eye; m. mouth ;pt. upper end of mouth, forming pituitary involution ; lao. mandibular aortic arch ; \pp. and ipp. first and second head cavities ; \vc. first visceral cleft; V. fifth nerve ; aim. auditory nerve ; VII. seventh nerve; aa. roots of dorsal aorta ; acv. anterior cardinal vein ; ch. notochord.


NERVOUS SYSTEM OF THE VERTEBRATA. 437

there grow in amongst them numerous vascular and connectivetissue elements. The process of the infundibulum thus metamorphosed becomes inseparably connected with the true pituitary body, of which it is usually described as the posterior lobe. The part of the infundibulum which undergoes this change is very probably homologous with the saccus vasculosus of Fishes.

The true nature of the pituitary body has not yet been made out. It is clearly a rudimentary organ in existing craniate Vertebrates, and its development indicates that when functional it was probably a sense organ opening into the mouth, its blind end reaching to the base of the brain. No similar organ has as yet been found in Amphioxus, but it seems possible perhaps to identify it with the peculiar ciliated sack placed at the opening of the pharynx in the Tunicata, the development of which was described at p. 1 8. If the suggestion is correct, the division of the body into lobes in existing Vertebrata must be regarded as a step towards a retrogressive metamorphosis.

Another possible view is to regard the pituitary body as a glandular structure which originally opened into the mouth in the lower Chordata, but which has in all existing forms ceased to be functional. The intimate relation of the organ to the brain appears to me opposed to this view of its nature, while on the other hand its permanent structure is more easily explained on this view than on that previously stated. In the Ascidians a glandular organ has been described by Lacaze Duthiers^n juxtaposition to the ciliated sack, and it is possible that this organ as well as the ciliated sack may be related to the pituitary body. In view of this possibility further investigations ought to be carried out in order to determine whether the whole pituitary body is derived from the oral involution, or whether there may not be a nervous part and a glandular part of the organ.

The Cerebral Hemispheres. It will be convenient to treat separately the development of the cerebral hemispheres proper, and that of the olfactory lobes.

Although the cerebral hemispheres vary more than any other part of the brain, they are nevertheless developed from the unpaired cerebral rudiment in a nearly similar manner throughout the series of Vertebrata.

In the cerebral rudiment two parts may be distinguished, viz. the floor and the roof. The former gives rise to the ganglia at the base of the hemispheres corpora striata, etc. the latter to the hemispheres proper.

1 " Les Ascidies simples des Cotes de France." Archives de Biologie exper. et generate, Vol. III. 1874, p. 329.


43


THE CEREBRAL HEMISPHERES.


The two lobes



cc


The first change which takes place consists in the roof growing out into two lobes, between which a shallow median constriction makes its appearance (fig. 257). thus formed are the rudiments of the two hemispheres. The cavity of each of them opens by a widish aperture into the vestibule at the base of the cerebral rudiment, which again opens directly into the cavity of the third ventricle (3 v). The Y-shaped aperture thus formed, which leads from the cerebral hemispheres into the third ventricle, is the foramen of Munro. The cavity (lv) in each of the rudimentary hemispheres is a lateral ventricle. The part of the cerebrum which lies between the two hemispheres, and passes forwards from the roof of the third ventricle round the end of the brain to the optic chiasma, is the rudiment of the lamina terminalis (figs. 257 It and 255 trm}. Up to this point the development of the cerebrum is similar in all Vertebrata, but in some forms it practically does not proceed much further.

In Elasmobranchii, although the cerebrum reaches a considerable size (fig. 254 cer\ and grows some way backwards over the thalamencephalon, yet it is not in many forms divided into two distinct lobes, but its paired nature is only marked by a shallow constriction on the surface. The lamina terminalis in the later stages of development grows backwards as a thick median septum which completely separates the two lateral ventricles 1 (fig. 263).

There are, it may be mentioned, considerable variations in


op.t/t


FIG. 257. DIAGRAMMATIC LONGITUDINAL HORIZONTAL SECTION THROUGH THE FORE-BRAIN.

j>.v. third ventricle ; lv. lateral ventricle ; //. lamina terminalis ; ce, cerebral hemisphere ; op.th. optic thalamus.


1 A comparison of the mode of development of this septum with that of the septum lucidum with its contained commissures in Mammalia clearly shews that the two structures are not homologous, and that Miklucho-Maclay is in error in attempting to treat them as being so.


NERVOUS SYSTEM OF THE VERTEBRATA. 439

the structure of the cerebrum in Elasmobranchii into which it is not however within the scope of this work to enter.

In the Teleostei the vesicles of the cerebral hemispheres appear at first to have a wide lumen, but it subsequently becomes almost or quite obliterated, and the cerebral rudiment forms a small bilobed nearly solid body. In Petromyzon (fig. 253 c/i) the cerebral rudiment is at first an unpaired anterior vesicle, which subsequently becomes bilobed in the normal manner. The walls of the hemispheres become much thickened, but the lateral ventricles persist

In all the higher Vertebrates the division of the cerebral rudiment into two distinct hemispheres is quite complete, and with the deepening of the furrow between the two hemispheres the lamina terminalis is carried backwards till it forms a thin layer bounding the third ventricle anteriorly, while the lateral ventricles open directly into the third ventricle.

In Amphibians the two hemispheres become united together immediately in front of the lamina terminalis by commissural fibres, forming the anterior commissure. They also send out anteriorly two solid prolongations, usually spoken of as the olfactory lobes, which subsequently fuse together.

In all Reptilia and Aves there is formed an anterior commissure, and in the higher members of the group, especially Aves (fig. 250), the hemispheres may obtain a considerable development. Their outer walls are much thickened, while their inner walls become very thin ; and a well-developed ganglionic mass, equivalent to the corpus striatum, is formed at their base.

The cerebral hemispheres undergo in Mammalia the most complicated development. The primitive unpaired cerebral rudiment becomes, as in lower Vertebrates, bilobed, and at the same time divided by the ingrowth of a septum of connective tissue into two distinct hemispheres (figs. 260 and 26 \f and 258 I). From this septum is formed the falx cerebri and other parts.

The hemispheres contain at first very large cavities, communicating by a wide foramen of Munro with the third ventricle (fig. 260). They grow rapidly in size, and extend, especially backwards, and gradually cover the thalamencephalon and the


440


THE CEREBRAL HEMISPHERES.


mid-brain (fig. 258 I,/). The foramen of Munro becomes very much narrowed and reduced to a mere slit.

The walls are originally , ^

nearly uniformly thick, but the floor becomes thickened on each side, and gives rise to the corpus striatum (figs. 260 and 261 st). The corpus striatum projects upwards into each lateral ventricle, giving to it a somewhat semilunar form, the two horns of which constitute the permanent anterior and descending cornua of the lateral ventricles (fig. 262 st).



FIG. 258. BRAIN OF A THREE MONTHS' HUMAN EMBRYO: NATURAL SIZE. (From Kolliker.)

i. From above with the dorsal part of hemispheres and mid-brain removed ; i. From below, f. anterior part of cut wall of the hemisphere ; f ' . cornu ammonis ; f/io. optic thalamus ; cst. corpus striatum ; to. optic tract ; cm. corpora mammillaria ; /. pons Varolii.


With the further growth of the hemisphere the corpus


CftZ


Ams



spt.


FIG. 259. TRANSVERSE SECTION THROUGH THE BRAIN OF A RABBIT OF FIVE CENTIMETRES. (After Mihalkovics.)

The section passes through nearly the posterior border of the septum lucidum, immediately in front of the foramen of Munro.

hms. cerebral hemispheres ; cal. corpus callosum ; amm. cornu ammonis (hippocampus major) ; cms. superior commissure of the cornua ammonis ; spt. septum lucidum ; frx i. vertical fibres of the fornix; ana. anterior commissure ; trm. lamina terminalis; str. corpus striatum; Iff. nucleus lenticularis of corpus striatum; vtr i. lateral ventricle; vtr 3. third ventricle; ipl. slit between cerebral hemispheres.


NERVOUS SYSTEM OF THE VERTEBRATA. 44!

striatum loses its primitive relations to the descending cornu. The reduction in size of the foramen of Munro above mentioned is, to a large extent, caused by the growth of the corpora striata. The corpora striata are united at their posterior border with the optic thalami. In the later stages of development the area of contact between these two pairs of ganglia increases to an immense extent (fig. 261), and the boundary between them becomes somewhat obscure, so that the sharp distinction which exists in the embryo between the thalamencephalon and cerebral hemispheres becomes lost. This change is usually (Mihalkovics,



FIG. 260. TRANSVERSE SECTION THROUGH THE BRAIN OF A SHEEP'S EMBRYO

OF 27 CM. IN LENGTH. (From Kolliker.) The section passes through the level of the foramen of Munro. st. corpus striatum ; m. foramen of Munro ; t. third ventricle ; pi. choroid plexus of lateral ventricle; f. falx cerebri; th. anterior part of optic thalamus; ch. optic chiasma; o. optic nerve; c. fibres of the cerebral peduncles; h. cornu ammonis; /. pharynx; sa. pre-sphenoid bone; a. orbito-sphenoid bone; s. points to part of the roof of the brain at the junction between the roof of the third ventricle and the lamina terminalis ; /. lateral ventricle.

Kolliker) attributed to a fusion between the corpora striata and optic thalami, but it has recently been attributed by Schwalbe (No. 349), with more probability, to a growth of the original surface of contact, and an accompanying change in the relations of the parts.


442 THE CEREBRAL HEMISPHERES.

The outer wall of the hemispheres gradually thickens, while the inner wall becomes thinner. In the latter, two curved folds, projecting towards the interior of the lateral ventricle, become formed. These folds extend from the foramen of Munro along nearly the whole of what afterwards becomes the descending cornu of the lateral ventricle.

The upper fold becomes the hippocampus major (cornu ammonis) (figs. 259 amm, 260 and 261 /i, and 262 am). When



P'IG. 261. TRANSVERSE SECTION THROUGH THE BRAIN OF A SHEEP'S EMBRYO OF 27 CM. IN LENGTH. (From Kolliker.)

The section is taken a short distance behind the section represented in fig. 260, and passes through the posterior part of the hemispheres and the third ventricle.

st. corpus striatum ; th. optic thalamus; to. optic tract; t. third ventricle; d. roof of third ventricle; c. fibres of cerebral peduncles; c' '. divergence of these fibres into the walls of the hemispheres ; e. lateral ventricle with choroid plexus //; h. cornu ammonis; f. primitive falx; am. alisphenoid; a. orbito-sphenoid ; sa. presphenoid; /. pharynx; mk. Meckel's cartilage.

the rudiment of the descending cornu has become transformed into a simple process of the lateral ventricle the hippocampus major forms a prominence upon its floor.

The wall of the lower fold becomes very thin, and a vascular plexus, derived from the connective-tissue septum between the hemispheres, and similar to that of the roof of the third ventricle,


NERVOUS SYSTEM OF THE VKRTEBRATA. 443

is formed outside it. It constitutes a fold projecting far into the cavity of the lateral ventricle, and together with the vascular connective tissue in it gives rise to the choroid plexus of the lateral ventricle (figs. 260 and 261 //).

It is clear from the above description that a marginal fissure leading into the cavity of the lateral ventricle does not exist in the sense often implied in works on human anatomy, in that the epithelium covering the choroid plexus, which forms the true wall of the brain, is a continuous membrane. The epit/ielium of the choroid plexus of the lateral ventricle is quite independent of that of the choroid plexus of the third ventricle, though at the foramen of Munro the roof of the third ventricle is of course continuous with the inner wall of the lateral ventricle (fig. 260 s). The vascular elements of the two plexuses form however a continuous structure.

The most characteristic parts of the Mammalian cerebrum are the commissures connecting the two hemispheres. These commissures are (i) the anterior commissure, (2) the fornix, and (3) the corpus callosum, the two latter being peculiar to Mammalia.

By the fusion of the inner walls of the hemispheres in front of the lamina terminalis a solid septum is formed, known as the septum lucidum, continuous behind with the lamina terminalis, and below with the corpora striata (figs. 255 and 259 spt). It is by a series of differentiations within this septum that the above commissures originate. In Man there is a closed cavity left in the septum known as the fifth ventricle, which has however no communication with the true ventricles of the brain.

In the septum lucidum there become first formed, below, the transverse fibres of the anterior commissure (fig. 255 and fig. 259 cma), and in the upper part the vertical fibres of the fornix (fig. 255 and fig. 259 frx 2). The vertical fibres meet above the foramen of Munro, and thence diverge backwards, as the posterior pillars, to lose themselves in the cornu ammonis (fig. 259 amm}. Ventrally they are continued, as the descending or anterior pillars of the fornix, into the corpus albicans, and thence into the optic thalami.

The corpus callosum is not formed till after the anterior commissure and fornix. It arises in the upper part of the region


444


THE OLFACTORY LOBES.



(septum lucidum) formed by the fusion of the lateral walls of the hemispheres (figs. 255 and 259 cal), and at first only its curved anterior portion the genu or rostrum is developed. ^ This portion is alone found in Monotremes and Marsupials. The posteriorportion, which is present in all the Monodelphia, is gradually formed as the hemispheres are prolonged further backwards.

Primitively the Mammalian cerebrum, like that of the lower Vertebrata, is quite smooth. In many of the Mammalia, Monotremata, Insectivora, etc., this condition is nearly retained through life, while in the majority of Mammalia a more or less complicated system of fissures is developed on the surface. The most important, and first formed, of these is the Sylvian fissure. It arises at the time when the hemispheres, owing to their growth in front of and behind the corpora striata, have assumed a somewhat bean-shaped form. At the root of the hemispheres the hilus of the bean there is formed a shallow depression, which constitutes the first trace of the Sylvian fissure. The part of the brain lying in this fissure is known as the island of Reil.

The olfactory lobes. The olfactory lobes, or rhinencephala, are secondary outgrowths of the cerebral hemispheres, and contain prolongations of the lateral ventricles, but may however be solid in the adult state. According to Marshall they develop in Birds and Elasmobranchs and presumably other forms later than the olfactory nerves, so that the olfactory region of the hemispheres is indicated before the appearance of the olfactory lobes.

In most Vertebrates the olfactory lobes arise at a fairly early


FIG. 262. LATERAL VIEW or THE BRAIN OF A CALF EMBRYO OF 5 CM. (After Mihalkovics.)

The outer wall of the hemisphere is removed, so as to give a view of the interior of the left lateral ventricle.

hs. cut wall of hemisphere ; st. corpus striatum; am. hippocampus major (cornu ammonis) ; d. choroid plexus of lateral ventricle ; fm. foramen of Munro; op. optic tract; in. infundibulum ; mb. mid-brain ; cb. cerebellum ; IV. V. roof of fourth ventricle ; ps. pons Varolii, close to which is the fifth nerve with Gasserian ganglion.


NERVOUS SYSTEM OF THE VKRTEBRATA.


445


stage of development from the under and anterior part of the hemispheres (fig. .250 olf}. In Elasmobranchs they arise, not



FIG. 263. SECTION THROUGH THE BRAIN AND OLFACTORY ORGAN OF AN EMBRYO OF SCYLLIUM. (Modified from figures by Marshall and myself.)

ch. cerebral hemispheres ; ol.v. olfactory vesicle ; olf. olfactory pit ; Sch. Schneiderian folds ; I. olfactory nerve. The reference line has been accidentally taken through the nerve to the brain ; pn. anterior prolongation of pineal gland.

from the base, but from the lateral parts of the brain (fig. 263), and become subsequently divided into a bulbous portion and a stalk. They vary considerably in their structure in the adult.

In Amphibia the solid anterior prolongations of the cerebral hemispheres already spoken of are usually regarded as the olfactory lobes, but according to Gotte, whose view appears to me well founded, small papillae, situated at the base of these prolongations, from which olfactory nerves spring, and which contain a process of the lateral ventricle, should properly be regarded as the olfactory lobes. These papillse arise prior to the solid anterior prolongations of the hemispheres.

In Birds the olfactory lobes are small. In the chick they arise (Marshall) on the seventh day of incubation.


General conclusions as to the Central Nervous System.

It has been shewn above that both the brain and spinal cord are primitively composed of a uniform wall of epithelial cells, and that the first differentiation results in the formation of an external layer of white matter, a middle layer of grey matter (ganglion cells), and an inner epithelial layer. This primitive


446 GENERAL CONCLUSIONS.

histological arrangement, which in many parts of the brain at any rate, is only to be observed in the early developmental stages, has a simple phylogenetic explanation.

As has been already explained in an earlier part of this chapter the central nervous system was originally a differentiated part of the superficial epidermis.

This differentiation (as may be concluded from the character of the nervous system in the Ccelenterata and Echinodermata) consisted in the conversion of the inner ends of the epithelial cells into nerve-fibres ; that is to say, that the first differentiation resulted in the formation of a layer of white matter on the inner side of the epidermis. The next stage was the separation of a deeper layer of the epidermis as a layer of ganglion cells from the superficial epithelial layer, i.e. the formation of a middle layer of ganglion cells and an outer epithelial layer. Thus, phylogenetically, the same three layers as those which first make their appearan-ce in the ontog'eny of the vertebrate nervous system became successively differentiated, and in both cases they are clearly placed in the same positions, because the central canal of the vertebrate nervous system, as formed by an involution, is at the true outer surface, and the external part of the cord is at the true inner surface.

It is probable that a very sharp distinction between the white and grey matter is a feature acquired in the higher Vertebrata, since in Amphioxus there is no such sharp separation ; though the nerve-fibres are mainly situated externally and the nerve-cells internally.

As already stated in Chapter Xll. the primitive division of the nervous axis was probably not into brain and spinal cord, but into (i) a fore-brain, representing the ganglion of the praeoral lobe, and (2) the posterior part of the nervous axis, consisting of the mid- and hind-brains and the spinal cord. This view of the division of the central nervous system fits in fairly satisfactorily with the facts of development. The fore-brain is, histologically, more distinct from the posterior part of the nervous system than the posterior parts are from each other ; the front end of the notochord forms the boundary between these two parts of the central nervous system (vide fig. 253), ending as it does at the front termination of the floor of the mid-brain, and finally,


NERVOUS SYSTEM OF THE VERTEBRATA. 447

the nerves of the fore-brain have a different character to those of the mid- and hind-brain.

This primitive division of the central nervous system is lost in all the true Vertebrata, and in its place there is a secondary division corresponding with the secondary vertebrate head into a brain and spinal cord. The brain, as it is established in these forms, is again divided into a fore-brain, a mid-brain and a hind-brain. The fore-brain is, as we have already seen, the original ganglion of the praeoral lobe. The mid-brain appears to be the lobe, or ganglion, of the third pair of nerves (first pair of segmental nerves), while the hind-brain is a more complex structure, each section of which (perhaps indicated by the constrictions which often appear at an early stage of development) giving rise to a pair of segmental nerves is, roughly speaking, homologous with the whole mid-brain.

The type of differentiation of each of the primitively simple vesicles forming the fore-, the mid- and the hind-brains is very uniform throughout the Vertebrate series, but it is highly instructive to notice the great variations in the relative importance of the parts of the brain in the different types. This is especially striking in the case of the fore-brain, where the cerebral hemispheres, which on embryological grounds we may conclude to have been hardly differentiated as distinct parts of the fore-brain in the most primitive types now extinct, gradually become more and more prominent, till in the highest Mammalia they constitute a more important section of the brain than the whole of the remaining parts put together.

The little that is known with reference to the significance of the more or less corresponding outgrowths of the floor and roof of the thalamencephalon, constituting the infundibulunv and pineal gland, has already been mentioned in connection with the development of these parts.


(332) C. J. Cams. Vcrsnch einer Darstellnng d. Nervensy stems, etc. Leipzig,

1814.

(333) J. L. Clark. " Researches on the development of the spinal cord in Man, Mammalia and Birds." Phil. Trans., 1862. .


448 BIBLIOGRAPHY.


(334) E. Dursy. " Beitrage zur Entwicklungsgeschichte des Hirnanhanges. " Centralblatt f. d, med. Wissenschaften, 1868. Nr. 8.

(335) E. Dursy. Zur Entwicklungsgeschichte des Kopfes des Menschen and der hoheren Wirbelthiere. Tiibingen, 1869.

(336) A. Ecker. "Zur Entwicklungsgeschichte der Furchen und Windungen der Grosshirn-Hemispharen im Foetus des Menschen." Archiv f. Anthropologie, v. Ecker und Lindenschmidt. Vol. ill. 1868.

(337) E. Ehlers. "Die Epiphyse am Gehirn d. Plagiostomen." Zeit. f. wiss. Zool. Vol. xxx., suppl. 1878.

(338) P. Flechsig. Die Leitungsbahnen im Gehirn und Riickenmark des Menschen. Auf Grund cntwicklungsgeschichtlicher Untersucfumgen. Leipzig, 1876.

(339) V. Hensen. "Zur Entwicklung des Nervensystems." Virchoitfs Archiv, Bd. xxx. 1864.

(340) L. Lowe. "Beitrage z. Anat. u. z. Entwick. d. Nervensystems d. Saugethiere u. d. Menschen." Berlin, 1880.

(341) L. Lowe. " Beitrage z. vergleich. Morphogenesis d. centralen Nervensystems d. Wirbelthiere." Mittheil. a. d. embryo!. Instit. Wien, Vol. II. 1880.

(342) A. M. Marshall. "The Morphology of the Vertebrate Olfactory organ." Quart. J. of Micr. Science, Vol. XIX. 1879.

(343) V. v. Mihalkovics. Entwicklungsgeschichte d. Gehirns. Leipzig, 1877.

(344) W. Mil Her. " Ueber Entwicklung und Bau der Hypophysis und des Processus infundibuli cerebri. " yenaische Zeitschrift. Bd. VI. 1871.

(345) H. Rahl-Riickhard. "Die gegenseitigen Verhaltnisse d. Chorda, Hypophysis etc. bei Haifischembryonen, nebst Bemerkungen lib. d. Deutung d. einzelnen Theile d. Fischgehirns." Morphol. Jahrbttch, Vol. vi. 1880.

(348) H. Rathke. " Ueber die Entstehung der glandula pituitaria." Mutter's Archiv f. Anat. und Physiol., Bd. V. 1838.

(347) C. B. Reichert. Der Bau des mcnschlichen Gehirns. Leipzig, 1859 u 1861.

(348) F. Schmidt. "Beitrage zur Entwicklungsgeschichte des Gehirns." Zeitschrift f. wiss. Zoologie, 1862. Bd. xi.

(349) G. Schwalbe. "Beitrag z. Entwick. d. Zwischenhirns. " Sitz. d. Jenaischcn Gesell.f. Med. u. Naturwiss. Jan. 23, 1880.

(350) F'ried. Tiedemann. Anatomic und Bildtmgsgeschichte des Gehirns im Foetus des Menschen. Niirnberg, 1816.


THE DEVELOPMENT OF THE CRANIAL AND SPINAL NERVES 1 .

All the nerves are outgrowths of the central nervous system, but the differences in development between the cranial and spinal nerves are sufficiently great to make it convenient to treat them separately.

1 Remak derived the posterior ganglia from the tissue of the mesoblastic somites, and following in Remak's steps most authors believed the peripheral nervous system to have a mesoblastic origin. This view, which had however been rejected on theoretical grounds by Hensen and others, was finally attacked on the ground of observation by His (No. 297). His (No. 352, p. 458) found that in the Fowl " the


NERVOUS SYSTEM OF THE VERTEBRATA. 449

Spinal nerves. The posterior roots of the spinal nerves, as well as certain of the cranial nerves, arise in the same manner, and from the same structure, and are formed considerably before the anterior roots. Elasmobranch fishes may be taken as the type to illustrate the mode of formation of the spinal nerves.

The whole of the nerves in question arise as outgrowths of a median ridge of cells, which makes its appearance on the dorsal side of the spinal cord (fig. 264 A, pr). This ridge has been called by Marshall the neural crest. At each point, where a pair of nerves will be formed, two pear-shaped outgrowths project from it, one on each side ; and apply themselves closely to the walls of the spinal cord (fig. 264 B, pr). These outgrowths are the rudiments of the posterior nerves. While still remaining attached to the dorsal summit of the neural cord they grow to a considerable size (fig. 264 B, pr).

The attachment to the dorsal summit is not permanent, but

spinal ganglia of the head and trunk arose from a small band of matter which is placed between the medullary plate and epiblast, and the material of which he called the 'intermediate cord'." He further states that: "Before the closure of the medullary tube this band forms a special groove the 'intermediate groove' placed close to the border of the medullary plate. As the closure of the medullary plate into a tube is completed, the earlier intermediate groove becomes a compact cord. In the head of the embryo a longitudinal ridge arises in this way, which separates the suture of the brain from that of the epiblast. In the parts of the neck and in the remaining region of the neck the intermediate cord does not lie over the line of junction of the medullary tube, but laterally from this and forms a ridge, triangular in section, with a slight indrawing." This intermediate ridge gives rise to four ganglia in the head, viz. the g. trigemini, g. acousticum, g. glossopharyngei, and g. vagi, and in the trunk to the spinal ganglia. In both cases it unites first with the spinal cord.

I have given in the above account, as far as possible, a literal translation of His' own words, because the reader will thus be enabled fairly to appreciate his meaning.

Subsequently to His' memoir (No. 297) I gave an account of some researches of my own on this subject (No. 351), stating the whole of the nerves to be formed as cellular outgrowths of the spinal cord. I failed fully to appreciate that some of the stages I spoke of had been already accurately described by His, though interpreted by him very differently. Marshall, and afterwards Kolliker, arrived at results in the main similar to my own, and Hensen, independently of and nearly simultaneously with myself, published briefly some observations on the nerves of Mammals in harmony with my results.

His has since worked over the subject again (No. 352), and has reaffirmed as a result of his work his original statements. I cannot, however, accept his interpretations on the subject, and must refer the reader who is anxious to study them more fully, to His' own paper.

B. III. 29


450


SPINAL NERVES.



FIG. -264 A. TRANSVERSE SECTION THROUGH A PRISTIURUS EMBRYO SHEWING THE PROLIFERATION OF CELLS TO FORM THE NEURAL CREST.

pr. neural crest ; nc. neural canal ; ch. notochord ; ao. aorta.



FIG. 2646. TRANSVERSE SECTION THROUGH THE TRUNK OK AN EMBRYO SLIGHTLY OLDER THAN FIG. 28 E.

nc. neural canal ; pr. posterior root of spinal nerve ; x. subnotochordal rod ; ao. aorta ; sc . somatic mesoblast ; sp. splanchnic mesoblast ; mp. muscle-plate ; mp'. portion of muscle-plate converted into muscle ; Vv. portion of the vertebral plate which will give rise to the vertebr.il bodies ; al. alimentary tract.


before describing the further fate of the nerve-rudiments it is necessary to say a few words as to the neural crest. At the period when the nerves have begun to shift their attachment to the spinal cord, there makes its appearance, in Elashiobranchii, a longitudinal commissure connecting the dorsal ends of all the spinal nerves (figs. 265, 266 com}, as well as those of the vagus and glosso-pharyngeal nerves. This commissure has as yet only been found in a complete form in Elasmobranchii ;



FIG. 265. VERTICAL LONGITUDINAL SECTION THROUGH PART OF THETRUNK OF A YOUNG SCYLLIUM EMBRYO.

com. commissure uniting the dorsal ends of the posterior nerve-roots ; pr. ganglia of posterior roots; ar. anterior roots; st. segmental tubes; sd. segmental duct; g.c. epithelium lining the body cavity in the region of the future germinal ridge.


NERVOUS SYSTEM OF THE VERTEBRATA.


451


but it is nevertheless to be regarded as a very important morphological structure.



FIG. 266. SPINAL NERVES OF SCYLLIUM IN LONGITUDINAL SECTION TO SHEW THE COMMISSURE CONNECTING THEM.

A. Section through a series of nerves.

B. Highly magnified view of the dorsal part of a single nerve, and of the commissure connected with it.

com. commissure; sp.g. ganglion of posterior root; ar. anterior root.

It is probable, though the point has not yet been definitely made out, that this commissure is derived from the neural crest, which appears therefore to separate into two cords, one connected with each set of dorsal roots.


7' r



FIG. 267. SECTION THROUGH THE DORSAL PART OF THE TRUNK OF A

TORPEDO EMBRYO.

pr. posterior root of spinal nerve ; g . spinal ganglion ; n. nerve ; ar. anterior root of spinal nerve; ch. notochord; nc. neural canal; mp. muscle-plate.

29 2


452 SPINAL NERVES.


Returning to the original attachment of the nerve-rudiments to the medullary wall, it has been already stated that this attachment is not permanent. It becomes, in fact, at about the time of the appearance of the above commissure, either extremely delicate or absolutely interrupted.

The nerve-rudiment now becomes divided into three parts (figs. 267 and 268), (i) a proximal rounded portion, to which is attached the longitudinal commissure (pr) \ (2) an enlarged portion, forming the rudiment of a ganglion (g and sp g}\ (3) a distal portion, forming the commencement of the nerve (#). The proximal portion may very soon be observed to be united with the side of the spinal cord at a very considerable distance from its original point of attachment. Moreover the proximal portion of the nerve is attached, not by its extremity, but by its side, to the spinal cord (fig. 268 x\ The dorsal extremities of the posterior roots are therefore free.

This attachment of the posterior nerve-root to the spinal cord is, on account of its small size, very difficult to observe. In favourable specimens there may however be seen a distinct cellular prominence from the spinal cord, which becomes continuous with a small prominence on the lateral border of the nerve root near its proximal extremity. The proximal extremity of the nerve is composed of cells, which, by their small size and circular form, are easily distinguished from those which form the succeeding or ganglionic portion of the nerve. This part has a swollen configuration, and is composed of large elongated cells with oval nuclei. The remainder of the rudiment forms the commencement of the true nerve. This also is, at first, composed of elongated cells 1 .

1 The cellular structure of embryonic nerves is a point on which I should have anticipated that a difference of opinion was impossible, had it not been for the fact that His and Kolliker, following Remak and other older embryologists, absolutely deny the fact. I feel quite sure that no one studying the development of the nerves in Elasmobranchii with well-preserved specimens could for a moment be doubtful on this point, and I can only explain His' denial on the supposition that his specimens were utterly unsuited to the investigation of the nerves. I do not propose in this work entering into the histogenesis of nerves, but may say that for the earlier stages of their growth, at any rate, my observations have led me in many respects to the same results as Gotte (Entwick. d. Unke, pp. 482 483), except that I hold that adequate proof is supplied by my investigations to demonstrate that the nerves are for their whole length originally formed as outgrowths of the central nervous system. As the nerve-fibres become differentiated from the primitive spindle-shaped cells, the nuclei become relatively more sparse, and this fact has probably misled Kolliker. Lowe, while admitting the existence of nuclei in the nerves, states that they belong to mesoblastic cells which have wandered into the nerves. This is a purely gratuitous assumption, not supported by observation of the development.


NERVOUS SYSTEM OF THE VERTEBRATA.


453


It is extremely difficult to decide whether the permanent attachment of the posterior nerve-roots to the spinal cord is entirely a new formation, or merely due to the shifting of the original point of attachment. I am inclined to adopt the former view, which is also held by Marshall and His, but may refer to fig. 269, shewing the roots after they have become attached to the side, as distinct evidence in favour of the view that the attachment simply becomes shifted, a process which might perhaps be explained by a growth of the dorsal part of the spinal cord. The change of position in the case of some of the cranial nerves is, however, so great that I do not think that it is possible to account for it without admitting the formation of a new attachment.

The anterior roots of the spinal nerves appear somewhat later than the posterior roots, but while the latter are still quite small. Each of them (fig. 269 ar) arises as a small but distinct conical outgrowth from a ventral corner of the spinal cord, before the latter has acquired its covering of white matter. From the very first the rudiments of the anterior roots have a somewhat fibrous appearance and an indistinct form of peripheral



FIG. 268. SECTION THROUGH THE DORSAL REGION OF A PRISTIURUS EMBRYO. pr. posterior root; sp.g. spinal ganglion; n. nerve; x. attachment of ganglion to spinal cord ; nc. neural canal ; mp. muscle-plate ; ch. notochord ; i. investment of spinal cord.

termination, while the protoplasm of which they are composed becomes attenuated towards its end. They differ from the posterior roots in never shifting their point of attachment to the spinal cord, in not being united with each other by a commissure, and in never developing a ganglion.


454


SPINAL NERVES.


The anterior roots grow rapidly, and soon form elongated cords of spindle-shaped cells with wide attachments to the spinal cord (fig. 267). At first they pass obliquely and nearly horizontally outwards, but, before reaching the muscle-plates, they take a bend downwards.

One feature of some interest with reference to the anterior roots is the fact that they arise not vertically below, but alternately with the posterior roots : a condition which persists in the adult. They are at first quite separate from the posterior roots ; but about the stage represented in fig. 267 a junction is effected between each posterior root and the corresponding anterior root. The anterior root joins the posterior at some little distance below its ganglion (figs. 265 and 266).

Although I have made some efforts to determine the eventual fate of the commissure uniting the dorsal roots, I have not hitherto met with success. It grows thinner and thinner, becoming at the same time composed of fibrous protoplasm with imbedded nuclei, and finally ceases to be recognisable. I can only conclude that it gradually atrophies, and ultimately vanishes.

After the junction of the posterior and anterior roots the compound nerve extends downwards, and may easily be traced for a considerable distance. A special dorsal branch is given off from the ganglion on the posterior root (fig. 275 dn\ According to Lowe the fibres of the anterior and posterior roots can easily be distinguished in the higher types by their structure and behaviour towards colouring reagents, and can be separately traced in the compound



FIG. 269. TRANSVERSE SKI TION THROUGH THE DORSAL REGION OF A YOUNG TORPEDO EMBRYO TO SHEW THE ORIGIN OF THE ANTERIOR AND POSTERIOR ROOTS OF THE SPINAL NERVES.

pr. posterior root of spinal nerve ; ar. anterior root of spinal nerve; mp. muscle-plate; ch. notochord; vr. mesoblast cells which will form the vertebral bodies.

nerve.


So far as has been made out, the development of the spinal nerves of other Vertebrates agrees in the main with that in Elasmobranchii, but no dorsal commissure has yet been discovered, except in the case of the first two or three spinal nerves of the Chick.

In the Chick (Marshall, No. 353) the posterior roots, during their early stages, closely resemble those in Elasmobranchii, though their relatively smaller size makes them difficult to observe. They at first extend more or


NERVOUS SYSTEM OF THE VERTEBRATA.


455


less horizontally outwards above the muscle-plates (as a few of the nerves also do to some extent in Elasmobranchii), but subsequently lie close to the sides of the neural canal. They are shewn in this position in fig. 116 sp.g. There does not appear to be a continuous crest connecting the roots of the posterior nerves. The later stages of the development are precisely like those in Elasmobranchii.

The anterior roots have not been so satisfactorily investigated as the posterior, but they grow out, possibly by several roots for each nerve, from the ventral corners of the spinal cord, and subsequently become attached to the posterior nerves.

I have observed the development of the posterior roots in Lepidosteus, in which they appear as projections from the dorsal angles of the spinal cord, extending laterally outwards and, at first, having their extremities placed dorsally to the muscle-plates.

The cranial nerves 1 . The earliest stages in the development of the cranial nerves have been most satisfactorily studied, especially by Marshall (No. 354), in the Chick, while the later stages have been more fully worked out in Elasmobranchii, where, moreover, they present a very primitive arrangement.


hi,



fy


FIG. 270.


TRANSVERSE SECTION THROUGH THE POSTERIOR PART OF THE

HEAD OF AN EMBRYO CHICK OF THIRTY HOURS.

hb. hind-brain; vg. vagus nerve; cp. epiblast; ch. notochord; x. thickening of hypoblast (possibly a rudiment of the subnotochordal rod) ; al. throat ; ht. heart ; //. body cavity ; so. somatic mesoblast ; sf. splanchnic mesoblast ; hy. hypoblast.

1 The optic nerves are for obvious reasons dealt with in connection with the development of the eye.


456 CRANIAL NERVES.


In the Chick certain of the cranial nerves arise before the complete closure of the neural groove. These nerves are formed as paired outgrowths of a continuous band composed of two laminae, connecting the dorsal end of the incompletely closed medullary canal with the external epiblast. This mode of development will best be understood by an examination of fig. 270, where the two roots of the vagus nerve (vg) are shewn growing out from the neural band. Shortly after this stage the neural band, becoming separated from the epiblast, constitutes a crest attached to the roof of the brain, while its two laminae become fused. The relation of the cranial nerves to the brain then becomes exactly the same as that of the posterior roots of the spinal nerves to the spinal cord.

It does not appear possible to decide whether the mode of development of the cranial nerves in the Chick, or that of the posterior roots of the spinal nerves, is the more primitive. The difference in development between the two sets of nerves probably depends upon the relative time of the closure of the neural canal. The neural crest clearly belongs to the brain, from the fact of its remaining connected with the latter when the medullary tube separates from the external epiblast.

It is not known whether the cranial nerves originate before the closure of the neural canal in other forms besides the Chick.

The neural crest of the brain is continuous with that of the spinal cord, and on its separation from the central nervous axis forms on each side a commissure, uniting the posterior cranial nerves with the spinal nerves, and continuous with the commissure connecting together the latter nerves.

Anteriorly, the neural crest extends as far as the roof of the mid-brain 1 . The pairs of nerves which undoubtedly grow out from it are the third pair (Marshall), the fifth, the seventh and auditory (as a single root), the glossopharyngeal, and the various elements of the vagus (as separate roots in Elasmobranchii, but as a single root in Aves). Marshall holds that the olfactory

1 Marshall holds that the neural crest extends in front of the region of the optic vesicle. I have been unable completely to satisfy myself of the correctness of this statement. In my specimens the epiblast along the line of infolding of this part of the roof of the brain is much thickened, but what Marshall represents as a pair of outgrowths from it like those of a true nerve (No. 354, PI. n. fig. 6) appears to me in my specimens to be part of the external epiblast ; and I believe that they remain connected with the external epiblast on the complete separation of the brain from it.


NERVOUS SYSTEM OF THE VERTEBRATA. 457

nerve probably also originates from this crest. It will however be convenient to deal separately with this nerve, after treating of the other nerves which undoubtedly arise from the neural crest.

The cranial nerves just enumerated present in their further development many points of similarity ; and the glossopharyngeal nerve, as it develops in Elasmobranchii, may perhaps be taken as typical. This nerve is connected by a commissure with those behind, but this fact may for the moment be left out of consideration. Springing at first from the dorsal line of the hind-brain immediately behind the level of the auditory capsule, it apparently loses this primitive attachment and acquires a secondary attachment about half-way down the side of the hind-brain. The primitive undifferentiated rudiment soon becomes divided, exactly like a true posterior root of a spinal nerve, into a root, a ganglion and a nerve. The main branch of the nerve passes ventralwards, and supplies the^ first branchial arch (fig. 271 gl}. Shortly afterwards it sends forwards a smaller branch, which passes to the hyoid arch in front ; so that the nerve forks over the hyobranchial cleft. A typical cranial nerve appears therefore, except as concerns its relations to the clefts, to develop precisely like the posterior root of the spinal nerve.

Most of the cranial nerves of the above group, in correlation with the highly differentiated character of the head, acquire secondary differentiations, and render necessary a brief description of what is known with reference to their individual development.

The Glossopharyngeal and Vagus Nerves. Behind the ear there are formed, in Scyllium, a series of five nerves which pass down to respectively the first, second, third, fourth and fifth branchial arches.

For each arch there is thus one nerve, whose course lies close to the posterior margin of the preceding cleft ; a second anterior branch, forking over the cleft and passing to the arch in front, being developed later. These nerves are connected with the brain by roots at first attached to the dorsal summit, but eventually situated about half-way down the sides. The foremost of them is the glossopharyngeal. The next four are, as has been shewn by Gegenbaur 1 , equivalent to four independent nerves, but form together a compound nerve, which we may briefly call the vagus.

1 "Ueber d. Kopfnerven von Hexanchus," etc., Jenaische Zeitschrift, Vol. VI. 1871.


CRANIAL NERVES.


This compound nerve together with the glossopharyngeal soon attains a very complicated structure, and presents several remarkable features. There are present five branches (fig. 271 B), viz. the glossopharyngeal (gl) and four branches of the vagus, the latter probably arising by a considerably greater number of strands from the brain 1 . All the strands from the brain are united together by a thin commissure (fig. 271 B, vg) } continuous with the commissure of the posterior roots of the spinal nerves, and from this commissure the five branches are continued obliquely ventralwards and backwards, and each of them dilates into a ganglionic swelling. They all become again united together by a second thick commissure, which is continued backwards as the intestinal branch of the vagus nerve. The nerves, however, are continued ventralwards each to its respective arch.


A6


t'A



FlG. 271. VIEWS OF THE HEAD OF El.ASMOBRANCH EMBRYOS AT TWO STAGES AS TRANSPARENT OBJECTS.

A. Pristiurus embryo of the same stage as fig. 28 F.

B. Somewhat older Scyllium embryo.

///. third nerve ; V. fifth nerve ; VII. seventh nerve ; au.n. auditory nerve ; gl. glossopharyngeal nerve; Vg. vagus nerve; fb. fore-brain; pn. pineal gland ; mb. midbrain; hb. hind-brain; iv.v. fourth ventricle; cb. cerebellum; ol. olfactory pit; op. eye; au.V. auditory vesicle; m. mesohlast at base of brain; t/i. notochord; /it. heart; Vc. visceral clefts; eg. external gills; //. sections of body cavity in the head.


1 " Ueber d. Kopfnerven von Hexanchus," etc., Jenaische Zeitschrift, Vol. vi. i S; i .


NERVOUS SYSTEM OF THE VERTEBRATA. 459

From the lower commissure springs the lateral nerve, at a point whose relations to the branches of the vagus I have not certainly determined.

With reference to the dorsal commissure, which is almost certainly derived from the original neural crest, it is to be noted that there is a longish stretch of it between the last branch of the vagus and the first spinal nerve, which is probably the remains of a part of the commissure which connected the posterior branches of the vagus, at a stage in the evolution of the Vertebrata, when the posterior visceral clefts were still present. These branches of the vagus are probably partially preserved in the ramifications of the intestinal stem of the vagus (Gegenbaur). The origin of the ventral commissure, continued as the intestinal branch of the vagus, has not been embryologically worked out.

The lateral nerve may very probably be a dorsal sensory branch of the vagus, whose extension into the posterior part of the trunk has been due to the gradual backward elongation of the lateral line 1 , causing the nerve supplying it to elongate at the same time (vide Section on lateral line).

In the Chick the common rudiment for the vagus and glossopharyngeal nerves (Marshall), which has already been spoken of, subsequently divides into two parts, an anterior forming the glossopharyngeal nerve, and a posterior forming the vagus nerve.

The seventh and auditory nerves. As shewn by Marshall's and my own observations 'there is a common rudiment for the seventh and auditory nerves. This rudiment divides almost at once into two branches. The anterior of these pursues a straight course to the hyoid arch (fig. 271 A, VII.} and forms the rudiment of the facial nerve ; the second of the two (fig. 271 A, au.ti), which is the rudiment of the auditory nerve, develops a ganglionic enlargement and, turning backwards, closely hugs the ventral wall of the auditory involution (fig. 272).

The seventh or facial nerve soon becomes more complicated. It early develops, like the glossopharyngeal and vagus nerves, a branch, which forks over the cleft in front (spiracle), and supplies the mandibular arch (fig. 27 1 B). This branch forms the praespiracular nerve of the adult, and is homologous with the chorda tympani of Mammalia. Besides however giving rise to this typical branch it gives origin, at a very early period, to two other rather remarkable branches ; one of these, arising from its dorsal anterior border, passes forwards to the front part of the head, immediately dorsal to the ophthalmic branch of the fifth to be described directly. This nerve is the portio major or superficialis of the nerve usually known as the ramus ophthalmicus superficialis in the adult 2 .

1 The peculiar distribution of branches of the fifth and seventh nerves to the lateral line, which is not uncommon, is to be explained in the same manner.

2 The two branches of the ramus ophthalmicus superficialis were spoken of as the ram. opth. superficialis and ram. opth. profundus in my Monograph on Elasmobranch Fishes. The nomenclature in the text is Schwalbe's, which is probably more correct than mine.


460 CRANIAL NERVES.


The other branch of the seventh is the palatine branch superficial petrosal of Mammalia the course of which has been more fully investigated by Marshall than by myself. He has shewn that it arises "just below the root of the ophthalmic branch," and " runs downwards and forwards, lying parallel and immediately superficial to the maxillary branch of the fifth nerve." This branch of the seventh nerve appears to bear the same sort of relation to the superior maxillary branch of the fifth nerve, that the ophthalmic branch of the seventh does to the ophthalmic branch of the fifth.

Both the root of the seventh and its main branches are gangliated.

The auditory nerve is probably to be regarded as a specially differentiated part of a dorsal branch of the seventh, while the ophthalmic branch may not improbably be a dorsal branch comparable to a dorsal branch of one of the spinal nerves.

The fifth nerve. Shortly after its development the root of the fifth nerve shifts so as to be attached about half-way down the side of the brain. A large ganglion becomes developed close to the root, which forms the rudiment of the Gasserian ganglion. The main branch of the nerve grows into the mandibular arch (fig. 271 A, V), maintaining towards it similar relations to those of the posterior nerves to their respective arches.

Two other branches very soon become developed, which were not properly distinguished in my original account. The dorsal one takes a course parallel to the ophthalmic branch of the seventh nerve, and forms, according to the nomenclature already adopted, the portio profunda of the ophthalmicus superficialis of the adult.

The second nerve (fig. 271 A) passes forwards, above the mandibular head cavity, and is directed straight towards the eye, near which it meets and unites with the third nerve, where the ciliary ganglion is developed (Marshall). This branch is usually called the ophthalmic branch of the fifth nerve, but Marshall rightly prefers to call it the communicating branch between the fifth and third nerves 1 .

Later than these two branches there is developed a third branch, passing to the front of the mouth, and forming the superior maxillary branch of the adult (fig. 271 B).

Of the branches of the fifth nerve the main mandibular branch is obviously comparable to the main branch of the posterior nerves. The superficial ophthalmic branch is clearly equivalent to the ophthalmic branch of the seventh. The superior maxillary is usually held to be equivalent to that branch of the posterior nerves which forms the anterior limb of the fork over a cleft. The similarity between the course of this nerve and that of the palatine branch of the seventh, resembling as it does the similar course of the ophthalmic branches of the two nerves, suggests that it may perhaps really be the homologue of the palatine branch of the seventh, there

1 Marshall thinks that this nerve may be the remains of the commissure originally connecting the roots of the third and fifth nerves. This suggestion can only be tested by further observations.


NERVOUS SYSTEM OF THE VERTEBRATA. 461

being no homologue of the typical anterior branch of the other cranial nerves.

The third nerve. Our knowledge of the development of the third nerve is entirely due to Marshall. He has shewn that in the Chick there is developed from the neural crest, on the roof of the mid-brain, an outgrowth on each side, very similar to the rudiment of the posterior nerves. This outgrowth, the presence of which I can confirm, he believes to be the third nerve, but although he is probably right in this view, it must be borne in mind that there is no direct evidence on the point, the fate of the outgrowth in question not having been satisfactorily followed.

At a very considerably later period a nerve may be found springing from the floor of the mid-brain, which is undoubtedly the third nerve, and which Marshall supposes to be the above rudiment, which has shifted its position. It is shewn in Scyllium in fig. 271 B, ///. A few intermediate stages between this and the earliest condition of the nerve have been imperfectly traced by Marshall.

The nerve at the stage represented in fig. 271 B arises from a ganglionic root, and " runs as a long slender stem almost horizontally backwards, then turns slightly outwards to reach the interval between the dorsal ends of the first and second head cavities, where it expands into a small ganglion." This ganglion, as first suggested by Schwalbe (No. 359), and subsequently proved embryologically by Marshall, is the ciliary ganglion. From the ciliary ganglion two branches arise ; one branch continuing the main stem of the nerve, and obviously homologous with the main branch of the other nerves, and the other passing directly forwards " along the top of the first head cavity, then along the inner side of the eye, and finally terminating at the anterior extremity of the head, just dorsal of the olfactory pit."

The partial separation, in many forms, of the ciliary ganglion from the stem of the third nerve has led to the erroneous view (disproved by the researches of Marshall and Schwalbe) that the ciliary ganglion belongs to the fifth nerve. The connecting branch of the fifth nerve often becomes directly continuous with the anterior branch of the third nerve, and the two together probably constitute the nerve known as the ramus ophthalmicus profundus (Marshall). Further embryological investigations will be required to shew whether this nerve is homologous with the nasal branch of the fifth nerve in Mammalia.

Relations of the nerves to the head-cavities. The cranial nerves, whose development has just been given, bear certain very definite relations to the mesoblastic structures in the head, of the nature of somites, which are known as the head-cavities. Each cranial nerve is typically placed immediately behind the head-cavity of its somite. Thus the main branch of the fifth nerve lies in contact with the posterior wall of the mandibular cavity, as shewn in section in fig. 272 V. ipp and in surface view in fig. 271 ; the main branch of the seventh nerve occupies a similar position in relation to the hyoid cavity ; and, as Marshall has recently shewn, the main branch of the third nerve adjoins the posterior border of the front


462


CRANIAL NERVES.


cavity, described by me as the premandibular cavity. Owing to the early conversion of the walls of the posterior headcavities into muscles, their relations to the nerves are not quite so clear as in the case of the anterior cavities, though, as far as is known, they are precisely the same.

Anterior nerve-roots in the brain.

During my investigations on the development of the cranial nerves I was unable to find any roots comparable with the anterior roots of the spinal nerves, and propounded an hypothesis (suggested by the absence of anterior spinal roots in Amphioxus 1 ) that the head and trunk had become differentiated from each other at a stage when mixed motor and sensory posterior roots were the only roots present, and I supposed the cranial and spinal nerves to have been independently evolved from a common ground form, the resulting types of nerves being so different that no roots strictly comparable with the anterior roots of spinal nerves were to be found in the cranial nerves.

The views put forward by me on this subject, though accepted by Schwalbe


Vll



FIG. 272. TRANSVERSE SECTION THROUGH THE FRONT PART OF THE HEAD OF A YOUNG PRISTIURUS

EMBRYO.

The section, owing to the cranial flexure, cuts both the fore- and the hind-brain. It shews the pramandibular and mandibular head-cavities \pp and ipp, etc.

fb. fore-brain; /. lens of eye; m. mouth ; pt. upper end of mouth, forming pituitary involution; \ao. mandibular aortic arch; ipp. and ipp. first and second head-cavities ; ivc. first visceral cleft ; V. fifth nerve ; aun. ganglion of auditory nerve ; VII. seventh nerve ; aa. dorsal aorta ; acv. anterior cardinal vein ; ch. notochord.


(No. 357), have in other quarters not met with much favour. Wiedersheim holds that it is impossible to believe that the cranial nerves are simpler than the spinal nerves. Such simplicity, which is clearly not found, I have never asserted to exist ; I have only stated that the cranial nerves, in acquiring the complicated character they have in the adult, do not develop anterior roots comparable with those of the spinal nerves. Marshall also strongly objects to my views, and has made some observations for the purpose of testing them, leading to some very interesting results, which I proceed to state, and I will then explain my opinion concerning them.

The most important observation of Marshall on this subject concerns the sixth nerve. In both the Chick and Scy Ilium he has detected a nerve (the first development of which has unfortunately not been made out) arising by a series of roots from the base of the hind-brain. By tracing this nerve to the external rectus muscle of the eye he has satisfactorily identified


1 Schneider holds that anterior roots are present in Amphioxus, but I have been unable to satisfy myself of their presence.


NERVOUS SYSTEM OF THE VERTEBRATA. 463

it as the sixth nerve. " Neither in the nerve nor in its roots are there any ganglion cells." This nerve he finds to be placed vertically below the roots of the seventh nerve ; and it is not visible till much later than the cranial nerves above described.

In addition to this nerve Marshall has found, both in the third nerve and in the fifth nerve, a series of non-gangliated roots, which arise in a manner not yet satisfactorily elucidated, considerably later than, and in front of, the main roots. These roots join the gangliated roots on the proximal side of the ganglion or in the ganglion 1 ; and Marshall believes them to be homologous with the anterior roots of spinal nerves, while he holds the sixth nerve to be an anterior root of the seventh nerve.

In addition to these nerves Marshall holds certain ventral roots, which occur in Elasmobranchs close to the boundary of the spinal cord and medulla, and which probably form the hypoglossal nerve of higher types, to be anterior roots of the vagus. It is very difficult to prove anything definitely about these nerves, but, for reasons stated in my work on Elasmobranch Fishes, I am inclined to regard them as anterior roots of one or more spinal nerves.

Before attempting to decide how far Marshall's views about the so-called anterior roots of the seventh, the fifth and the third nerves are well founded it will conduce to clearness to state the characters and relations of the two roots of spinal nerves.

The posterior root is (i) always purely sensory ; (2) it always develops a ganglion. The anterior root is (i) always purely motor ; (2) it always joins the posterior root below the ganglion, except in Petromyzon (though not in Myxine) where the two roots are stated to be independent.

How far do Marshall's anterior and posterior roots of the cranial nerves exhibit these respective peculiarities ?

With reference to the sixth and seventh nerves he states " we must regard the sixth nerve as having the same relation to the seventh that the anterior root of a spinal nerve has to the posterior root." On this I would remark (i) that the posterior root of this nerve is a mixed sensory and motor nerve and therefore differs in a very fundamental point from that of a spinal nerve ; (2) the sixth nerve though resembling the anterior root of a spinal nerve in being motor and without a ganglion, differs from the nearly universal arrangement of spinal nerves in not uniting with the seventh.

With reference to the fifth nerve it is to be observed that it is by no means certain that the whole of the motor fibres are supplied by the socalled anterior roots, and that these roots differ again in the most marked manner from the anterior roots of spinal nerves in joining the main root of the nerve above (nearer the brain), and not as in a spinal nerve below the

1 These non-gangliated roots of the fifth nerve are not to be confounded with the motor root of the fifth nerve in higher types. They appear to form the anterior root of the adult which gives origin to the ramus ophthalmicus.


464 CRANIAL NERVES.


ganglion. The gangliated root of the third nerve is purely motor 1 , and its so-called anterior roots again differ from the anterior roots of spinal nerves, in the same manner as those of the fifth nerve.

With reference to the glossopharyngeal and vagus nerves I would merely remark that no anterior root has even been suggested for the glossopharyngeal nerve and that the posterior roots of both these nerves contain a mixture of sensory and motor fibres.

In view of these facts, my original hypothesis appears to me to be confirmed by Marshall's observations.

The fact of all the posterior roots of the above cranial nerves (except the third which may be purely motor) being mixed motor and sensory roots appears to me to demonstrate that the starting-point of their differentiation was a mixed nerve with a single dorsal root ; and that they did not therefore become differentiated from nerves built on the same type as the spinal nerves with dorsal sensory and ventral motor roots. The presence of such non-gangliated roots as those of the third and fifth nerves is not a difficulty to this view. Considering that the cranial nerves are more highly differentiated than the spinal nerves, and have more complicated functions to perform, it would be surprising if there had not been developed nonganglionated roots analogous to, but not of course homologous with, the anterior roots of the spinal nerves 2 .

As to the sixth nerve further embryological investigations are requisite before its true position in the series can be determined ; but it appears to me very probable that it is a product of the differentiation of the seventh nerve.

The fourth nerve. No embryological investigations have been made with reference to the fourth nerve. It is possible that it is a segmental nerve comparable with the third nerve, and that the only remnant still left of the segment to which it belongs is the superior oblique muscle of the eye. If this is the case there must have been two praemandibular segments, viz. that belonging to the third nerve, and that belonging to the fourth nerve. Against this view of the fourth nerve is the fact, urged with great force by Marshall, that the superior oblique muscle is in front of the other eye muscles, and that the fourth nerve therefore crosses the third nerve to reach its destination.

The Olfactory nerve. It was shewn in my monograph on Elasmobranch Fishes that the olfactory nerve grew out from the brain in the

1 If Marshall's view about the ramus ophthalmicus profundus (p. 461) is correct, the third must still be, as it no doubt was primitively, a mixed motor and sensory nerve.

2 In the higher types, as is well known, the fifth nerve has its roots formed on the same type as a spinal nerve. The fact that this is not the case in the lower types, either in the embryo or the adult, is a clear indication, to my mind, that the mammalian arrangement of the roots of the fifth nerve has been secondarily acquired, a fact which is a most striking confirmation of my views as to the differences between the cranial and spinal nerves.


NERVOUS SYSTEM OF THE VERTEBRATA. 465

same manner as other nerves ; and Marshall (No. 355), to whom we are indebted for the greater part of our knowledge on the development of this nerve, has proved that it arises prior to the differentiation of the olfactory lobes.

The earliest stages in the development of the nerve have not been made out. Marshall, as already stated, finds that in the Chick the neural crest is continued in front of the optic vesicles, and holds that this fact is strong a priori evidence in favour of the nerve growing out from it. As mentioned above, note on p. 456, I cannot without further evidence accept Marshall's statements on this point. In any case Marshall has not yet been



FIG. 273. SECTION THROUGH THE BRAIN AND OLFACTORY ORGAN OF AN EMBRYO OF ScvLLiUM. (Modified from figures by Marshall and myself.)

c.h. cerebral hemispheres; ol.v. olfactory vesicle ; olf. olfactory pit; Sch. Schneiderian folds; /. olfactory nerve. The reference line has been accidentally taken through the nerve to the brain; pn. pineal gland.

able again to find an olfactory nerve till long after the disappearance of the neural crest. The olfactory nerve at the next stage observed forms an outgrowth of fusiform cells springing on either side from near the summit of the fore-brain ; and at fifty hours it ends close to a slight thickening of the epiblast forming the first rudiment of the olfactory pit, with the walls of which it soon becomes united.

The growth of the cerebral hemispheres causes its point of insertion in the brain to be relatively shifted ; and on the development of the olfactory lobes (vide pp. 444, 445) it arises from them (fig. 273). In Elasmobranchs there is a large development of ganglion cells near its root. From Marshall's figures these appear also to be present in the Chick, but they do not seem to have been found in other forms. In both Teleostei and Amphibia the olfactory nerves are at first extremely short.

Marshall holds that the olfactory nerve is a segmental nerve equivalent to the third, fifth, seventh etc. nerves. It has been already stated that in my opinion the origin of the olfactory nerves from the fore-brain, which I hold to be the ganglion of the prseoral lobe, negatives this view. The mere fact

B. HI- 30


466 SYMPATHETIC NERVOUS SYSTEM.

of these nerves originating as an outgrowth from the central nervous system is no argument in favour of Marshall's view of their nature ; and even if Marshall's opinion that they arise from the neural crest should turn out to be well founded, this fact would not prove their segmental nature, because their origin from this crest would, as indicated in the next paragraph, merely seem to imply that they primitively arose from the lateral borders of the nerve-plate from which the cerebro-spinal tube has been formed.

Situation of the dorsal roots of the cranial and spinal nerves. The probable explanation of the origin of nerves from the neural crest has already been briefly given (p. 316). It is that the neural crest represents the original lateral borders of the nervous plate, and that, in the mechanical folding of the nervous plate to form the cerebro-spinal canal, its two lateral borders have become approximated in the median dorsal line to form the neural crest. The subsequent shifting of the nerves I am unable to explain, and the meaning of the transient longitudinal commissure connecting the nerves is also unknown. The folding of the neural plate must have extended to the region of the origin of the olfactory nerves, so that, as just stated, there would be no special probability of the olfactory nerves belonging to the same category as the other dorsal nerves from the fact of their springing from the neural crest.


BIBLIOGRAPHY OF THE PERIPHERAL NERVOUS SYSTEM.

(351) F. M. Balfour. "On the development of the spinal nerves in Elasmobranch Fishes." Philosophical Transactions, Vol. CLXVI. 1876; vide also, A monograph on the development of Elasmobranch Fishes. London, 1878, pp. 191 216.

(352) W. His. " Ueb. d. Anfange d. peripherischen Nervensystems." Archiv f. Anat. it. Physiol., 1879.

(353) A. M. Marshall. " On the early stages of development of the nerves in Birds." Journal of Anat. and P/iys.,No\. xi. 1877.

(354) A. M. Marshall. "The development of the cranial nerves in the Chick." Quart, y. of Micr. Science, Vol. xvm. 1878.

(355) A. M> Marshall. "The morphology of the vertebrate olfactory organ." Quart. J. of Micr. Science, Vol. xix. 1879.

(356) A. M. Marshall. " On the head-cavities and associated nerves in Elasmobranchs." Quart. J. of Micr. Science, Vol. xxi. 1881.

(357) C. Schwalbe. "Das Ganglion oculomotorii." Jenaische Zeitschrift, Vol. xili. 1879.

Sympathetic nervous system.

The discovery that the spinal and cranial nerves together with their ganglia were formed from the epiblast was shortly afterwards extended to the sympathetic nervous system, which has now been shewn to arise in connection with the spinal and


NERVOUS SYSTEM OF THE VERTEBRATA.


467


cranial nerves. The earliest observations on this subject were those contained in my Monograph on Elasmobranck Fishes (P- T 73)> while Schenk and Birdsell (No. 361) have since arrived at the same result for Aves and Mammalia.

In my account of the development of these ganglia, it is stated that they were first met with as small masses situated at the ends of short branches of the spinal nerves (fig. 275 sy.g). More recent investigations have shewn me that the sympathetic ganglia are at first simply swellings on the main branches of the spinal nerves some way below the ganglia. Their situation may be understood from fig. 274, sy.g, which belongs however to a somewhat later stage. Subsequently the sympathetic ganglia become removed from the main stem of their respective nerves, remaining however connected with those stems by a short branch (fig. 275, sy.g). I have been unable to find a longitudinal commissure connecting them in their early stages; and I presume that they are at first independent, and become subsequently united into a continuous cord on each side.

The observations of Schenk and Birdsell on the Mammalia seem to indicate that the main parts of the sympathetic system arise in continuity with the posterior spinal ganglia : they also shew that in the neck and other parts the sympathetic cords arise as a continuous ganglionic chain. The observations on the topographical features of the development of the sympathetic system in higher types are however as yet very imperfect.

The later history of the sympathetic ganglia is intimately bound up with that of the so-called supra-renal bodies, which are dealt with in another chapter.



FIG. 274. LONGITUDINAL VERTICAL SECTION THROUGH PART OF THE BODY WALL OF AN ELASMOBRANCH EMBRYO SHEWING PARTOFTWOSPINAL NERVES AND THESYMPATHETICGANGLIA BELONGING TO THEM.

ar. anterior root ; pr. posterior root ; sy.g. sympathetic ganglion ; tnp. part of muscle-plate.


302


468


SYMPATHETIC NERVOUS SYSTEM.



time.


FIG. 275. TRANSVERSE SECTION THROUGH THE ANTERIOR PART OF THE TRUNK OF AN EMBRYO OF SCYLLIUM SLIGHTLY OLDER THAN FIG. 29 B.

The section is diagrammatic in the fact that the anterior nerve-roots have been inserted for their whole length ; whereas they join the spinal cord half-way between two posterior roots.

sp.c. spinal cord; sp.g. ganglion of posterior root; ar, anterior root; d.n. dorsally directed nerve springing from posterior root; mp. muscle plate; mp'. part of muscle plate already converted into muscles ; mp. /. part of muscle plate which gives rise to the muscles of the limbs; /. nervus lateralis; ao. aorta; ch. notochord; sy.g. sympathetic ganglion; ca.v. cardinal vein; sp.n. spinal nerve; sd. segmental (archinephric) duct; st. segmental tube; dn. duodenum; pan. pancreas; hp.d. point of junction of hepatic duct with duodenum; nmc. umbilical canal.


NERVOUS SYSTEM OF THE VEKTEBRATA. 469


BIBLIOGRAPHY OF THE SYMPATHETIC NERVOUS SYSTEM.

(360) F. M. Balfour. Monograph on the development of Elasmobranch Fishes. London, 1878, p. 173.

(361) S. L. Schenk and W. R. Birdsell. "Ueb. d. Lehre vond. Entwicklung d. Ganglien d. Sympatheticus. " Mittheil. a. d. embryologischen histit. Wien, Heft in. 1879.


CHAPTER XVI. ORGANS OF VISION.

IN the lowest forms of animal life the whole surface is sensitive to light, and organs of vision have no doubt arisen in the first instance from limited areas becoming especially sensitive to light in conjunction with a deposit of pigment. Lens-like structures, formed either as a thickening of the cuticle, or as a mass of cells, were subsequently formed ; but their function was not, in the first instance, to throw an image of external objects on the perceptive part of the eye, but to concentrate the light on it. From such a simple form of visual organ it is easy to pass by a series of steps to an eye capable of true vision.

There are but few groups of the Metazoa which are not provided with optic organs of greater or less complexity.

In a large number of instances these organs are placed on the anterior part of the head, and are innervated from the anterior ganglia. It is possible that many of the eyes so situated may be modifications of a common prototype. In other instances organs of vision are situated in different regions of the body, and it is clear that such eyes have been independently evolved in each instance.

The percipient elements of the eye would invariably appear to be cells, one end of each of which is continuous with a nerve, while the other terminates in a cuticular structure, or indurated part of the cell forming what is known as the rod or cone.

The presence of such percipient elements in various eyes is therefore no proof of genetic relationship between these eyes* but merely of similarity of function.

Embryological data as to the development of the eye do not


ORGANS OF VISION.


471


exist except in the case of the Arthropoda, Mollusca and Chordata. From such data as there are, combined with study of the adult structure of the eye, it can be shewn that two types of development are found. In one of these the percipient elements are formed from the central nervous system, in the other from the epidermis. The former may be called cerebral eyes. It is probable however that this distinction is not, in all cases at any rate, so fundamental as might be supposed ; but that in both instances the eye may have taken its origin from the epidermis. In the eyes in which the retina is continuous with the central nervous system, these two organs were probably evolved simultaneously as differentiations of the epidermis, and continue to develop together in the ontogenetic growth of the eye.

Some of the eyes in which the retina is formed from the epidermis have also probably arisen simultaneously with part of the central nervous system, while in other instances they have arisen as later formations subsequently to the complete establishment of a central nervous system.

Coelenterata. The actual evolution of the eye is best shewn in the Hydrozoa. The simplest types are those found in Oceania and Lizzia 1 . In "Lizzia. the eye is placed at the base of a tentacle and consists of (fig. 276) a lens (/) and a percipient bulb (oc). The lens is a simple thickening of the cuticle, while the percipient part of the eye is formed of three kinds of elements: (i) pigment cells; (2) sense cells, forming the true retinal elements, and consisting of a central swelling with the nucleus, a peripheral process representing a hardly differentiated rod, and a central process continuous with (3) ganglion cells at the base of the eye. In this eye there is present a commencing differentiation of a ganglion as well as of a retina.

The eye of Oceania is simpler than that of Lizzia in the absence of a lens. Claus has shewn that in



oc.


(From Lankester; after Hertwig.)

/. lens; oc. perceptive part of eye.


1 O. and R. Hertwig. Das Nei~uen system #. Sinnesorgane d. Medtisen. 1878.


Leipzig,


472


MOLLUSCA.


Charybdea amongst the Acraspeda a more highly differentiated eye is present, with a lens formed of cells like the vertebrate eye.

Mollusca. In a large number of the odontophorous Mollusca eyes, innervated by the supracesophageal ganglia, are present on the dorsal side of the head. These eyes exhibit very various degrees of complexity, but are shewn both by their structure and development to be modifications of a common prototype.

The simplest type of eye is that found in the Nautilus, and although the possibility of this eye being degenerated must be borne in mind, it is at the same time very interesting to note (Hensen) that it retains permanently the early embryonic structure of the eyes of the other groups.

It has (fig. 277 A) the form of a vesicle, with a small opening in the outer wall, placing the cavity of the vesicle in free communication with the exterior. The cells lining the posterior face of the vesicle form a retina (7?); and are continuous with the fibres of the optic nerve (N.op). We have no knowledge of the development of this eye.

In the Gasteropods the eye (fig. 277 B) has the form of a closed vesicle: the cells lining the inner side form the retina, while the outer wall of the vesicle constitutes the cornea. A



N.op


G.op


FIG. 277. THREE DIAGRAMMATIC SECTIONS OF THE EYES OF MOLLUSCA.

(After Grenacher.) A. Nautilus. B. Gasteropod (Limax or Helix). C. Dibranchiate Cephalopod.

Pal. eyelid; Co. cornea; Co.ep. epithelium of ciliary body ; Ir. iris; Int, Int" 1 ... Int*. different parts of the integument; /. lens; I 1 , outer segment of lens; R. retina; N.op. optic nerve; G.op. optic ganglion; x. inner layer of retina; N.S. nervous stratum of retina.


ORGANS OF VISION. 473


cuticular lens is placed in the cavity, on the side adjoining the cornea. This eye originates from the ectoderm, within the velar area, and close to the supra-cesophageal ganglia, usually at the base of the tentacles. According to Rabl (Vol. II. No. 268) it is formed as an invagination, the opening of which soon closes ; while according to Bobretzky (Vol. II. No. 242) and Fol it arises as a thickening of the epiblast, which becoming detached takes the form of a vesicle. It is quite possible that both types of development may occur, the second being no doubt abbreviated. The vesicle, however formed, soon acquires a covering of pigment, except for a small area of its outer wall, where the lens becomes formed as a small body projecting into the lumen of the vesicle. The lens seems to commence as a cuticular deposit, and to grow by the addition of concentric layers. The inner wall of the vesicle gives rise to the retina.

The most highly differentiated molluscan eye is that of the Dibranchiate Cephalopoda, which is in fact more highly organized than any other invertebrate eye.

A brief description of its adult structure l will perhaps render more clear my account of the development. The most important features of the eye are shewn in fig. 277 C. The outermost layer of the optic bulb forms a kind of capsule, which may be called the sclerotic. Posteriorly the sclerotic abuts on the cartilaginous orbit, which encloses the optic ganglion (G. op~) ; and in front it becomes transparent and forms the cornea Co, which may be either completely closed, or (as represented in the diagram) perforated by a larger or smaller opening. Behind the cornea is a chamber known as the anterior optic chamber. This chamber is continued back on each side round a great part of the circumference of the eye, and separates the sclerotic from a layer internal to it.

In the anterior optic chamber there are placed (i) the anterior part of the lens (7 1 ) and (2) the folds of the iris (Ir). The whole chamber, except the part formed by the lens, is lined by the epidermis (InP and Infi}. Bounding the inner side of the anterior optic chamber is a layer which is called the choroid (Int 1 } which is continued anteriorly into the fold of the iris (Ir). The most superficial layer of the choroid is the epithelium already mentioned, next comes a layer of obliquely placed plates known as the argentea externa, then a layer of muscles, and finally the argentea interna. The argentea interna abuts on a cartilaginous capsule, which completely invests the inner part of the eye.

The lens is a nearly spherical body composed of concentric lamellae of a structureless material. It is formed of a small outer (7 1 ) and large inner

1 Vide Hensen, Zeit. f. wiss. Zool. Bd. XV.


474 CEPHALOPODA.


(/) segment, the two being separated by a thin membrane. It is supported by a peculiar projection of the wall of the optic cup, known as the ciliary body (Co.ep), inserted at the base of the iris, and mainly formed of a continuation of the retina. This body is however muscular, and presents a series of folds on its outer and inner surfaces, which are especially developed on the latter.

The membrane dividing the lens into two parts is continuous with the ciliary body. Within the lens is the inner optic chamber, bounded in front by the lens and the ciliary body, and behind by the retina.

The retina is formed of two main divisions, an anterior division adjoining the inner optic chamber, and a posterior division (N.S) adjoining the cartilage of the choroid. The two layers are separated by a membrane. Passing from within outwards the following layers in the retina may be distinguished :

(1) Homogeneous membrane. | Anterior division of

(2) Layer of rods. retina

(3) Layer of granules imbedded in pigment. J

(4) Cellular layer.


(5) Connective tissue layer.


Posterior layer of retina.


(6) Layer of nerve-fibres.

At the side of the optic ganglion is a peculiar body, known as the white body (not shewn in the figure), which has the histological characters of glandular tissue.

The first satisfactory account of the development of the eye is due to Lankester (No. 365). The more important features in it were also independently worked out by Grenacher (No. 363), and are beautifully illustrated in Bobretzky's paper (No. 362). The eye first appears as an oval pit of the epiblast, the edge of which is formed by a projecting rim (fig. 278 A). The epiblast

A



FlG. 278. TWO SECTIONS THROUGH THE DEVELOPING EYE OF A CEI'HALUl'OD

TO SHEW THE FORMATION OF THE OPTIC CUP. (After Lankester.)

layer lining the floor of the pit soon becomes considerably thickened. By the growth inwards of the rim the mouth of the pit


ORGANS OF VISION.


475


is gradually narrowed (fig. 278 B), resembling at this stage the eye of Nautilus, and finally closed. There is thus formed a flattened sack, lined by epiblast, which may be called the primary optic vesicle. Its cavity eventually forms the inner optic chamber. The anterior wall of the sack is lined by a much less columnar layer than the posterior, the former giving rise to the epithelium on the inner side of the ciliary processes, the latter to the retina. The cavity of the sack rapidly enlarges, and assumes a spherical form. At the same time a layer of mesoblast grows in between the walls of the sack and the external epiblast.



FIG. 279. TRANSVERSE SECTION THROUGH THE HEAD OF AN ADVANCED EMBRYO OF LoLlGO. (After Bobretzky.)

gls. salivary gland; g.vs. visceral ganglion; gc. cerebral ganglion; g.op. optic ganglion; adk. optic cartilage; ak. and_y. lateral cartilage or (?) white body; rt. retina; gm. limiting membrane of retina ; vk, ciliary region of eye ; cc. iris ; ac. auditory sack (the epithelium lining the auditory sacks is not represented) ; vc. vena cava ; ff. folds of funnel ; x, epithelium of funnel.

Two new structures soon arise nearly simultaneously (fig. 279), which become in the adult eye the iris (cc) and the posterior segment of the lens. The iris is formed as a circular fold of the skin in front of the optic vesicle. It consists both of epiblast and mesoblast, and gives rise to a pit lined by epiblast. The posterior segment of the lens arises as a structureless rod-like body, which is shewn in fig. 279 depending from the inner side


476 CEPHALOPODA.


of the anterior wall of the optic vesicle. Its exact mode of origin is somewhat obscure. The following is Lankester's account of it 1 : "It is formed entirely within the primitive optic chamber, and at first depends as a short cylindrical rod from the middle point of the anterior wall of that chamber, that is to say, from the point at which the chamber finally closed up. It grows subsequently by the deposition of concentric layers of a horny material round this cone. No cells appear to be immediately concerned in effecting the deposition, and it must be looked upon as an organic concretion, formed from the liquid contained in the primitive optic chamber."

The lens would thus appear to be a cuticular structure. It gradually assumes a nearly spherical form ; and is then composed of concentrically arranged layers (fig. 280, /if).

While the lens is being formed, the ciliary epithelium of the optic vesicle becomes divided into two layers, an outer layer of large cells and an inner of small cells. Both layers are at first continuous across the anterior wall of the optic chamber in front of the lens, but soon become confined to the sides (fig. 280 A, cc and gz). The inner layer is stated by Lankester to give rise to the muscles present in the adult. The mesoblast cells also disappear from the region in front of the lens, and the outer epithelium is converted into a kind of cuticular membrane. By these changes the original layers of cells in front of the lens become reduced to mere membranes, a change which appears to be preparatory to the appearance of the anterior segment of the lens. The formation of the latter has not been fully followed out by any investigator except Bobretzky. His figures would seem to indicate that it is formed as a cuticular deposit in front of the membrane already spoken of (fig. 280 B, vl). The two segments of the lens appear at any rate to be separated by a membrane continuous with the ciliary region of the optic vesicle.

Grenacher believes that the front part of the lens is formed in a pocketlike depression of the epiblastic layer covering the outer side of the optic cup ; and Lankester thinks that the lens " pushes its way through the median anterior area of the primitive optic chamber, and projects into the second or anterior optic chamber where the iridian folds lie closely upon it."

1 "Devel. of Cephalopoda." Q. J. Micro. Scien. 1875, p. 44.


ORGANS OF VISION.


477


While the lens is attaining its complete development there appears a fresh fold round the circumference of the eye, which gradually grows inwards so as to form a chamber outside the parts already present. This chamber is the anterior optic chamber of the adult. In most Cephalopods (fig. 277 C) the edges of the fold do not quite meet, but leave a larger or smaller aperture leading into the chamber containing the iris, outer segment of the lens, etc. In some forms however they meet and coalesce, and so shut off this chamber from communication with the exterior. The edge of the fold constitutes the cornea while the remainder of it gives rise to the sclerotic.

The retina is at first a thick layer of numerous rows of oval



<>



FIG. 280. SECTIONS THROUGH THE DEVELOPING EYE OF LOLIGO

AT TWO STAGES. (After Bobretzky.)

///. inner segment of lens ; vl. outer segment of lens ; a and a. epithelium lining the anterior optic chamber; gz. large epiblast cells of ciliary body; cc. small epiblast cells of ciliary body ; ms . layer of mesoblast between the two epiblastic layers of the ciliary body; of. and if. fold of iris; rt. retina; rt". inner layer of retina; st. rods ; aq. cartilage of the choroid.


478 ONCHIDIUM.


cells (fig. 279). When the inner segment of the lens is far advanced towards its complete formation pigment becomes deposited in the anterior part of the retina, and a layer of rods grows out from the surface turned towards the cavity of the optic vesicle (fig. 280 A, st). At a slightly later stage the retina becomes divided into two layers (Bobretzky), a thicker anterior layer, and a thinner posterior layer (fig. 280, rt and rf}. The former is composed of two strata, (i) the rods and (2) a stratum with numerous rows of nuclei which becomes in the adult the granular layer with its pigment. The posterior layer gives rise to the cellular part of the posterior division of the retina, while layers of connective tissue around it give rise to the connective tissue of this portion of the retina (layer 6 in the scheme on p. 474). The nervous layer is derived from the optic ganglion which attaches itself to the inner side of the connective tissue layer.

The greater part of the choroid is formed from the mesoblast adjoining the retina, but the epithelium covering its outer wall is of epiblastic origin.

It is difficult to decide from development whether the Molluscan eyes, so far dealt with, originated in the first instance part passu with the supra-cesophageal ganglia or independently at a later period. On purely a priori ground I should be inclined to adopt the former alternative.

In addition to the above eyes there occur amongst Mollusca highly complicated eyes, of a very different kind, in two widely separated groups, viz. certain species of a genus of slug (Onchidium), and certain Lamellibranchiata. These eyes, though they have no doubt been evolved independently of each other, present certain remarkable points of agreement. In both of them the rods of the retina are turned away from the surface, and the nerve-fibres are placed, as in the Vertebrate eye, on the side of the retina which faces outwards.

The peculiar eyes of Onchidium, investigated by Semper 1 , are scattered on the dorsal surface, there being normal eyes in the usual situation on the head. The eyes on the dorsal surface are formed of a cornea, a lens composed of i 7 cells, and a retina surrounded by pigment ; which is perforated in the centre by an optic nerve, the retinal elements being in the inverted position above mentioned.

The development of these eyes has been somewhat imperfectly studied in the adult, in which they continue to be formed anew. They arise by a

1 Ueber Sehorgane von Typus d. Wirbdthieraugen, etc., Wiesbaden, 1877, anf l Archiv f. mikr. Anat. Vol. xiv. pp. 118 122.


ORGANS OF VISION. 479


differentiation of the epidermis at the end of a papilla. At first a few glandular cells appear in the epidermis in the situation where an eye is about to be formed. Then, by a further process of growth, an irregular mass of epidermic cells becomes developed, which pushes the glandular cells to one side, and constitutes the rudiment of the eye. This mass, becoming surrounded by pigment, unites with the optic nerve, and its cells then differentiate themselves, in situ, into the various elements of the eye. No explanation is offered by Semper of the inverted position of the rods, nor is any suggested by his account of the development. As pointed out by Semper these eyes are no doubt modifications of the sensory epithelium of the papillce.

The eyes of Pecten and Spondylus 1 are placed on short stalks at the edge of the mantle, and are probably modifications of the tentacular processes of the mantle edge. They are provided with a cornea, a cellular lens, a vitreous chamber, and a retina. The retinal elements are inverted, and the optic nerve passes in at the side, but occupies, in reference to its ramifications, the same relative situation as the optic nerve in the Vertebrate eye. The development has unfortunately not yet been studied.

Our knowledge of the structure or still more of the development of the organ of vision of the Platyelminthes, Rotifera, and Echinodermata is too scanty to be of any general interest.

Chaetopoda. Amongst the Chaetopoda the cephalic eyes of Alciope (fig. 281) have been adequately investigated as to their anatomy by Greeff. These are provided with a large cuticular lens (/), separated from the retina by a wide cavity containing the vitreous humour. The retina is formed of a single row of cells, with rods at their free extremities, continuous at their opposite ends with nerve-fibres. The development of this eye has not been worked out. Eyes not situated on the head are found in Polyophthalmus, and have probably been evolved from the more indifferent type of senseorgan found by Eisig in the allied Capitellidas.

Chaetognatha 2 . The paired cephalic eyes of Sagitta are spherical bodies imbedded in the epidermis. They are formed of a central mass of pigment with three lenses partially imbedded in it. The outer covering of the eye is the retina, which is mainly composed of rod-bearing cells ; the rods being placed in contact with the outer surface of each of the lenses. In the presence of three lenses the eye of Sagitta approaches in some respects the eye of the Arthropoda.

Arthropodan eye. A satisfactory elucidation of the phylogeny of Arthropodan eyes has not yet been given.

All the types of eyes found in the group (with exception of

1 Vide Hensen (No. 364) and S. J. Hickson, "The Eye of Pecten," Quart. J. of Micr. Science, Vol. xx. 1 880.

2 O. Hertwig. " Die Chaetognathen." Jenaischc Zcitschrift, Vol. XTV. 1880.


480 ARTHROPODA.


that of Peripatus) 1 present marked features of similarity, but I am inclined to view this similarity as due rather to the character of the exoskeleton modifying in a more or less similar way all the forms of visual organs, than to the descent of all these eyes from a common prototype. In none of these eyes is there present a chamber filled with fluid between the lens and the



FIG. 281. EYE OF AN ALCIOPID (NEOPHANTA CELOX). (From Gegenbaur;

after Greef.)

i. cuticle; c. continuation of cuticle in front of eye; /. lens; h. vitreous humour; o. optic nerve; o. expansion of the optic nerve; b. layer of rods; /. pigment layer.

retina, but the space in question is filled with cells. This character sharply distinguishes them from such eyes as those of Alciope (fig. 281). The types of eyes which are found in the Arthropoda are briefly the following :

(i) Simple eyes. In all simple eyes the corneal lens is formed by a thickening of the cuticle. Such eyes are confined to the Tracheata.

There are three types of simple eyes, (a) A type in which the retinal cells are placed immediately behind the lens, found

1 The eye of Peripatus is similar neither to the eye of the Arthropoda, nor to that of the Choetopoda, but resembles much more closely the Molluscan eye. The hypodermis and cuticle form together a highly convex cornea, within which is a large optic chamber, the posterior wall of which is formed by the retina. The optic chamber would appear to contain a structureless lens, but it is possible that what I regard as a lens may, on fuller investigation, turn out to be only a coagulum.


ORGANS OF VISION.


481



(Lowne) in the larvae of some Diptera (Eristalis), and also in some Chilognatha.

(b] A type of simple eye found in some Chilopoda, and in some Insect larvae (Dytiscus, etc.) (fig. 282), the parts of which are entirely derived from the epidermis. There is present a lens (/) formed as a thickening of the cuticle, a so-called vitreous humour (gl] formed of modified hypodermis cells, and a retina (r) derived from the same source.

The outer ends of the retinal cells terminate in rods, and their inner ends are continuous with nervefibres.

(c) A type of simple eye found in the Arachnida, and apparently some Chilopoda, and forming the simple eyes of most Insects, which differs from type (a) in the cells of the retina forming a distinct layer beneath the hypodermis ; the latter only obviously giving rise to the vitreous humour.

The development of the simple eyes has not yet been studied.

The simple eyes so far described are always placed on the head, and are usually rather numerous.

(2) Compound eyes. Compound eyes are almost always present in the Crustacea, and are usually found in adult Insects. In both groups they are paired, though in the Crustacea a median much simplified compound eye may either take the place of the paired eyes in the Nauplius larva and lower forms, or be present together with them during a period in the development of higher forms.

The typical compound eye is formed (fig. 283) of a series of corneal lenses (c) developed from the cuticle; below which are placed bodies known as the crystalline cones, one to each corneal lens ; and below the crystalline cones are placed bodies known as the retinulae (r) constituting the percipient elements of the eye, each of them being formed of an axial rod, the rhabdom, and a number of cells surrounding it.

B. in. 3 1


FIG. 282. SECTION THROUGH THE SIMPLE EYE OF A YOUNG DYTISCUS LARVA. (From Gegenbaur ; after Grenadier.)

/. corneal lens ; g. vitreous hu mour ; r. retina ; o. optic nerve ; h. hypodermis.


482


ARTHROPODA.


The crystalline cones are formed from the coalescence of cuticular deposits in several cells, the nuclei of which usually remain as Semper's nuclei. These cells are probably simple hypodermis cells, but in some forms, e.g. Phronima, there may be a continuous layer of hypodermis cells between them and the cuticle. In various Insect eyes the cells which usually give rise to a crystalline cone may remain distinct, and such eyes have been called by Grenacher aconouseyes, while eyes with incompletely formed crystalline cones are called by him pseudoconouseyes.

The rhabdom of the retinulae is, like the crystalline cone, developed by the coalescence of a series of parts, which are primitively separate rods placed each in its own cell : this condition of the retinulas is permanently retained in the eyes of the Tipulidae.

The development of the compound eye has so far only been satisfactorily studied in some Crustacea by Bobretzky (No. 367) ; by whom it has been worked out in Palaemon and Astacus, but more fully in the latter, to which the following account refers :

The eye of Astacus takes its origin from two distinct parts, (i) the external epidermis of the procephalic lobes which will be spoken of as the epidermic layer of the eye, (2) a portion of the supracesophageal ganglia, which will be spoken of as the neural layer of the eye. The mesoblast is moreover the source of some of the pigment between the two above layers. The epidermic layer gives rise to the corneal lenses, the crystalline cones, and the pigment around the latter. The neural layer on the other hand seems to give rise to the retinulae with their rhabdoms, and to the optic ganglion.

After the separation of the supra-cesophageal ganglia from the superficial epiblast, the cells of the epidermis in the region of the future eye become columnar, and so form the above-mentioned epidermic layer of the eye. This layer soon becomes two or three cells deep. At the same time the most superficial part of the adjoining supra- oesophageal ganglion becomes partially constricted off from the remainder as the neural layer of the eye, but is separated by a small space from the thickened patch of epidermis.



FIG. 283. DIAGRAMMATIC REPRESENTATIONS OF PARTS OF A COMPOUND ARTHROPOD EYE. (From Gegenbaur.)

A. Section through the eye.

B. Corneal facets.

C. Two segments of the eye.

c. corneal (cuticular) lenses ; r. retinulae with rhabdoms ; n. optic nerve ; g. ganglionic swelling of optic nerve.


ORGANS OF VISION. 483


Into this space some mesoblast cells penetrate at a slightly later period. Both the epidermic and neural layers next become divided into two strata. The outer stratum of the epidermic layer gives rise to the crystalline cones and Semper's nuclei ; each crystalline cone being formed from four coalesced rods, developed as cuticular differentiations of four cells, the nuclei of which may be seen in the embryo on its outer side. The lower ends of the cones pass through the inner stratum of the epidermic disc, the cells of which become pigmented, and constitute the pigment cells surrounding the lower part of the crystalline cones in the adult. The outer end of each of the crystalline cones is surrounded by four cells, believed by Bobretzky to be identical with Semper's nuclei 1 . These cells give rise in a later stage (not worked out in Astacus) to the cuticular corneal lenses.

Of the two strata of the neural layer the outer is several cells deep, while the inner is formed of elongated rod-like cells. Unfortunately however the fate of the two neural layers has not been worked out, though there can be but little doubt that the retinuke originate from the outer layer.

The mesoblast which grows in between the neural and epidermic layers becomes a pigment layer, and probably also forms the perforated membrane between the crystalline cones and the retinulas.

The above observations of Bobretzky would appear to indicate that the paired compound eyes of Crustacea belong to the type of cerebral eyes. How far this is also the case with the compound eyes of Insects is uncertain, in that it is quite possible that the latter eyes may have had an independent origin.

The relation between the paired and median eye of the Crustacea is also uncertain.

In the genus Euphausia amongst the Schizopods there is present a series of eyes placed on the sides of some of the thoracic legs and on the sides of the abdomen. The structure of these eyes, though not as yet satisfactorily made out, would appear to be very different from that of other Arthropodan visual organs.

The Eye of the Vertebrata. In view of the various structures which unite to form it, the eye is undoubtedly the most complicated organ of the Vertebrata ; and though its mode of development is fairly constant throughout the group, it will be convenient shortly to describe what may be regarded as its typical development, and then to proceed to a comparative view of the origin of its various parts, and to enter into greater detail with reference to some of them. At the end of the section

1 There would appear to be some confusion as to the nomenclature of these parts in Bobretzky's account,

31


4 8 4


PRIMARY OPTIC VESICLE.



there is an account of the accessory structures connected with the eye.

The formation of the eye commences with the appearance of a pair of hollow outgrowths from the anterior cerebral vesicle or thalamencephalon, which arise in many instances, even before the closure of the medullary canal. These outgrowths, known as the optic vesicles, at first open freely into the cavity of the anterior cerebral vesicle. From this they soon however become partially constricted, and form vesicles (fig. 284, a], united to the base of the brain by comparatively narrow hollow stalks, the rudiments of the optic nerves. The constriction to which the stalk or optic nerve is due takes place obliquely downwards and backwards, so that the optic nerves open into the base of the front part of the thalamencephalon (fig. 284, ff).

After the establishment of the optic nerves, there take place (i) the formation of the lens, and (2) the formation of the optic cup from the walls of the primary optic vesicle.

The external or superficial epiblast which covers, and is in most forms in immediate contact with, the most projecting portion of the optic vesicle, becomes thickened. This thickened portion is then driven inwards in the form of a shallow open pit with thick walls (fig. 285 A, o), carrying before it the front wall (r) of the optic vesicle. To such an extent does this involution of the superficial epiblast take place, that the front wall of the optic vesicle is pushed close up to the hind wall, and the cavity of the vesicle becomes almost obliterated (fig. 285 B).

The bulb of the optic vesicle is thus converted into a cup with double walls, containing in its cavity the portion of involuted epiblast. This cup, in order to distinguish its cavity from that of the original optic vesicle, is generally called the secondary optic vesicle. We may, for the sake of brevity, speak of it as the optic cup; in reality it never is a vesicle, since it


FIG. 284. SECTION THROUGH THE HEAD OF AN EMBRYO TELEOSTEAN, TO SHEW THE FORMATION OF

THE OPTIC VESICLES, ETC. (From

Gegenbaur; after Schenk.)

c. fore-brain ; a. optic vesicle ; b. stalk of optic vesicle ; d. epidermis.


ORGANS OF VISION OF THE VERTEBRATA.


485



always remains widely open in front. Of its double walls the inner or anterior (fig. 285 .

B, r) is formed from the front portion, the outer or posterior (fig. 285 B, u] from the hind portion of the wall of the primary optic vesicle. The inner or anterior (r), which very speedily becomes thicker than the other, is converted into the retina : in the outer or posterior (), which remains thin, pigment is eventually deposited, and it ultimately becomes the tesselated pigmentlayer of the choroid.

By the closure of its mouth the pit of the involuted epiblast becomes a completely closed sac with thick walls and a small central cavity (fig. 285 B, /). At the same time it breaks away from the external epiblast, which forms a continuous layer in front of it, all traces of the original opening being lost. There is thus left lying in the cup of the secondary optic vesicle, an isolated elliptical mass of epiblast. This is the rudiment of the lens. The small cavity within it speedily becomes still less by the thickening of the walls, especially of the hinder one.

At its first appearance the lens is in immediate contact with the anterior wall of the secondary optic vesicle (fig. 285 B). In a short time however, the lens is seen to lie in the mouth of the cup (fig. 288 D), a space (vh] (which is occupied by the vitreous humour) making its appearance between the lens and anterior wall of the vesicle.

In order to understand how this space is developed, the position of the optic vesicle and the relations of its stalk must be borne in mind.

The vesicle lies at the side of the head, and its stalk is directed downwards, inwards and backwards. The stalk in fact


FIG. 285. DIAGRAMMATIC SECTIONS ILLUSTRATING THE FORMATION OF THE EYE. (After Remak.)

In A the thin superficial epiblast h is seen to be thickened at x, in front of the optic vesicle, and involuted so as to form a pit o, the mouth of which has already begun to close in. Accompanying this involution, which forms the rudiment of the lens, the optic vesicle is doubled in, its front portion r being pushed against the back portion u, and the original cavity of the vesicle thus reduced in size. The stalk of the vesicle is shewn as still broad.

In B the optic vesicle is still further doubled in so as to form a cup with a posterior wall u and an anterior wall r. In the hollow of this cup lies the lens /, now completely detached from the superficial epiblast xh.


486


CHOROID FISSURE.



slants away from the vesicle. Hence, when the involution of the lens takes place, the direction in which the front wall of the vesicle is pushed in is not in a line with the axis of the stalk, as for simplicity's sake has been represented in the diagram (fig. 285), but forms an obtuse angle with that axis, after the manner of fig. 286, where / represents the cavity of the stalk leading away from the almost obliterated cavity of the primary vesicle.

Fig. 286 represents the early stage at which the lens fills the whole cup of the secondary vesicle. The subsequent condition is brought about through the rapid growth of the walls of the cup. This growth however does not take place equally in all parts of the cup. The walls of the cup rise up all round except that point of the circumference of the cup which adjoins the stalk. While elsewhere the walls increase rapidly in height, carrying so to speak the lens with them, at this spot, which in the natural position of the eye is on its under surface, there is no growth : the wall is here imperfect, and a gap is left. Through this gap, which afterwards receives the name of the choroidal fissure, a way is open from the mesoblastic tissue surrounding the optic vesicle and stalk into the interior of the cavity of the cup.

From the manner of its formation the gap or fissure is evidently in a line with the axis of the optic stalk, and in order to be seen must be looked for on the under surface of the optic vesicle. In this position it is readily recognised in the embryo seen as a transparent object (fig. 1 18, chs).

Bearing in mind these relations of the gap to the optic stalk, the reader will understand how sections of the optic vesicle at this stage present very different appearances according to the plane in which the sections are taken.

When the head is viewed from underneath as a transparent


FIG. 286. DIAGRAMMATIC SECTION OF THE EYE AND THE OPTIC NERVE AT AN EARLY STAGE. (From Lieberkiihn.)

To shew the lens / occupying the whole hollow of the optic cup, the inclination of the stalk s to the optic cup, and the continuity of the cavity of the stalk s' with that of the primary vesicle c ; r. anterior, u. posterior wall of the optic cup.


ORGANS OF VISION OF THE VERTEBRATA.


487



object the eye presents very much the appearance represented in the diagram (fig. 287).

A section of such an eye taken along the line y, perpendicular to the plane of the paper, would give a figure corresponding to that of fig. 288 D. The lens, the cavity and double walls of the secondary vesicle, the remains of the primary cavity, would all be represented (the superficial epiblast of the head would also be shewn) ; but there would be nothing seen of either the stalk or the fissure. If on the other hand the section were taken in a plane parallel to the plane of the paper, at some distance above the level of the stalk, some such figure would be obtained as that shewn in fig. 288 E. Here the fissure f is obvious, and the communication of the cavity vh of the secondary vesicle with the outside of the eye evident ; the section of course would not go through the superficial epiblast. Lastly, a section, taken perpendicular to the plane of the paper along the line z, i.e. through the fissure itself, would present the appearances of fig. 288 F, where the wall of the vesicle is entirely wanting in the region of the fissure marked by the position of the letter f. The external epiblast has been omitted in this figure.

With reference to the above description, taken with very slight alterations from the Elements of Embryology, Pt. I., two points require to be noticed. Firstly it is extremely doubtful whether the invagination of the secondary optic vesicle is to be viewed as an actual mechanical result of the ingrowth of the lens. Secondly it seems probable that the choroid fissure is not simply due to an inequality in the growth of the walls of the secondary optic cup, but is partly due to a doubling up of the primary vesicle from the side


FIG. 287. DIAGRAMMATIC REPRESENTATION OF THE EYE OF THE CHICK OF ABOUT THE THIRD DAY AS SEEN WHEN THE HEAD IS VIEWED FROM UNDERNEATH AS A TRANSPARENT OBJECT.

/. the lens ; /'. the cavity of the lens, lying in the hollow of the optic cup ; r. the anterior, u. the posterior wall of the optic cup ; c. the cavity of the primary optic vesicle, now nearly obliterated. By inadvertence u has been drawn in some places thicker than r, it should have been thinner throughout, s. the stalk of the optic cup with s' its cavity, at a lower level than the cup itself and therefore out of focus; the dotted line indicates the continuity of the cavity of the stalk with that of the primary vesicle.

The line z z, through which the section shewn in fig. 288 F is supposed to be taken, passes through the choroidal fissure.


488 SECONDARY OPTIC CUP.

along the line of the fissure, at the same time that the lens is being thrust in in front. In Mammalia, the doubling up involves the optic stalk, which becomes flattened (whereby its original cavity is obliterated) and then folded in on itself, so as to embrace a new central cavity continuous with the cavity of the vitreous humour. And in other forms a partial phenomenon of the same kind is usually observable, as is more particularly described in the sequel.

Before describing the development of the cornea, aqueous humour, etc. we may consider the further .growth of the parts, whose first development has just been described, commencing with the optic cup.

During the above changes the mesoblast surrounding the optic cup assumes the character of a distinct investment, whereby the outline of the eye-ball is definitely formed. The internal portions of this investment, nearest to the retina, become the choroid (i.e. the chorio-capillaris, and the lamina fusca; the pigment epithelium, as we have seen, being derived from the epiblastic optic cup), and pigment is subsequently deposited in it. The remaining external portion of the investment forms the sclerotic.

The complete differentiation of these two coats of the eye does not however take place till a late period.

The cavity of the original optic vesicle was left as a nearly obliterated space between the two walls of the optic cup. By the end of the third day the obliteration is complete, and the two walls are in immediate contact.

The inner or anterior wall is, from the first, thicker than the outer or posterior ; and over the greater part of the cup this contrast increases with the growth of the eye, the anterior wall becoming markedly thicker and undergoing changes of which we shall have to speak directly (fig. 289).

In the front portion however, along, so to speak, the lip of the cup, anterior to a line which afterwards becomes the ora serrata, both layers cease to take part in the increased thickening, accompanied by peculiar histological changes, which the rest of the cup is undergoing. Thus a hind portion or true retina is marked off from a front portion.

The front portion, accompanied by the mesoblast which immediately overlies it, is behind the lens thrown into folds, the


ORGANS OF VISION OF THE VERTEBRATA. 489

ciliary ridges ; while further forward it bends in between the lens and the cornea to form the iris. The original wide opening of the optic cup is thus narrowed to a smaller orifice, the pupil ; and the lens, which before lay in the open mouth of the cup, is now inclosed in its cavity. While in the hind portion of the cup or retina proper no deposit of black pigment takes place in

D

E



FIG. 288.

D. Diagrammatic section taken perpendicular to the plane of the paper, along the linejjy, fig. 287. The stalk is not seen, the section falling quite out of its region. vh. hollow of optic cup filled with vitreous humour ; other letters as in fig. 285 B. (After Remak.)

E. Section taken parallel to the plane of the paper through fig. 287, so far behind the front surface of the eye as to shave off a small portion of the posterior surface of the lens /, but not so far behind as to be carried at all through the stalk. Letters as before ; f. the choroidal fissure.

F. Section along the line zz, perpendicular to the plane of the paper, to shew the choroidal fissure/, and the continuity of the cavity of the optic stalk with that of the primary optic vesicle. Had this section been taken a little to one side of the line zs, the wall of the optic cup would have extended up to the lens below as well as above. Letters as before. The external epiblast is omitted in this section.

the layer formed out of the inner or anterior wall of the vesicle ; in the front portion forming the region of the iris, pigment is largely deposited throughout both layers, though first of all in the outer one, so that eventually this portion seems to become nothing more than a forward prolongation of the pigment epithelium of the choroid.

Thus, while the hind moiety of the optic cup becomes the retina proper, including the choroid-pigment in which the rods and cones are imbedded, the front moiety is converted into the ciliary portion of the retina, covering the ciliary processes, and into the uvea of the iris ; the bodies of the ciliary processes and the substance of the iris, their vessels, muscles, connective tissue and ramified pigment, being derived from the mesoblastic choroid. The margin of the pupil marks the extreme lip of the optic


490


THE RETINA.


vesicle, where the outer or posterior wall turns round to join the inner or anterior.

The ciliary muscle and the ligamentum pectinatum are both derived from the mesoblast between the cornea and the iris.

The Retina. At first the two walls of the optic cup do not greatly differ in thickness. On the third day the outer or posterior becomes much thinner than the inner or anterior, and by the middle of the fourth day is reduced to a single layer of flattened


c.t


p.Ch



FIG. 289. SECTION OF THE EYE OF CHICK AT THE FOURTH DAY.

e.p. superficial epiblast of the side of the head ; /?. true retina : anterior wall of the optic cup; p.Ch. pigment-epithelium of the choroid: posterior wall of the optic cup. b is placed at the extreme lip of the optic cup at what will become the margin of the iris. /. the lens. The hind wall, the nuclei of whose elongated cells are shewn at /, now forms nearly the whole mass of the lens, the front wall being reduced to a layer of flattened cells el. m. the mesoblast surrounding the optic cup and about to form the choroid and sclerotic. It is seen to pass forward between the lip of the optic cup and the superficial epiblast.

Filling up a large part of the hollow of the optic cup is seen a hyaline mass, the rudiment of the hyaloid membrane, and of the coagulum of the vitreous humour, y. In the neighbourhood of the lens it seems to be continuous as at d with the tissue a, which appears to be the rudiment of the capsule of the lens and suspensory ligament.


ORGANS OF VISION OF THE VERTEBRATA. 491

cells (fig. 289, p.C/i). At about the 8oth hour its cells commence to receive a deposit of pigment, and eventually form the so-called pigmentary epithelium of the choroid ; from them no part of the true retina (or no other part of the retina, if the pigment-layer in question be supposed to belong more truly to the retina than to the choroid) is derived.

On the fourth day, the inner (anterior) wall of the optic cup (fig. 289, R) has a perfectly uniform structure, being composed of elongated somewhat spindle-shaped cells, with distinct nuclei. On its external (posterior) surface a distinct cuticular membrane, the membrana limitans externa, early appears.

As the wall increases in thickness, its cells multiply rapidly, so that it soon becomes several cells thick : each cell being however probably continued through the whole thickness of the layer. The wall at this stage corresponds closely in its structure with the brain, of which it may properly be looked upon as part. According to the usual view, which is not however fully supported by the development, the retina becomes divided in the subsequent growth into (i) an outer part, corresponding morphologically to the epithelial lining of the cerebro-spinal canal, composed of what may be called the visual cells of the eye, i.e. the cells forming the outer granular (nuclear) layer and the rods and cones attached to them ; and (2) an inner portion consisting of the inner granular (nuclear) layer, the inner molecular layer, the ganglionic layer and the layer of nerve-fibres corresponding morphologically to the walls of the brain. According to Lowe, however, only the outer limbs of the rods and cones, which he holds to be metamorphosed cells, correspond to the epithelial layer of the brain.

The actual development of the retina is not thoroughly understood. According to the usual statements (Kolliker, No. 298, p. 693) the layer of ganglion cells and the inner molecular layer are first differentiated, while the remaining cells give rise to the rest of the retina proper, and are bounded externally by the membrana limitans externa. On the inner side of the ganglionic layer the stratum of nerve-fibres is also very early established. The rods and cones are formed as prolongations (Kolliker, Babuchin), or cuticularizations (Schultze, W. Miiller) of the cells which eventually form the outer granular layer. The layer of cells external to the molecular layer is not divided till comparatively late into the inner and outer granular (nuclear) layers, and the interposed outer molecular layer.


492 THE OPTIC NERVE.


Lowe's account of the development of the retina in the Rabbit is in many points different from the above. He finds that three stages in the differentiation of the layers of the retina may be distinguished.

In the first stage, in an embryo of four or five millimetres, the following layers are present, commencing at the outer side, adjoining the external wall of the secondary optic cup.

(1) A membrane, which does not however, as usually believed, become the membrana limitans externa.

(2) A layer of clear elements, derived from metamorphosed cells, constituting the outer limbs of the rods and cones.

(3) A layer of dark rounded elements.

(4) An indistinctly striated layer, the future layer of nerve-fibres. The third of these layers gives rise to all the eventual strata of the

retina proper, except the outer limbs of the rods and cones.

In the next stage, when the embryo has reached a length of 2 cm., this layer becomes divided into three strata : viz. an outer and inner layer of dark elements and a middle one of clearer elements. The two inner of these layers become respectively the inner molecular layer and the layer of ganglion cells, while the outer layer gives rise to the parts of the retina external to the inner molecular layer.

In the newly born animal the outer darker layer of the previous stage has become considerably subdivided. Its outermost part forms a stratum of darkly coloured elements, which develop into the inner limbs of the rods and cones. It is bounded internally by a membrane the true membrana elastica externa. The part of the layer within this is soon divided into the outer and inner granular layers, separated from each other by the delicate outer molecular layer. Thus, shortly after birth, all the layers of the retina are established in the Rabbit. It is important to notice that, according to Lowe's views, the outer and inner limbs of the rods and cones are metamorphosed cells. The outer limbs at first form a continuous layer, in which separate elements cannot be recognised.

At a very early period there appears a membrane on the side of the retina adjoining the vitreous humour. This membrane is the hyaloid membrane. The investigations of Kessler and myself lead to the conclusion that it may be formed at a time when there is no trace of mesoblastic structures in the cavity of the vitreous humour, and that it is therefore necessarily developed as a cuticular deposit of the cells of the optic cup. Lieberkiihn, Arnold, Lowe, and other authors regard it however as a mesoblastic product ; and Kolliker believes that a primitive membrane is developed from the cells of the optic cup, and that a true hyaloid membrane is developed much later as a product of the mesoblast.

For fuller information on this subject the reader is referred to the authors quoted above.

The optic nerve. The optic nerves are derived, as we have said, from the at first hollow stalks of the optic vesicles. Their


ORGANS OF VISION OF THE VERTEBRATA. 493

cavities gradually become obliterated by a thickening of the walls, the obliteration proceeding from the retinal end inwards towards the brain. While the proximal ends of the optic stalks are still hollow the rudiments of the optic chiasma are formed from fibres at the roots of the stalks, the fibres of the one stalk growing over into the attachment of the other. The decussation of the fibres would appear to be complete. The fibres arise in the remainder of the nerves somewhat later. At first the optic nerve is equally continuous with both walls of the optic cup ; as must of necessity be the case, since the interval which primarily exists between the two walls is continuous with the cavity of the stalk. When the cavity within the optic nerve vanishes, and the fibres of the optic nerve appear, all connection is ruptured between the outer wall of the optic cup and the optic nerve, and the optic nerve simply perforates the outer wall, and becomes continuous with the inner one.

There does not appear to me any ground for doubting (as has been done by His and Kolliker) that the fibres of the optic nerve are derived from a differentiation of the epithelial cells of which the nerve is at first formed.

Choroid Fissure. With reference to the choroid fissure we may state that its behaviour varies somewhat in the different types. It becomes for the greater part of its extent closed, though its proximal end is always perforated by the optic nerve, and in many forms by a mesoblastic process also.

The lens when first formed is an oval vesicle with a small central cavity, the front and hind walls being of nearly equal thickness, and each consisting of a single layer of elongated columnar cells. In the subsequent stages the mode of growth of the hind wall is of precisely an opposite character to that of the front wall. The hind wall becomes much thicker, and tends to obliterate the central cavity by becoming convex on its front surface. At the same time its cells, still remaining as a single layer, become elongated and fibre-like. The front wall on the contrary becomes thinner and thinner and its cells flattened.

These modes of growth continue until, as shewn in fig. 289, the hind wall / is in absolute contact with the front wall el, and the cavity thus becomes entirely obliterated. The cells of the hind wall have by this time become veritable fibres, which, when


494 THE VITREOUS HUMOUR.

seen in section, appear to be arranged nearly parallel to the optic axis, their nuclei nl being seen in a row along their middle. The front wall, somewhat thickened at either side where it becomes continuous with the hind wall, is now a single layer of flattened cells separating the hind wall of the lens, or as we may now say the lens itself, from the front limb of the lens-capsule ; of the latter it becomes the epithelium.

The subsequent changes undergone consist chiefly in the continued elongation and multiplication of the lens-fibres, with the partial disappearance of their nuclei.

During their multiplication they become arranged in the manner characteristic of the adult lens of the various forms. The lens-capsule, as was originally stated by Kolliker, appears to be formed as a cuticular membrane deposited by the epithelial cells of the lens.

The views of Lieberkiihn, Arnold, Lowe and others, according to which the lens-capsule is a mesoblastic structure, do not appear to be well founded. The contrary view, held by Kolliker, Kessler, etc., is supported mainly by the fact that at the time when the lens-capsule first appears there are no mesoblast cells to give rise to it. It should however be stated that W. Miiller has actually found cellular elements in what he believes to be the lens-capsule of the Ammoccete lens. Considering the degraded character of the Ammoccete eye, evidence derived from its structure must be accepted with caution.

The vitreous humour. The vitreous humour is derived (except in Cyclostomata) from a vascular ingrowth, which differs considerably in different types, through the choroid slit. Its real nature is very much disputed. According to Kessler's view, it is of the nature of a fluid transudation, but the occasional presence in it of ordinary embryonic mesoblast cells, in addition to more numerous blood-corpuscles, gives it a claim to be regarded as intercellular substance. The number of cells in it is however at best extremely small and in many cases there is no trace of them. In Mammals there appear to be some mesoblast cells invaginated with the lens, which are not improbably employed in the formation of the vessels of the so-called membrana capsulopupillaris. In the Ammoccete the vitreous humour originates from a distinct mesoblastic ingrowth, though the cells which give rise to it subsequently disappear.


ORGANS OF VISION OF THE VERTEBRATA. 495


The development of the zonula of Zinn in Mammalia, which ought to throw some light on the nature of the vitreous humour, has not been fully investigated. According to Lieberkiihn (No. 373, p. 43), this structure appears in half-grown embryos of the sheep and calf.

He says "At the point where the ciliary processes and the ciliary part of the retina are entirely removed, one sees in the meridian bundles of fine fibres, which correspond to the valleys between the ciliary processes and fill them ; also between these bundles there extend, as a thin layer, similar finely striated masses, and these would have been on the top of the ciliary processes." He further states that these fibres may be traced to the anterior and posterior limb of the lens-capsule, and that amongst them are numerous cells. Kolliker confirms Lieberkiihn's statements. There can be little doubt that the fibres of the zonula are of the nature of connective tissue : they are stated to be elastic. By Lowe they are believed to be developed out of the substance of the vitreous humour, but this does not appear to me to follow from the observations hitherto made. It seems quite possible that they arise from mesoblast cells which have grown into the cavity of the vitreous humour, solely in connection with their production.

The integral parts of the eye in front of the lens are the cornea, the aqueous humour, and the iris. The development of the latter has already been described, and there remain to be dealt with the cornea, and the cavity containing the aqueous humour.

The cornea. The cornea is formed by the coalescence of two structures, viz. the epithelium of the cornea and the cornea proper. The former is directly derived from the external epiblast, which covers the eye after the invagination of the lens. The latter is formed in a somewhat remarkable manner, first clearly made out by Kessler.

When the lens is completely separated from the epidermis its outer wall is directly in contact with the external epiblast (future corneal epithelium). At its edge there is a small ringshaped space bounded by the outer skin, the lens and the edge of the optic cup. In the chick, which we may take as typical, there appears at about the time when the cavity of the lens is completely obliterated a structureless layer external to the above ring-like space and immediately adjoining the inner face of the epiblast. This layer, which forms the commencement of the cornea proper, at first only forms a ring at the border of the lens, thickest at its outer edge, and gradually thinning off to


496 THE CORNEA.


nothing towards the centre. It soon however becomes broader, and finally forms a continuous stratum of considerable thickness, interposed between the external skin and the lens. As soon as this stratum has reached a certain thickness, a layer of flattened cells grows in along its inner side from the mesoblast surrounding the optic cup (fig. 290, dm). This layer is the epithelioid layer of the membrane of Descemet. After it 1 has become



FIG. 290. SECTION THROUGH THE EYE OF A FOWL ON THE EIGHTH DAY OF DEVELOPMENT, TO SHEW THE IRIS AND CORNEA IN THE PROCESS OF FORMATION. (After Kessler.)

ep. epiblastic epithelium of cornea; cc. corneal corpuscles growing into the structureless matrix of the cornea; dm. Descemet's membrane; ir. iris; cb. mesoblast of the iris (this reference letter points a little too high).

The space between the layers dm. and ep. is filled with the structureless matrix of the cornea.

completely established, the mesoblast around the edge of the cornea becomes divided into two strata ; an inner one (fig. 290, cb) destined to form the mesoblastic tissue of the iris already described, and an outer one (fig. 290, cc] adjoining the epidermis. The outer stratum gives rise to the corneal corpuscles, which are the only constituents of the cornea not yet developed. The corneal corpuscles make their way through the structureless corneal layer, and divide it into two strata, one adjoining the epiblast, and the other adjoining the inner epithelium. The two strata become gradually thinner as the corpuscles invade a larger and larger portion of their substance, and finally the outermost portion of them alone remains as the membrana elastica anterior and posterior (Descemet's membrane) of the cornea. The corneal

1 It appears to me possible that Lieberkiihn may be right in stating that the epithelium of Descemet's membrane grows in between the lens and the epiblast before the formation of the cornea proper, and that Kessler's account, given above, may on this point require correction. From the structure of the eye in the Ammocoete it seems probable that Descemet's membrane is continuous with the choroid.


ORGANS OF VISION OF THE VERTEBRATA. 497

corpuscles, which have grown in from the sides, thus form a layer which becomes continually thicker, and gives rise to the main substance of the cornea. Whether the increase in the thickness of the layer is due to the immigration of fresh corpuscles, or to the division of those already there, is not clear. After the cellular elements have made their way into the cornea, the latter becomes continuous at its edge with the mesoblast which forms the sclerotic.

The derivation of the original structureless layer of the cornea is still uncertain. Kessler derives it from the epiblast, but it appears to me more probable that Kolliker is right in regarding it as derived from the mesoblast. The grounds for this view are, (i) the fact of its growth inwards from the border of the mesoblast round the edge of the eye, (2) the peculiar relations between it and the corneal corpuscles at a later period. This view would receive still further support if a layer of mesoblast between the lens and the epiblast were really present as believed by Lieberkiihn. It must however be admitted that the objections to Kessler's view of its epiblastic nature are rather a priori than founded on definite observation.

The observations of Kessler, which have been mainly followed in the above account, are strongly opposed by Lieberkiihn (No. 374) and Arnold (No. 370), and are not entirely accepted by Kolliker. It is especially on the development of these parts in Mammalia (to be spoken of in the sequel) that the above authors found their objections. I have had through Kessler's kindness an opportunity of looking through some of his beautiful preparations, and have no hesitation in generally accepting his conclusions, though as mentioned above I cannot agree with all his interpretations.

The aqueous humour. The cavity for the aqueous humour has its origin in the ring-shaped space round the front of the lens, which, as already mentioned, is bounded by the external skin, the edge of the optic cup, and the lens. By the formation of the cornea this space is shut off from the external skin, and on the appearance of the epithelioid layer of Descemet's membrane a continuous cavity is developed between the cornea and the lens. This cavity enlarges and receives its final form on the full development of the iris.

Comparative view of the development of the Vertebrate Eye.

The organ of vision, when not secondarily aborted, contains in all Vertebrata the essential parts above described. The most interesting cases of partial degeneration are those of Myxine and the Ammoccete. The development of such aborted eyes has as yet been studied only in the

B. III. 3 2


498


THE AMMOCCETE EYE.


Ammocoete 1 , in which it resembles in most important features that of other Vertebrata.

Eye of Ammoccetes. The optic vesicle arises as an outgrowth of the fore-brain, but the secondary optic cup is remarkable in the young larva for its small size (fig. 291, opv). The thicker outer wall gives rise to the retina, and the thinner inner wall to the choroid pigment. The lens is formed as an invagination of the single-layered epidermis (fig. 291, /). As development proceeds the parts of the eye gradually enlarge, and the mesoblast around the hinder and dorsal part of the optic cup becomes pigmented. There is at first no cavity for the vitreous humour, but eventually the growth of the optic cup gives rise to a space, into which a cellular process of mesoblast grows at a slight notch in the ventral edge of the optic cup (W. Muller, No. 377). This notch is the only rudiment of the choroid fissure of other types. The mesoblastic process is probably the homologue of the processus falciformis and pecten, and appears to give rise to the vitreous humour ; for a long time it retains its connection with the surrounding mesoblast. Its cells eventually disappear, and it never contains any vascular structures.

The lens for a long time remains as an oval vesicle with a central cavity. In a later stage, when the Ammoccete is fully developed, the secondary optic cup forms a deep pit (fig. 292, r) ; in the mouth of which is placed the lens (/). The two walls of the retina have now the normal vertebrate structure, though the pigment is as yet imperfectly present in the choroid layer. The lens has the embryonic forms of higher types (cf. fig. 289), consisting of an inner thicker segment, the true lens, and an outer layer forming the epithelium of the lens capsule. The edge of the optic cup, which forms the rudiment of the epiblast of the iris, is imperfectly separated from the remainder of the optic cup ; and a mesoblastic element of the iris, distinct from Descemet's membrane (dm\ can hardly be spoken of.

There is no cavity for the aqueous humour in front of the lens ; and there is no cornea as distinct from the epidermis and subepidermic tissues. The elements in front of the lens are (i) the epidermis (ep} ; (2) the dermis (dc) ; (3) the subdermal connective tissue (sdc) which passes without any sharp line of demarcation into the dermis ; (4) a thick membrane, continuous with the mesoblastic part of the choroid, which appears to represent Descemet's membrane. The subdermal connective tissue is continued as an



FIG. 291. HORIZONTAL

SECTION THROUGH THE HEAD OF A JUST HATCHED LARVA OF PETROMYZON SHEWING THE DEVELOPMENT OF THE LENS OF THE

EYE.

th.c. thalamencephalon ; op.v. optic vesicle ; /. lens of eye ; h.c. head cavity.


The most detailed account is that of W. Muller (No. 377).


ORGANS OF VISION OF THE VERTEBRATA.


499


investment round the whole eye ; and there is no differentiated sclerotic and only an imperfect choroid.

In a still later stage a distinct mesoblastic element for the iris is formed. When the Ammoccete is becoming a Lamprey, the eye approaches the surface ; an anterior chamber is established ; and the eye differs from that of the higher types mainly in the fact that the cornea is hardly distinguished from the remainder of the skin, and that a sclerotic is very imperfectly represented.

Optic vesicles. The development of the primitive optic vesicles, so far as is known, is very constant throughout the Vertebrata. In Teleostei and Lepidosteus alone is there an important deviation from the ordinary type, dependent however upon the mode of formation of the medullary keel, the optic vesicles arising while the medullary keel is still solid, and being at first also solid. They subsequently acquire a lumen and undergo the ordinary changes.

The lens. In the majority of groups, viz. Elasmobranchii, Reptilia, Aves, and Mammalia, the lens is formed by an open invagination of the epiblast, but in Amphibia, Teleostei and Lepidosteus, where the nervous


S.d.c



FIG. 292. EYE OF AN AMMOCCETES LYING BENEATH THE SKIN.

ep. epidermis; d.c. dermal connective tissue continuous with the sub-dermal connective tissue (s.d.c}, which is also shaded. There is no definite boundary to this tissue where it surrounds the eye.

m. muscles; dm. membrane of Descemet ; /.lens; v.h. vitreous humour ; r. retina; rp. retinal pigment.

layer of the skin is early established, this layer alone takes part in the formation of the lens (fig. 293, /). The lens is however formed even in these types as a hollow body by an invagination ; but its opening remains permanently shut off from communication with the exterior by the epidermic

322


500 THE CORNEA.


layer of the epiblast. Gotte describes the lens as formed by a solid thickening of the nervous layer in Bombinator. This is probably a mistake.

The cornea. The mode of formation of the cornea already described appears to be characteristic of most Vertebrata except the Ammocoete. It has been found by Kessler in Aves, Reptilia and Amphibia, and probably also occurs in Pisces. In Mammals it is not however so easy to establish. There are at first no mesoblast cells between the lens and the epiblast (fig. 295) but in many Mammals (vide Kessler, No. 372, pp. 91 94) a layer of rounded mesoblast cells, which forms Descemet's membrane, grows in between the two, at a time when it is not easy to recognise a corneal lamina, as distinct from a simple coagulum.

After the formation of this layer the mesoblast cells grow into the corneal lamina from the sides, and becoming flattened arrange themselves in rows between the laminae of the cornea. The cornea continues to increase in thickness by the addition of laminae on the side adjoining the epiblast.

We have already seen that in the Lamprey the cornea is nothing else but the slightly modified and more transparent epidermis and dermis.

The optic nerve and the choroid fissure. It will be convenient to consider together the above structures, and with them the vascular and other processes which pass into the cavity of the optic cup through the choroid fissure. These parts present on the whole a greater amount of variation than any other parts of the eye.

I commence with the Fowl which is both a very convenient general type for comparison, and also that in which these structures have been most fully worked out.

During the third day of incubation there passes in through the choroid slit a vascular loop, which no doubt supplies the transuded material for the growth of the vitreous humour. Up to the fifth day this vascular loop is the only structure passing through the choroid slit. On this day however a new structure appears, which remains permanently through life, and is known as the pec ten. It consists of a lamellar process of the mesoblast cells round the eye, passing through the choroid slit near the optic nerve, and enveloping part of the afferent branch of the vascular loop above mentioned. The proximal part of the free edge of the pecten is somewhat swollen, and sections through this part have a club-shaped form. On the sixth day the choroid slit becomes rapidly closed, so that at the end of the sixth day it is reduced to a mere seam. There are however two parts of this seam where the edges of the optic cup have not coalesced. The proximal of these adjoins the optic nerve, and permits the passage of the pecten and at a later period of the optic nerve ; and the second or distal one is placed near the ciliary edge of the slit, and is traversed by the efferent branch of the above-mentioned vascular loop. This vessel soon atrophies, and with it the distal opening in the choroid slit completely vanishes. In some varieties of domestic Fowl (Lieberkiihn) the opening however persists. The seam which marks the original site of the choroid slit is at first


ORGANS OF VISION OF THE VERTEBRATA. 501

conspicuous by the absence of pigment, and at a later period by the deep colour of its pigment. Finally, a little after the ninth day, no trace of it is to be seen.

Up to the eighth day the pecten remains as a simple lamina ; by the tenth or twelfth day it begins to be folded or rather puckered, and by the seventeenth or eighteenth day it is richly pigmented and the puckerings



FIG. 293. SECTION THROUGH THE FRONT PART OF THE HEAD OF A LEPIDOS TEUS EMBRYO ON THE SEVENTH DAY AFTER IMPREGNATION. al. alimentary tract ; fb. thalamencephalon ; /. lens of eye ; op.v. optic vesicle. The mesoblast is not represented.

have become nearly as numerous as in the adult, there being in all seventeen or eighteen. The pecten is almost entirely composed of vascular coils, which are supported by a sparse pigmented connective tissue ; and in the adult the pecten is still extremely vascular. The original artery which became enveloped at the formation of the pecten continues, when the latter becomes vascular, to supply it with blood. The vein is practically a fresh development after the atrophy of the distal portion of the primitive vascular loop of the vitreous humour.

There are no true retinal blood-vessels.

In the formation of the optic cup the extreme peripheral part of the optic nerve, which is in immediate proximity with the artery of the pecten, becomes folded. The permanent opening in the choroid fissure for the pecten is intimately related to the entrance of the optic nerve into the eyeball ; the fibres of the optic nerve passing in at the inner border of the pecten, coursing along its sides to its outer border, and radiating from it as from a centre to all parts of the retina.

In the Lizard the choroid slit closes considerably earlier than in the Fowl. The vascular loop in the vitreous humour is however more developed. The pecten long remains without vessels, and does not in fact become at all


502 THE CHOROID FISSURE.

vascular till after the very late disappearance of the distal part of the vascular loop of the vitreous humour.

The arrangement of the ingrowth through the choroid slit in Elasmobranchii (Scyllium) has been partially worked out, and so far as is at present known the agreement between the Avian and Elasmobranch type is fairly close.

At the time when the cavity between the lens and the secondary optic cup is just commencing to be formed, a process of mesoblast accompanied by a vascular loop passes into the vitreous humour, through the choroid slit, close to the optic nerve. The vessel in this process is no doubt equivalent to the vascular loop in the Avian eye, but I have not made out that it projects beyond the mesoblastic process accompanying it. As the cavity of the vitreous humour enlarges and the choroid slit elongates, the process through it takes the form of a lamina with a somewhat swollen border, and projects for some distance into the cavity of the vitreous humour.

At a later stage, after the outer layer of the optic cup has become pigmented, the distal part of the choroid slit adjoining the border of the lens closes up ; but along the line where it was present the walls of the optic cup remain very thin and are thrown into three folds, two lateral and one median, projecting into the cavity of the vitreous humour. The median fold is in contact with the lens, and the vascular mesoblast surrounding the eye projects into the space between the two laminae of which it is formed. In passing from the region of the lens to that of the optic nerve the lateral folds of the optic cup disappear, and the median fold forms a considerable projection into the cavity of the vitreous humour. It consists of a core of mesoblast covered by a delicate layer derived from both strata of the optic cup. Still nearer the optic nerve the choroid slit is no longer closed, and the mesoblast, which in the neighbourhood of the lens only extended into the folds of the wall of the optic cup, now projects freely into the cavity of the vitreous humour, and forms the lamina already described. It is not very vascular, but close to the optic nerve there passes into it a considerable artery.

In the young animal the choroid slit is no longer perforated by a mesoblastic lamina. At its inner end it remains open to allow of the passage of the optic nerve. The line of the slit can easily be traced along the lower side of the retina ; and close to the lens the retinal wall continues, as in the embryo, to be raised into a projecting fold. Traces of these structures are visible even in the fully grown examples of Scyllium.

As has been pointed out by Bergmeister the mesoblastic lamina projecting into the vitreous humour resembles the pecten at an early stage of development, and is without doubt homologous with it. The artery which supplies it is certainly equivalent to the artery of the pecten.

There can be no doubt that the mesoblastic lamina projecting into the vitreous humour is equivalent to the processus falciformis of Teleostei, and it seems probable that the whole of it, including the free part as well as that covered by epiblast, ought to be spoken of under this title. The optic nerve


ORGANS OF VISION OF THE VERTEJ5RATA.


503



in Elasmobranchii is not included in the folding to which the secondary optic vesicle owes its origin, and would seem to perforate the walls of the optic cup only at the distal end of the processus falciformis.

In Teleostei there is at first a vascular loop like that in Birds, passing through the choroid fissure. This has been noticed by Kessler in the Pike, and by Schenk in the Trout. At a later period a mesoblastic ingrowth with a blood-vessel makes its way in many forms into the cavity of the vitreous humour, accompanied by two folds in the walls of the free edges of the choroid fissure (fig. 294). These structures, which constitute the processus falciformis, clearly resemble very closely the mesoblastic process and folds of the optic cup in Elasmobranchii. The processus falciformis comes in contact with, and perhaps becomes attached to the wall of the lens ; and persists through life.

In Triton there is no vascular ingrowth through the choroid fissure, but a few mesoblastic cells pass in which represent the vascular ingrowth of other types. The optic nerve perforates the proximal extremity of the original choroid slit.

The absence of an embryonic blood-vessel does not however hold good for all Amphibia, as there is present in the embryo Alytes (Lieberkiihn) an artery, which breaks up into a capillary system on the retinal border of the vitreous humour.

In the Ammoccete the choroid slit is merely represented by a slight notch on the ventral edge of the optic cup, and the mesoblastic process which passes through the choroid slit in most types is represented by a large cellular process, from which the vitreous humour would appear to be derived.

Mammalia differ from all the types already described in the immense fcetal development of the blood-vessels of the vitreous humour. There are however some points in connection with the development of these vessels which are still uncertain. The most important of these points concerns the presence of a prolongation of the mesoblast around the eye into the cavity of the vitreous humour. It is maintained by Lieberkiihn, Arnold, Kolliker, etc., that in the invagination of the lens a thin layer of mesoblast is carried before it ; and is thus transported into the cavity of the vitreous humour. This is denied by Kessler, but the layer is so clearly figured by the above embryologists, that the existence of it in some Mammalia (the Rabbit, etc.) must I think be accepted.

In the folding in of the optic vesicle, which accompanies the formation of the lens, the optic nerve becomes included, and on the development of the cavity of the vitreous humour an artery, running in the fold of the optic


FIG. 294. HORIZONTAL SECTION THROUGH THE EYE OF A TELEOSTEAN EMBRYO. (From Gegenbaur ; after Schenk.)

s. choroid fissure, with two folds forming part of the processus falciformis ; a. choroid layer of optic cup ; b. retinal layer of optic cup ; c. cavity of vitreous humour ; d. lens.


504


THE CIIOROID FISSURE.


nerve, passes through the choroid slit into the cavity of the vitreous humour (fig. 295, acr). The sides of the optic nerve subsequently bend over, and completely envelope this artery, which at a later period gives off branches to the retina, and becomes known as the arteria centralis retinas. It is homologous with the arterial limb of the vascular loop projecting into the vitreous humour in Birds, Lizards, Teleostei, etc.

Before becoming enveloped in the optic nerve this artery is continued through the vitreous humour (fig. 295), and when it comes in close proximity


a. c.



,m, e o


FIG. 295. SECTION THROUGH THE EYE OF A RABBIT EMBRYO OF

ABOUT TWELVE DAYS.

c. epithelium of cornea ; /. lens ; mec. mesoblast growing in from the side to form the cornea: rt. retina ; a.c.r. arteria centralis retinae; of.n. optic nerve.

The figure shews (i) the absence at this stage of mesoblast between the lens and the epiblast : the interval between the two has however been made too great ; (2) the arteria centralis retinae forming the vascular capsule of the lens and continuous with vascular structures round the edges of the optic cup.

to the lens it divides into a number of radiating branches, which pass round the edge of the lens, and form a vascular sheath which is prolonged so as to cover the anterior wall of the lens. In front of the lens they anastomose with vessels, coming from the iris, many of which are venous (fig. 295) and the whole of the blood from the arteria centralis is carried away by these veins. The vascular sheath surrounding the lens receives the name of the membrana capsulo-pupillaris. The posterior part of it appears (Kessler, No. 372) to be formed of vessels without the addition of any other structures and is either formed simply by branches of the arteria centralis, or out of


ORGANS OF VISION OF THE VERTEBRATA. 505

the mesoblast cells involuted with the lens. The anterior part of the vascular sheath is however inclosed in a very delicate membrane, the membrana pupillaris, continuous at the sides with the epithelium of Descemet's membrane. On the formation of the iris this membrane lies superficially to it, and forms a kind of continuation of the mesoblast of the iris over the front of the lens.

The origin of this membrane is much disputed. By Kessler, whose statements have been in the main followed, it is believed to appear comparatively late as an ingrowth of the stroma of the iris ; while Kolliker believes it to be derived from a mesoblastic ingrowth between the front wall of the lens and the epiblast. According to Kolliker this ingrowth subsequently becomes split into two laminae, one of which forms the cornea, and the other the anterior part of the vascular sheath of the lens with its membrana pupillaris. Between the two appears the aqueous humour.

The membrana capsulo-pupillaris is simply a provisional embryonic structure, subserving the nutrition of the lens. The time of its disappearance varies somewhat for the different Mammalia in which this point has been investigated. In the human embryo it lasts from the second to the seventh month and sometimes longer. As a rule it is completely absorbed at the time of birth. The absorption of the anterior part commences in the centre and proceeds outwards.

In addition to the vessels of the vascular capsule round the lens, there arise from the arteria centralis retinas, just after its exit from the optic nerve, in many forms (Dog, Cat, Calf, Sheep, Rabbit, Man) provisional vascular branches which extend themselves in the posterior part of the vitreous humour. Near the ciliary end of the vitreous humour they anastomose with the vessels of the membrana capsulo-pupillaris.

In Mammals the choroid slit closes very early, and is not perforated by any structure homologous with the pecten. The only part of the slit which remains open is that perforated by the optic nerve ; and in the centre of the latter is situated the arteria centralis retinas as explained above. From this artery there grow out the vessels to supply the retina, which have however nothing to do with the provisional vessels of the vitreous humour just described (Kessler). On the atrophy of the provisional vessels the whole of the blood of the arteria centralis passes into the retina.

It is interesting to notice (Kessler, No. 372, p. 78) that there seems to be a blood-vessel supplying the vitreous humour in the embryos of nearly all vertebrate types, which is homologous throughout the Vertebrata. This vessel often exhibits a persisting and a provisional part. The latter in Mammalia is the membrana capsulo-pupillaris and other vessels of the vitreous humour ; in Birds and Lizards it is the part of the original vascular loop, not included in the pecten, and in Osseous Fishes that part (?) not involved in the processus falciformis. The permanent part is formed by the retinal vessels of Mammalia, by the vessels of the pecten in Birds and Lizards, and by those of the processus falciformis in Fishes.


506 THE IRIS.

The Iris and Ciliary processes. The walls of the edge of the optic cup become very much thinner than those of the true retinal part. In many Vertebrates (Mammalia, Aves, Reptilia, Elasmobranchii, etc.) the thinner part, together with the mesoblast covering it, becomes divided into two regions, viz. that of the iris, and that of the ciliary processes. In the Newt and Lamprey this differentiation does not take place, but the part in question simply becomes the iris.


Accessory Organs connected wit/i t/te Eye.

Eyelids. The most important accessory structures connected with the eye are the eyelids. They are developed as simple folds of the integument with a mesoblastic prolongation between their two laminas. They may be three in number, viz. an upper and lower, and a lateral one the nictitating membrane springing from the inner or anterior border of the eye. Their inner face is lined by a prolongation of conjunctiva, which is the modified epiblast covering the cornea and part of the sclerotic.

In Teleostei and Ganoidei eyelids are either not present or at most very rudimentary. In Elasmobranchii they are better developed, and the nictitating membrane is frequently present. The latter is also usually found in Amphibia. In the Sauropsida all three eyelids are usually present, but in Mammalia the nictitating membrane is rudimentary.

In many Mammalia the two eyelids meet together during a period of embryonic life, and unite in front of the eye. A similar arrangement is permanent through life in Ophidia and some Lacertilia ; and there is a chamber formed between the coalesced eyelids and the surface of the cornea, into which the lacrymal ducts open.

Lacrymal glands. Lacrymal glands are found in the Sauropsida and Mammalia. They arise (Remak, Kdlliker) as solid ingrowths of the conjunctival epithelium. They appear in the chick on the eighth day.

Lacrymal duct. The lacrymal duct first appears in Amphibia, and is present in all the higher Vertebrates. Its mode of development in the Amphibia, Lacertilia and Aves has recently been very thoroughly worked out by Born (Nos. 380 and 381).

In Amphibia he finds that the lacrymal duct arises as a solid ridge of the mucous layer of the epidermis, continued from the external opening of the nasal cavity backwards towards the eye. It usually appears at about the time when the nasal capsule is beginning to be chondrified. As this ridge is gradually prolonged backwards towards the eye its anterior end becomes separated from the epidermis, and grows inwards in the mesoblast to become continuous with the posterior part of the nasal sack. The posterior end which joins the eye becomes divided into the two collecting branches of the adult. Finally the whole structure becomes separated from the skin except at the external opening, and develops a lumen.


ORGANS OF VISION OF THE VERTEBRATA. 507

In Lacertilia the lacrymal duct arises very much in the same manner as in Amphibia, though its subsequent growth is somewhat different. It appears as an internal ridge of the epithelium, at the junction of the superior maxillary process and the fold which gives rise to the lower eyelid. A solid process of this ridge makes its way through the mesoblast on the upper border of the maxillary process till it meets the wall of the nasal cavity, with the epithelium of which it becomes continuous. At a subsequent stage a second solid growth from the upper part of the epithelial ridge makes its way through the lower eyelid, and unites with the inner epithelium of the eyelid ; and at a still later date a third growth from the lower part of the structure forms a second junction with the epithelium of the eyelid. The two latter outgrowths form the two upper branches of the duct. The ridge now loses its connection with the external skin, and, becoming hollow, forms the lacrymal duct. It opens at two points on the inner surface of the eyelid, and terminates at its opposite extremity by opening into the nasal cavity. It is remarkable, as pointed out by Born, that the original epithelial ridge gives rise directly to a comparatively small part of the whole duct.

In the Fowl the lacrymal duct is formed as a solid ridge of the epidermis, extending along the line of the so-called lacrymal groove from the eye to the nasal pit (fig. 120). At the end of the sixth day it begins to be separated from the epidermis, remaining however united with it on the inner side of the lower eyelid. After its separation from the epidermis it forms a solid cord, the lower end of which unites with the wall of the nasal cavity. The cord so formed gives rise to the whole of the duct proper and to the lower branch of the collecting tube. The upper branch of the collecting tube is formed as an outgrowth from this cord. A lumen begins to be formed on the twelfth day of incubation, and first appears at the nasal end. It arises by the formation of a space between the cells of the cord, and not by an absorption of the central cells.

In Mammalia Kolliker states that he has been unable to observe anything similar to that described by Born in the Sauropsida and Amphibia, and holds to the old view, originally put forward by Coste, that the duct is formed by the closure of a groove leading from the eye to the nose between the outer nasal process and the superior maxillary process. The upper extremity of the duct dilates to form a sack, from which two branches pass off to open on the lacrymal papillae. In view of Born's discoveries Kolliker's statements must be received with some caution.


The Eye of tJte Tunicata.

The unpaired eye of the larva of simple Ascidians is situated somewhat to the right side of the posterior part of the dorsal wall of the anterior cephalic vesicle (fig. 296, O\ It consists of a refractive portion, turned towards the cavity of the vesicle of


508 THE EYE OF THE TUNICATA.

the brain, and a retinal portion forming part of the wall of the brain. The refractive parts consist of a convex-concave meniscus in front, and a spherical lens behind, adjoining the concave side of the meniscus. The posterior part of this lens is im


FIG. 296. LARVA OF ASCIDIA MENTULA. (From Gegenbaur ; after Kupffer. ) Only the anterior part of the tail is represented.

IV'. anterior swelling of neural tube; N. anterior swelling of spinal portion of neural tube ; n. hinder part of neural tube ; ch. notochord ; K. branchial region of alimentary tract; d. oesophageal and gastric region of alimentary tract; 0. eye; a. otolith ; o. mouth ; s. papilla for attachment.

bedded in a layer of pigment The retina is formed of columnar cells, with their inner ends imbedded in the pigment which encloses the posterior part of the lens. The retinal part of the eye arises in the first instance as a prominence of the wall of the cerebral vesicle : its cells become very columnar and pigmented at their inner extremities (fig. 8, V, a). The lens is developed at a later period, after the larva has become hatched, but the mode of its formation has not been made out.

General considerations on the Eye of the Chordata.

There can be but little doubt that the eye of the Tunicata belongs to the same phylum as that of the true Vertebrata, different as the two eyes are. The same may also be said with reference to the degenerate and very rudimentary eye of Amphioxus.

The peculiarity of the eye of all the Chordata consists in the retina being developed from part of the wall of the brain. How is this remarkable feature of the eye of the Chordata to be explained ?

Lankester, interpreting the eye in the light of the Tunicata, has made the interesting suggestion 1 "that the original Vertebrate must have been a transparent animal, and had an eye or pair of eyes inside the brain, like that of the Ascidian Tadpole."

1 Degeneration, London, 1880, p. 49.


ORGANS OF VISION. 509


This explanation may possibly be correct, but another explanation appears to me possible, and I am inclined to think that the vertebrate eyes have not been derived from eyes like those of Ascidians, but that the latter is a degenerate form of vertebrate eye.

The fact of the retina being derived from the fore-brain may perhaps be explained in the same way as has already been attempted in the case of the retina of the Crustacea ; i.e. by supposing that the eye was evolved simultaneously with the fore part of the brain.

The peculiar processes which occur in the formation of the optic vesicle are more difficult to elucidate ; and I can only suggest that the development of a primary optic vesicle, and its conversion into an optic cup, is due to the retinal part of the eye having been involved in the infolding which gave rise to the canal of the central nervous system. The position of the rods and cones on the posterior side of the retina is satisfactorily explained by this hypothesis, because, as may be easily seen from figure 285, the posterior face of the retina is the original external surface of the epidermis, which is infolded in the formation of the brain ; so that the rods and cones are, as might be anticipated, situated on what is morphologically the external surface of the epiblast of the retina.

The difficulty of this view arises in attempting to make out how the eye can have continued to be employed during the gradual change of position which the retina must have undergone in being infolded with the brain in the manner suggested. If however the successive steps in this infolding were sufficiently small, it seems to me not impossible that the eye might have continued to be used throughout the whole period of change, and a transparency of the tissues, such as Lankester suggests, may have assisted in rendering this possible.

The difficulty of the eye continuing to be in use when undergoing striking changes in form is also involved in Lankester's view, in that if, as I suppose, he starts from the eye of the Ascidian Tadpole with its lenses turned towards the cavity of the brain ; it is necessary for him to admit that a fresh lens and other optical parts of the eye became developed on the opposite side of the eye to the original lens ; and it is difficult to understand such a change, unless we can believe that the refractive media on the two sides were in operation simultaneously. It may be noted that the same difficulty is involved in supposing, as I have done, that the eye of the Ascidian Tadpole was developed from that of a Vertebrate. I should however be inclined to suggest that the eye had in this case ceased for a period to be employed ; and that it has been re-developed again in some of the larval forms. Its characters in the Tunicata are by no means constant.

Accessory eyes in the Vertebrata.

In addition to the paired eyes of the Vertebrata certain organs are found in the skin of a few Teleostei living in very deep water, which, though clearly not organs of true vision, yet present characters which indicate that


510 ACCESSORY EYES IN THE VERTEBRATA.

they may be used in the perception of light. The most important of such organs are those found in Chauliodus, Stomias, etc., the significance of which was first pointed out by Leuckart, while the details of their structure have been recently worked out by Leydig 1 and Ussow. They are distributed not only in the skin, but are also present in the mouth and respiratory cavity, a fact which appears to indicate that their main function must be something else than the perception of light. It has been suggested that they have the function of producing phosphorescence.

Another organ, probably of the same nature, is found on the head of Scopelus.

The organs in Chauliodus are spherical or nearly spherical bodies invested in a special tunic. The larger of them, which alone can have any relation to vision, are covered with pigment except on their outer surface. The interior is filled with two masses, named by Leuckart the lens and vitreous humour. According to Leydig each of them is cellular and receives a nerve, the ultimate destination of which has not however been made out. According to Ussow the anterior mass is structureless, but serves to support a lens, placed in the centre of the eye, and formed of a series of crystalline cones prolonged into fibres, which in the posterior part of the eye diverge and terminate by uniting with the processes of multipolar cells, placed near the pigmented sheath. These cells, together with the fibres of the crystalline cones which pass to them, are held by Ussow to constitute a retina.

Eye of the Mollusca.

(362) N. Bobretzky. " Observations on the development of the Cephalopoda " (Russian). Nachrichten d. kaiserlichen Gesell.d. Freundcder Natunviss. Anthropolog. Ethnogr. bei d. Universitiit Moskau.

(363) H. Grenacher. " Zur Entwicklungsgeschichte d. Cephalopoden." Zeit. f. wiss. Zool., Bd. xxiv. 1874.

(364) V. Hensen. " Ueber d. Auge einiger Cephalopoden." Zeit. f. wiss. Zool., Vol. xv. 1865.

(365) E. R. Lankester. " Observations on the development of the Cephalopoda." Quart, y. of Micr. Science, Vol. xv. 1875.

(366) C. Semper. Ueber Sehorgane von Typus d. Wirbelthieratigen. Wiesbaden, 1877 Eye of the Arthropoda.

(367) N. Bobretzky. Development of Astacus and Palaemon. Kiew, 1873.

(368) A. Dohrn. " Untersuchungen lib. Bau u. Entwicklung d. Arthropoden. Palinurus nnd Scyllarus. " Zeit. f. wiss. Zool., Bd. xx. 1870, p. 264 et seq.

1 F. Leydig. "Ueber Nebenaugen d. Chauliodus Sloani." Archiv f. Anal, und Phys., 1879. M. Ussow. " Ueb. d. Bau d. augenahnlichen Flicken einiger Knochenfische." Bui. d. la Soc. d. Naturalistes de Moscon, Vol. i.iv. 1879. Vide for general description and further literature, Giinther, The Study of Fish>-s t Edinburgh, 1880.


ORGANS OF VISION. 51 1


(369) E. Claparede. " Morphologic d. zusammengesetzten Auges bei den Arthropoden." Zeit. f. wiss. Zool., Bd. x. 1860.

(370) H. Grenacher. Untersuchungen iib. d. Sehorgane d. Arthropoden. Gottingen, 1879.

Vertebrate Eye.

(371) J.Arnold. Beitrage zur Entwicklungsgeschichte des Auges. Heidelberg, 1874.

(372) Babuchin. "Beitrage zur Entwicklungsgeschichte des Auges." Wilrzburger natiinuissenschaftliche Zeitschrift, Bd. 8.

(373) L. Kessler. Zur Entwicklung d. Attges d. Wirbelthiere. Leipzig, 1877.

(374) N. Lieberkiihn. Ueber das Auge des Wirbelthierembryo. Cassel, 1872.

(375) N. Lieberkiihn. "Beitrage z. Anat. d. embryonalen Auges." Archiv f. Anat. imd Phys., 1879.

(376) L. Lowe. "Beitrage zur Anatomic des Auges" and "Die Histogenese der Retina." Archiv f. mikr. Anat., Vol. xv. 1878.

(377) V. Mihalkowics. " Untersuchungen iiber den Kamm des Vogelauges." Archiv f. mikr. Anat., Vol. ix. 1873.

(378) W. Miiller. " Ueber die Stammesentwickelung des Sehorgans der Wirbelthiere." Festgabe Carl Ltidwig. Leipzig, 1874.

(379) S. L. Schenk. "Zur Entwickelungsgeschichte des Auges der Fische." Wiener Sitzungsberichte, Bd. LV. 1867.

Accessory organs of the Vertebrate Eye.

(380) G. Born. "Die Nasenhohlen u. d. Thranennasengang d. Amphibien. Morphologisches Jahrbuch, Bd. II. 1876.

(381) G. Born. " Die Nasenhohlen u. d. Thranennasengang d. amnioten Wirbelthiere. I. Lacertilia. II. Aves." Morphologisches Jahrbuch, Bd. v. 1879.

Eye of the Tunicata.

(382) A. Kowalevsky. "Weitere Studien lib. d. Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. vil. 1871.

(383) C. Kupffer. "Zur Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. vii. 1872.


CHAPTER XVII.


AUDITORY ORGAN, OLFACTORY ORGAN AND SENSE ORGANS OF THE LATERAL LINE.


Auditory Organs.

A GREAT variety of organs, very widely distributed amongst aquatic forms, and also found, though less universally, in land forms, are usually classed together as auditory organs.

In the case of all aquatic forms, or of forms which have directly inherited their auditory organs from aquatic forms, these organs are built upon a common type ; although in the majority of instances the auditory organs of the several groups have no genetic relations. All the organs have their origin in specialized portions of the epidermis. Some of the cells of a special region become provided at their free extremities with peculiar hairs, known as auditory hairs; while in other cells concretions, known as otoliths, are formed, which appear often to be sufficiently free to be acted upon by vibrations of the surrounding medium, and to be so placed as to be able in their turn to transmit their vibrations to the cells with auditory hairs 1 . The auditory regions of the epidermis are usually shut off from the surface in special sacks.

The actual function of these organs is no doubt correctly described, in the majority of instances, as being auditory; but it appears to me very possible that in some cases their function may be to enable the animals provided with them to detect the presence of other animals in their neighbourhood, through the

1 The function of the otoliths is not always clear. There is evidence to shew that they sometimes act as dampers.


AUDITORY ORGANS. 513


unclulatory movements in the water, caused by the swimming of the latter.

Auditory organs with the above characters, sometimes freely open to the external medium, but more often closed, are found in various Ccelenterata, Vermes and Crustacea, and universally or all but universally in the Mollusca and Vertebrata.

In many terrestrial Insects a different type of auditory organ has been met with, consisting of a portion of the integument modified to form a tympanum or drum, and supported at its edge by a chitinous ring. The vibrations set up in the membranous tympanum stimulate terminal nerve organs at the ends of chitinous processes, placed in a cavity bounded externally by the tympanic membrane.

The tympanum of Amphibia and Amniota is an accessory organ added, in terrestrial Vertebrata, to an organ of hearing primitively adapted to an aquatic mode of life ; and it is interesting to notice the presence of a more or less similar membrane in the two great groups of terrestrial forms, i.e. terrestrial Vertebrata and Insecta.

Nothing is known with reference to the mode of development or evolution of the tympanic type of auditory organ found in Insects, and, except in the case of Vertebrates, but little is known with reference to the development of what may be called the vesicular type of auditory organ found in aquatic forms. Some very interesting facts with reference to the evolution of such organs have however been brought to light by the brothers Hertwig in their investigations on the Ccelenterata; and I propose to commence my account of the development of the auditory organs in the animal kingdom by a short statement of the results of their researches.

Ccelenterata. Three distinct types of auditory organ have been recognised in the Medusae ; two of them resulting from the differentiation of a tentacle-like organ, and one from ectoderm cells on the under surface of the velum. We may commence with the latter as the simplest. It is found in the Medusae known as the Vesiculata. The least differentiated form of this organ, so far discovered, is present in Mitrotrocha, Tiaropsis and other genera. It has the form of an open pit ; and a series of such organs are situated along the attached edge

B. in, 33


514 AUDITORY ORGANS OF THE CCELENTERATA.

of the velum with their apertures directed downwards. The majority of the cells lining the outer, i.e. peripheral side of the



FIG. 297. AUDITORY VESICLE OF PHIALIDIUM AFTER TREATMENT WITH DILUTE OSMIC ACID. (From Lankester; after O. and R. Hertwig.)

d l . epithelium of the upper surface of the velum; d 2 . epithelium of the under surface of the velum ; r. circular canal at the edge of the velum ; nr l . upper nervering ; h. auditory cells ; hh. auditory hairs ; np. nervous cushion formed of a prolongation of the lower nerve-ring. Close to the nerve-ring is seen a cell, shewn as black, containing an otolith.

pit, contain an otolith, while a row of the cells on the inner, i.e. central side, are modified as auditory cells. The auditory cells are somewhat strap-shaped, their inner ends being continuous with the fibres of the lower nerve-ring, and their free ends being provided with bent auditory hairs, which lie in contact with the convex surfaces of the cells containing the otoliths.

By the conversion of such open pits into closed sacks a more complicated type of auditory organ, which is present in many of the Vesiculata, viz. ^Equorea, Octorchis, Phialidium, &c., is produced. A closed vesicle of this type is shewn in fig. 297. Such organs form projections on the upper surface of the velum. They are covered by a layer of the epithelium (d 1 } of the upper surface of the velum, but the lining of the vesicle (d*} is derived from what was originally part of the epithelium of the lower surface of the velum, homologous with that lining the open pits in the type already described. The general arrangement of the cells lining such vesicles is the same as that of the cells lining the open pits.

A second type of auditory organ, found in the Trachymeclusa,", appears in its simplest condition as a modified tentacle.


AUDITORY ORGANS. 515


It is formed of a basal portion, covered by auditory cells with long stiff auditory hairs, supporting at its apex a club-shaped body, attached to it by a delicate stalk. An endodermal axis is continued through the whole structure, and in one or more of the endoderm cells of the club-shaped body otoliths are always present. The tails of the auditory cells are directly continued into the upper nerve-ring.

In more complicated forms of this organ the tentacle becomes enclosed in a kind of cup, by a wall-like upgrowth of the



FIG. 298. AUDITORY ORGAN OF RHOPALONEMA. (From Lankester; after O. and R. Hertwig.)

The organ consists of a modified tentacle (hk) with auditory cells and concretions, partially enclosed in a cup.

surrounding parts (fig. 298) ; and in some forms, e.g. Geryonia, by the closure of the cup, the whole structure takes the form of a completely closed vesicle, in the cavity of which the original tentacle forms an otolith-bearing projection.

The auditory organs found in the Acraspedote Medusae approach in many respects to the type of organ found in the Trachymedusse. They consist of tentacular organs placed in grooves on the under surface of the disc. They have a swollen extremity, and are provided with an endodermal axis for half the length of which there is a diverticulum of the gastrovascular canal system. The terminal portion of the endoderm is solid, and contains calcareous concretions. The ectodermal cells at the base of these organs have the form of auditory cells.

Mollusca. Auditory vesicles are found in almost all Mollusca on the ventral side of the body in close juxtaposition to the pedal ganglia. Except possibly in some Cephalopods, these

332


516 AUDITORY ORGANS OF THE VERTEBRATA.

vesicles are closed. They are provided with free otoliths, supported by the cilia of the walls of the sack, but in addition some of the cells of the sack are provided with stiff auditory hairs.

In many forms these sacks have been observed to originate by an invagination of the epiblast of the foot (Pahtdina, Nassa, Heteropoda, Limax, Clio, Cephalopoda and Lamellibranchiata). In other instances (some Pteropods, Lymnaeus, &c.) they appear, by a secondary modification in the development, to originate by a differentiation of a solid mass of epiblast.

According to Fol the otocysts in Gasteropods are formed by cells of the wall of the auditory sacks ; and the same appears to hold good for Cephalopoda (Grenacher) 1 shewing that free otoliths have in these instances originated from otoliths originally placed in cells.

Crustacea. In the decapodous Crustacea organs, which have been experimentally proved to be true organs of hearing, are usually present on the basal joint of the anterior antennae. They may have (Hensen, No. 384) the form either of closed or of open sacks, lined by an invagination of the epidermis. They are provided with chitinous auditory hairs and free otoliths. In the case of the open sacks the otoliths appear to be simply stones transported into the interior of the sacks, but in the closed sacks the otoliths, though free, are no doubt developed within the sacks.

The Schizopods, which, as mentioned in the last chapter, are remarkable as containing a genus (Euphausia) with abnormally situated eyes, distinguish themselves again with reference to their auditory organs, in that another genus (Mysis) is characterized by the presence of a pair of auditory sacks in the inner plates of the tail. These sacks have curved auditory hairs supporting an otolith at their extremity.

The development of the auditory organs in the Crustacea has not been investigated.

The Vertebrata. The Cephalochorda are without organs of hearing, and the auditory organ of the Urochorda is constructed on a special type of its own. The primitive auditory organs of the true Vertebrata have the same fundamental characters as those of the majority of aquatic invertebrate forms. They consist of a vesicle, formed by the invagination of a patch of epiblast, and usually shut off from the exterior, but occasionally (Elasmo 1 For the somewhat complicated details as to the development of the auditory sacks of Cephalopods I must refer the reader to Vol. II., pp. 278, 279, and to Grenacher (Vol. i., No. 280).


AUDITORY ORGANS.


517


branchii) remaining open. The walls of this vesicle are always much complicated and otoliths of various forms are present in its cavity. To this vesicle accessory structures, derived from the walls of the hyomandibular cleft, are added in the majority of terrestrial Vertebrata.

The development of the true auditory vesicle will be considered separately from that of the accessory structures derived from the hyomandibular cleft.

In all Vertebrata the development of the auditory vesicle commences with the formation of a thickened patch of epiblast, at the side of the hind-brain, on the level of the second visceral cleft.

t.v.v

This patch soon becomes invaginated in the form of a pit (fig. 299, aup), to the inner side of which the ganglion of the auditory nerve (ami), which as shewn in a previous chapter is primitively a branch of the seventh nerve, closely applies itself.

In those Vertebrata (viz. Teleostei, Lepidosteus and Amphibia) in which the epiblast is early divided into a nervous and epidermic stratum, the auditory pit arises as an invagination of the nervous stratum only, and the mouth of the auditory pit is always closed -(fig. 300) by the epidermic stratum of the skin. Since the opening of the pit is retained through life in Elasmobranchii the closed form of pit in the above forms is clearly secondary.

In Teleostei the auditory pit arises as a solid invagination of the epiblast.



T/t,


FIG. 299. SECTION THROUGH THE HEAD OF AN ELASMOBRANCH EMBRYO, AT THE LEVEL OF THE AUDITORY INVOLUTION.

aup. auditory pit; aun. ganglion of auditory nerve ; iv.v. roof of fourth ventricle; a.c.v. anterior cardinal vein; aa. aorta; I.aa. aortic trunk of mandibular arch ; pp. head cavity of mandibular arch ; Ivc. alimentary pouch which will form the first visceral cleft; 77?. rudiment of thyroid body.


The mouth of the auditory vesicle gradually narrows, and in most

forms soon becomes closed, though in Elasmobranchii it remains permanently open. In any case the vesicle is gradually removed from the surface, remaining connected with it by an elongated duct, either opening on the dorsal aspect of the head (Elasmobranchii), or ending blindly close beneath the skin.

In all Vertebrata the auditory vesicle undergoes further


5 i8


AUDITORY ORGANS OF THE VERTEBRATA.


changes of a complicated kind. In the Cyclostomata these changes are less complicated than in other forms, though whether this is due to degeneration, or to the retention of a primitive



FIG. 300. SECTION THROUGH THE HEAD OK A LEPIUOSTEUS EMBRYO ON

THE SIXTH DAY AFTER IMPREGNATION. au.v. auditory vesicle ; au.n. auditory nerve ; ch. notochord ; hy. hypoblast.

state of the auditory organ, is not known. In the Lamprey the auditory vesicle is formed in the usual way by an invagination


cv



cc


AOA

FIG. 301. SECTION THROUGH THE HIND-BRAIN OK A CHICK AT THE END OF THE THIRD DAY OF INCUBATION.

IV. fourth ventricle. The section shews the very thin roof and thicker sides of the ventricle. Ch. notochord ; C V. anterior cardinal vein; CC. involuted auditory vesicle (CC points to the end which will form the cochlear canal) ; RL. recessus labyrinthi (remains of passage connecting the vesicle with the exterior) ; hy. hypoblast lining the alimentary canal; AO., AO.A. aorta, and aortic arch.


AUDITORY ORGANS. 519


of the epiblast, which soon becomes vesicular, and for a considerable period retains a simple character. As pointed out by Max Schultze, a number of otoliths appears in the vesicle during larval life, and, although such otoliths are stated by J. Miiller to be absent both in the full-grown Ammoccete and in the adult, they have since been found by Ketel (No. 387). The formation of the two semicircular canals has not been investigated.

In all the higher Vertebrates the changes of the auditory sacks are more complicated. The ventral end of the sack is produced into a short process (fig. 301, CC}\ while at the dorsal end there is the canal-like prolongation of the lumen of the sack (RL}, derived from the duct which primitively opened to the exterior, and which in most cases persists as a blind diverticulum of the auditory sack, known as the recessus labyrinthi or aqueductus vestibuli. The parts thus indicated give rise to the whole of the membranous labyrinth of the ear. The main body of the vesicle becomes the utriculus and semicircular canals, while the ventral process forms the sacculus hemisphericus and cochlear canal.

The growth of these parts has been most fully studied in Mammalia, where they reach their greatest complexity, and it will be convenient to describe their development in this group, pointing out how they present, during some of the stages in their growth, a form permanently retained in lower types.

The auditory vesicle in Mammalia is at first nearly spherical, and is imbedded in the mesoblast at the side of the hind-brain. It soon becomes triangular in section, with the apex of the triangle pointing inwards and downwards. This apex gradually elongates to form the rudiment of the cochlear canal and sacculus hemisphericus (fig. 302, CC). At the same time the recessus labyrinthi (R.L) becomes distinctly marked, and the outer wall of the main body of the vesicle grows out into two protuberances, which form the rudiments of the vertical semicircular canals ( V.B}. In the lower forms (fig. 305) the cochlear process of the vestibule hardly reaches a higher stage of development than that found at this stage in Mammalia.

The parts of the auditory labyrinth thus established soon increase in distinctness (fig. 303) ; the cochlear canal (CC} becomes longer and curved ; its inner and concave surface being


520


AUDITORY ORGANS OF THE MAMMALIA.


lined by a thick layer of columnar epiblast. The recessus labyrinthi also increases in length, and just below the point where the bulgings to form the vertical semicircular canals are situated, there is formed a fresh protuberance for the horizontal semi


V.B



FIG. 302. TRANSVERSE SECTION OF THE HEAD OF A FCETAL SHEEP (16 MM. IN LENGTH) IN THE REGION OF THE HIND-BRAIN. (After Bottcher.)

HB. the hind -brain.

The section is somewhat oblique, hence while on the right side the connections of the recessus vestibuli R.L., and of the commencing vertical semicircular canal V.B., and of the ductus cochlearis CC., with the cavity of the primary otic vesicle are seen : on the left side, only the extreme end of the ductus cochlearis CC, and of the semicircular canal V.B. are shewn.

Lying close to the inner side of the otic vesicle is seen the cochlear ganglion GC ; on the left side the auditory nerve G and its connection N with the hind-brain are also shewn.

Below the otic vesicle on either side lies the jugular vein.

circular canal. At the same time the central parts of the walls of the flat bulgings of the vertical canals grow together, obliterating this part of the lumen, but leaving a canal round the periphery ; and, on the absorption of their central parts, each of the original simple bulgings of the wall of the vesicle becomes converted into a true semicircular canal, opening at its two extremities into the auditory vesicle. The vertical canals are first established and then the horizontal canal.


AUDITORY ORGANS.


521


Shortly after the formation of the rudiment of the horizontal semicircular canal a slight protuberance becomes apparent on the



FIG. 303. SECTION OF THE HEAD OF A FCETAL SHEEP 20 MM. IN LENGTH.

(After Bottcher.)

R. V. recessus labyrinthi ; V.B. vertical semicircular canal ; H.B. horizontal semicircular canal; C.C. cochlear canal ; G. cochlear ganglion.

inner commencement of the cochlear canal. A constriction arises on each side of the protuberance, converting it into a prominent hemispherical projection, the sacculus hemisphericus (fig. 304, S.R\

The constrictions are so deep that the sacculus is only connected with the cochlear canal on the one hand, and with the general cavity of the auditory vesicle on the other, by, in each case, a narrow though short canal.

The former of these canals (fig. 304, b) is known as the canalis reuniens. At this stage we may call the remaining cavity of the original otic vesicle, into which all the above parts open, the utriculus.

Soon after the formation of the sacculus hemisphericus, the


522 AUDITORY ORGANS OF THE MAMMALIA.

cochlear canal and the semicircular canals become invested with cartilage. The recessus labyrinthi remains however still enclosed in undifferentiated mesoblast

Between the cartilage and the parts which it surrounds there remains a certain amount of indifferent connective tissue, which is more abundant around the cochlear canal than around the semicircular canals.

As soon as they have acquired a distinct connective-tissue coat, the semicircular canals begin to be dilated at one of their terminations to form the ampullae. At about the same time a constriction appears opposite the mouth of the recessus labyrinthi, which causes its opening to be divided into two branches one towards the utriculus and the other towards the sacculus hemisphericus ; and the relations of the parts become so altered that communication between the sacculus and utriculus can only take place through the mouth of the recessus labyrinthi (fig. 305).

When the cochlear canal has come to consist of two and a half coils, the thickened epithelium which lines the lower surface of the canal forms a double ridge from which the organ of Corti is subsequently developed. Above the ridge there appears a delicate cuticular membrane, the membrane of Corti or membrana tectoria.

The epithelial walls of the utricle, the recessus labyrinthi, the semicircular canals, and the cochlear canal constitute together the highly complicated product of the original auditory vesicle. The whole structure forms a closed cavity, the various parts of which are in free communication. In the adult the fluid present in this cavity is known as the endolymph.

In the mesoblast lying between these parts and the cartilage, which at this period envelopes them, lymphatic spaces become established, which are partially developed in the Sauropsida, but become in Mammals very important structures.

They consist in Mammals partly of a space surrounding the utricle and semicircular canals, and partly of two very definite channels, which largely embrace between them the cochlear canal. The latter channels form the scala vestibuli on the upper side of the cochlear canal and the scala tympani on the lower. The scala vestibuli is in free communication with the lymphatic cavity surrounding the vestibule, and opens at the apex of the cochlea


AUDITORY ORGANS.


523


into the scala tympani. The latter ends blindly at the fenestra rotunda.

The fluid contained in the two scalae, and in the remaining lymphatic cavities of the auditory labyrinth, is known as perilymph.

The cavities just spoken of are formed by an absorption of


Ch.


JUB


C.C


FIG. 304. SECTION THROUGH THE INTERNAL EAR OF AN EMBRYONIC SHEEP 28 MM. IN LENGTH. (After Bottcher.)

D.M. dura mater; R. V. recessus labyrinthi ; H.V.B. posterior vertical semicircular canal ; U. utriculus ; H.B. horizontal semicircular canal; b. canalis reuniens ; a. constriction by means of which the sacculus hemisphericus S.R. is formed ; f. narrowed opening between sacculus hemisphericus and utriculus ; C. C. cochlea ; C.C. lumen of cochlea; K.K. cartilaginous capsule of cochlea; K.B. basilar plate; Ch. notochord.


524 ORGAN OF CORTI.


parts of the embryonic mucous tissue between the perichondrium and the walls of the membranous labyrinth.

The scala vestibuli is formed before the scala tympani, and both scalae begin to be developed at the basal end of the cochlea : the cavity of each is continually being carried forwards towards the apex of the cochlear canal by a progressive absorption of the mesoblast. At first both scalae are somewhat narrow, but they soon increase in size and distinctness.

The cochlear canal, which is often known as the scala media of the cochlea, becomes compressed on the formation of the scalae so as to be triangular in section, with the base of the triangle outwards. This base is only separated from the surrounding cartilage by a narrow strip of firm mesoblast, which becomes the stria vascularis, etc. At the angle opposite the base the canal is joined to the cartilage by a narrow isthmus of firm material, which contains nerves and vessels. This isthmus subsequently forms the lamina spiralis, separating the scala vestibuli from the scala tympani.

The scala vestibuli lies on the upper border of the cochlear canal, and is separated from it by a very thin layer of mesoblast, bordered on the cochlear aspect by flat epiblast cells. This membrane is called the membrane ofReissner. The scala tympani is separated from the cochlear canal by a thicker sheet of mesoblast, called the basilar membrane, which supports the organ of Corti and the epithelium adjoining it. The upper extremity of the cochlear canal ends in a blind extremity called the cupola, to which the two scalae do not for some time extend. This condition is permanent in Birds, where the cupola is represented by a structure known as the lagena (fig. 305, II. L}. Subsequently the two scalae join at the extremity of the cochlear canal ; the point of the cupola still however remains in contact with the bone, which has now replaced the cartilage, but at a still later period the scala vestibuli, growing further round, separates the cupola from the adjoining osseous tissue.

The ossification around the internal ear is at first confined to the cartilage, but afterwards extends into the thick periosteum between the cartilage and the internal ear, and thus eventually makes its way into the lamina spiralis, etc.

The organ of Corti. In Mammalia there is formed from the


AUDITORY ORGANS.


525


epithelium of the cochlear canal a very remarkable organ known as the organ of Corti, the development of which is of sufficient importance to merit a brief description. A short account of this organ in the adult state may facilitate the understanding of its development.

The cochlear canal is bounded by three walls, the outer one being the osseous wall of the cochlea. The membrane of Reissner bounds it towards



U


FIG. 305. DIAGRAMS OF THE MEMBRANOUS LABYRINTH. (From Gegenbaur.)

I. Fish. II. Bird. III. Mammal.

U. utriculus ; S. sacculus ; US. utriculus and sacculus ; Cr. canalis reuniens ; R. recessus labyrinthi ; UC. commencement of cochlea ; C. cochlear canal ; L. lagena ; PC. cupola at apex of cochlear canal; V. csecal sack of the vestibulum of the cochlear canal.

the scala vestibuli, and the basilar membrane towards the scala tympani. This membrane stretches from the margin of the lamina spiralis to the ligamentum spirale ; the latter being merely an expanded portion of the connective tissue lining the osseous cochlea.

The lamina spiralis is produced into two lips, called respectively the labium tympanicum and labium vestibulare ; it is to the former and longer of these that the basilar membrane is attached. At the margin of the junction of the labium tympanicum with the basilar membrane the former is perforated for the passage of the nervous fibres, and this region is called the habenula perforata.

The labium vestibulare, so called from its position, is shorter than the labium tympanicum and is raised above into numerous blunt teeth. Partly springing out from the labium vestibulare, and passing from near the inner attachment of the membrane of Reissner towards the outer wall of the cochlea, is an elastic membrane, the membrana tectoria. Resting on the basilar membrane is the organ of Corti.

Considering for the moment that a transverse section of the cochlear


$26 ORGAN OF CORTI.


canal only one cell deep is being dealt with, the organ of Corti will be found to consist of a central part composed of two peculiarly shaped rods widely separated below, but in contact above. These are the rods or fibres of Corti. On their outer side, i.e. on the side towards the osseous wall of the canal, is a reticulate membrane which passes from the inner rod of Corti towards the osseous wall of the canal. With their upper extremities fixed in that membrane, and their lower resting on the basilar membrane are three (four in man) cells with auditory hairs known as the outer 'hair cells,' which alternate with three other cells known as Deiters' cells. Between these and the outer attachment of the basilar membrane is a series of cells gradually diminishing in height in passing outwards. On the inner side of the rods of Corti is one hair cell, and then a number of peculiarly modified cells which fill up the space between the two lips of the lamina spiralis.

It will not be necessary to say much in reference to the development of the labium tympanicum and the labium vestibulare.

The labium vestibulare is formed by a growth of the connective tissue which fuses with and passes up between the epithelial cells. The epithelial cells which line its upper (vestibular) border become modified, and remain as its teeth.

The labium tympanicum is formed by the coalescence of the connective tissue layer separating the scala tympani from the cochlear canal with part of the connective tissue of the lamina spiralis. At first these two layers are separate, and the nerve fibres to the organ of Corti pass between them. Subsequently however they coalesce, and the region where they are penetrated by the nervous fibres becomes the habenula perforata.

The organ of Corti itself is derived from the epiblast cells lining the cochlear canal, and consists in the first instance of two epithelial ridges or projections. The larger of them forms the cells on the inner side of the organ of Corti, and the smaller the rods of Corti together with the inner and outer hair cells and Deiters' cells.

At first both these ridges are composed of simple elongated epithelial cells one row deep. The smaller ridge is the first to shew any change. The cells adjoining the larger ridge acquire auditory hairs at their free extremities, and form the row of inner hair cells ; the next row of cells acquires a broad attachment to the basilar membrane, and gives origin to the inner and outer rods of Corti.

Outside the latter come several rows of cells adhering together so as to form a compact mass which is quadrilateral in section. This mass is composed of three upper cells with nuclei at the same level, which form the outer hair cells, each of them ending above in auditory hairs, and three lower cells which form the cells of Deiters. Beyond this the cells gradually pass into ordinary cubical epithelial cells.

As just mentioned, the cells of the second row, resting with their broad bases on the basilar membrane, give rise to the rods of Corti. The breadth of the bases of these cells rapidly increases, and important changes take place in the structure of the cells themselves.


AUDITORY ORGANS. 527

The nucleus of each cell divides ; so that there come to be two nuclei or sometimes three which lie close together near the base of the cell. Outside the nuclei on each side a fibrous cuticular band appears. The two bands pass from the base of the cell to its apex, and there meet though widely separated below. The remaining contents of the cell, between the two fibrous bands, become granular, and are soon to a great extent absorbed ; leaving at first a round, and then a triangular space between the two fibres. The two nuclei, surrounded by a small amount of granular matter, come to lie, each at one of the angles between the fibrous bands and the basilar membrane.

The two fibrous bands become, by changes which need not be described in detail, converted into the rods of Corti each of their upper ends growing outwards into the processes which the adult rods possess.

Each pair of rods of Corti is thus (Bottcher) to be considered as the product of one cell ; and the nuclei embedded in the granular mass between them are merely the remains of the two nuclei formed by the division of the original nucleus of that cell 1 . The larger ridge is for the most part not permanent, and from being the most conspicuous part of the organ of Corti comes to be far less important than the smaller ridge. Its cells undergo a partial degeneration ; so that the epithelium in the hollow between the two lips of the lamina spiralis, which is derived from the larger ridge, comes to be composed of a single row of short and broad cells. In the immediate neighbourhood however of the inner hair cell, one or two of the cells derived from the larger ridge are very much elongated.

The membrana reticularis is a cuticular structure derived from the parts to which it is attached. .

Accessory structures connected with the organ of hearing- in Terrestrial Vertebrata.

In all the Amphibia, Sauropsida and Mammalia, except the Urodela and a few Anura and Reptilia, the first visceral or hyomandibular cleft enters into intimate relations with the organs of hearing, and from it and the adjoining parts are formed the tympanic cavity, the Eustachian tube, the tympanic membrane and the meatus auditorius externus. The tympanic membrane serves to receive from the air the sound vibrations, which are communicated to fluids contained in the true auditory labyrinth by one ossicle or by a chain of auditory ossicles.

The addition to the organ of hearing of a tympanic membrane to receive aerial sound vibrations is an interesting case of the

1 It is not clear from Bottcher's description how it comes about that the inner rods of Corti are more numerous than the outer.


528 THE TYMPANIC CAVITY.

adaptation of a structure, originally required for hearing in water, to serve for hearing in air ; and as already pointed out, the similarity of this membrane to the tympanic membrane of some Insects is also striking.

There is much that is obscure with reference to' the actual development of the above parts of the ear, which has moreover only been carefully studied in Birds and Mammals.

The Eustachian tube and tympanic cavity seem to be derived from the inner part of the first visceral or hyomandibular cleft, the external opening of which becomes soon obliterated. Kolliker holds that the tympanic cavity is simply a dorsally and posteriorly directed outgrowth of the median part of the inner section of this cleft; while Moldenhauer (No. 392) holds, if I understand him rightly, that it is formed as an outgrowth of a cavity called by him the sulcus tubo-tympanicus, derived from the inner aperture of the first visceral cleft together with the groove of the pharynx into which it opens ; and Moldenhauer is of opinion that the greater part of the original cleft atrophies.

The meatus auditorius externus is formed at the region of a shallow depression where the closure of the first visceral cleft takes place. It is in part formed by the tissue surrounding this depression growing up in the form of a wall, and Moldenhauer believes that this is the whole process. Kolliker states however that the blind end of the meatus becomes actually pushed in towards the tympanic cavity.

The tympanic membrane is derived from the tissue which separates the meatus auditorius externus from the tympanic cavity. This tissue is obviously constituted of an hypoblastic epithelium on its inner aspect, an epiblastic epithelium on its outer aspect, and a layer of mesoblast between them, and these three layers give rise to the three layers of which this membrane is formed in the adult. During the greater part of fcetal life it is relatively very thick, and presents a structure bearing but little resemblance to that in the adult.

A proliferation of the connective tissue-cells in the vicinity of the tympanic cavity causes in Mammalia the complete or nearly complete obliteration of the cavity during fcetal life.

The tympanic cavity is bounded on its inner aspect by the osseous investment of the internal ear, but at one point, known


AUDITORY ORGANS. 529


as the fenestra ovalis, the bone is deficient in the Amphibia, Sauropsida and Mammalia, and its place is taken by a membrane ; while in Mammalia and Sauropsida a second opening, the fenestra rotunda, is also present.

These two fenestrae appear early, but whether they are formed by an absorption of the cartilage, or by the nonchondrification of a small area, is not certainly known. The upper of the two, or fenestra ovalis, contains the base of a bone, known in the Sauropsida and Amphibia as the columella. The main part of the columella is formed of a stalk which is held by Parker to be derived from part of the skeleton of the visceral arches, but its nature is discussed in connection with the skeleton, while the base, forming the stapes, appears to be derived from the wall of the periotic cartilage.

In all Amphibia and Sauropsida with a tympanic cavity, the stalk of the columella extends to the tympanic membrane ; its outer end becoming imbedded in this membrane, and serving to transmit the vibrations of the membrane to the fluid in the internal ear. In Mammalia there is a stapes not directly attached to the tympanic membrane by a stalk, and two additional auditory ossicles, derived from parts of the skeleton of the visceral arches, are placed between the stapes and the tympanic membrane. These ossicles are known as the malleus and incus, and the chain of the three ossicles replaces physiologically the single ossicle of the lower forms.

These ossicles are at first imbedded in the connective tissue in the neighbourhood of the tympanic cavity, but on the full development of this cavity, become apparently placed within it ; though really enveloped in the mucous membrane lining it.

The fenestra ovalis is in immediate contiguity with the walls of the utricle, while the fenestra rotunda adjoins the scala tympani.

Hunt (No. 391) holds, from his investigations on the embryology of the pig, that " the Eustachian tube is an involution of the pharyngeal mucous membrane ;" and that "the meatus is an involution of the integument " while " the drum is formed by the Eustachian tube overlapping the extremity of the meatus." Urbantschitsch also holds that the first visceral cleft has nothing to do with the formation of the tympanic cavity and Eustachian tube, and that these parts are derived from lateral outgrowths of the oral cavity.

B. III. 34


530 THE TYMPANIC CAVITY.

The evolution of the accessory parts of the ear would be very difficult to explain on Darwinian principles if the views of Hunt and Urbantschitsch were correct ; and the accepted doctrine, originally proposed by Huschke (No. 389), according to which these structures have originated by a ' change of function' of the parts of the first visceral cleft, may fairly be held till more conclusive evidence has been brought against it than has yet been done.

Tunicata. The auditory organ of the Tunicata (fig. 306) is placed on the under surface of the anterior vesicle of the brain.



FIG. 306. LARVA OF ASCIDIA MENTULA. (From Gegenbaur ; after Kupffer.)

Only the anterior part of the tail is represented.

N'. anterior swelling of neural tube ; IV. anterior swelling of spinal portion of neural tube; n. hinder part of neural tube; ch. notochord ; A", branchial region of alimentary tract ; d. cesophageal and gastric region of alimentary tract ; O. eye ; a, otolith ; o. mouth ; s. papilla for attachment.

It consists of two parts (i) a prominence of the cells of the floor of the brain forming a crista acustica, and (2) an otolith projecting into the cavity of the brain, and attached to the crista by delicate hairs.

The crista acustica is formed of very delicate cylindrical cells, and in its most projecting part is placed a vesicle with clear contents. The otolith is an oval body with its dorsal half pigmented, and its ventral half clear and highly refractive. It is balanced on the highest point of the crista.

The crista acustica would seem to be developed from the cells of the lower part of the front vesicle of the brain. The otolith however is developed from a single cell on the dorsal and right side of the brain. This cell commences to project into the cavity of the brain and its free end becomes pigmented. It gradually grows inwards till it forms a spherical prominence in the cavity of the brain, to the wall of which it is attached by a


AUDITORY ORGANS. 531


stalk. At the same time it travels round the right side of the vesicle of the brain (in a way not fully explained) till it reaches the summit of the crista, which has become in the meantime established.

The auditory organ of the simple Ascidians can hardly be brought into relation with that of the other Chordata, and has most probably been evolved within the Tunicate phylum.

BIBLIOGRAPHY.

Invertebrata.

(384) V. Hensen. "Studien lib. d. Gehororgan d. Decapoden." Zeit.f. wiss. ZooL, Vol. xm. 1863.

(385) O. and R. Hertwig. Das Nervensystem u. d. Sinnesorgane d. Medusen. Leipzig, 1878.

Vertebrata.

(386) A. Boettcher. "Bau u. Entwicklung d. Schnecke." Denkschriften d. kaiserl. Leop. Carol. Akad. d. Wissenschaft., Vol. xxxv.

(387) C. H asse. Die vergleich. Morphologic u. Histologied. hiiutigen Gehororgane d. Wirbelthiere. Leipzig, 1873.

(388) V. Hensen. "Zur Morphologic d. Schnecke." Zeit. f. wiss. ZooL, Vol. XIII. 1863.

(389) E. Huschke. "Ueb. d. erste Bildungsgeschichte d. Auges u. Ohres beim bebriiteten Kiichlein." Isis von Oken, 1831, and Meckel's Archiv, Vol. vi.

(390) Reissner. De Auris internes formatione. Inaug. Diss. Dorpat, 1851.

Accessory parts of Vertebrate Ear.

(391) David Hunt. "A comparative sketch of the development of the ear and eye in the Pig. " Transactions of the International Otological Congress, \ 876.

(392) W. Moldenhaueir. "Zur Entwick. d. mittleren u. ausseren Ohres." Morphol. Jahrbuch) Vol. III. 1877.

(393) V. Urbantschitsch. " Ueb. d. erste Anlage d. Mittelohres u. d. Trommelfelles." Mittheil. a. d. embryol. Instit. Wien, Heft i. 1877.

Olfactory organ.

Amongst the Invertebrata numerous sense organs have been described under the title of olfactory organs. In aquatic animals they often have the form of ciliated pits or grooves, while in the Insects and Crustacea delicate hairs and other structures present on the antennae are usually believed to be organs of smell. Our knowledge of all these organs is however so vague that it

342


532


OLFACTORY PIT.


would not be profitable to deal with them more fully in this place. Amongst the Chordata there are usually well developed olfactory organs.

Amongst the Urochorda (Tunicata) it is still uncertain what organs (if any) deserve this appellation. The organ on the dorsal side of the opening of the respiratory pharynx may very possibly have an olfactory function, but it is certainly not homologous with the olfactory pits of the true Vertebrata, and as mentioned above (pp. 436 and 437), may perhaps be homologous with the pituitary body.

In the Cephalochorda (Amphioxus) there is a shallow ciliated pit, discovered by Kolliker, which is situated on the left side of the head, and is closely connected with a special process of the



FlG. 307. VIEWS OF THE HEAD OF ELASMOBRANCH EMBRYOS AT TWO STAGES AS TRANSPARENT OBJECTS.

A. Pristiurus embryo of the same stage as fig. 28 F.

B. Somewhat older Scyllium embryo.

///. third nerve ; V. fifth nerve ; VII. seventh nerve ; au.n. auditory nerve ; gl. glossopharyngeal nerve; Vg. vagus nerve; fb. fore-brain; pn. pineal gland; mb. midbrain; hb. hind-brain; iv.v. fourth ventricle; cb. cerebellum; ol. olfactory pit; op. eye; au.V. auditory vesicle; m. mesoblast at base of brain; ch. notochord; kt. heart; Vc. visceral clefts; eg. external gills; //. sections of body cavity in the head.


OLFACTORY ORGANS. 533

front end of the brain. It is most probably the homologue of the olfactory pits of the true Vertebrata.

In the true Vertebrata the olfactory organ has usually the form of a pair of pits, though in the Cyclostomata the organ is unpaired.

In all the Vertebrata with two olfactory pits these organs are formed from a pair of thickened patches of the epiblast, on the under side of the fore-brain, immediately in front of the mouth (fig. 307, ol). Each thickened patch of epiblast soon becomes involuted as a pit (fig. 308, N), the lining cells of which become the olfactory or Schneiderian epithelium. The surface of this epithelium is usually much increased by various foldings, which in the Elasmobranchii arise very early, and are bilaterally symmetrical, diverging on each side like the barbs of a feather from the median line. They subsequently become very pronounced (fig. 309), serving greatly to increase the surface of the olfactory epithelium. At a very early stage the olfactory nerve attaches itself to the olfactory epithelium.

In Petromyzon the olfactory organ arises as an unpaired thickening of the epiblast, which in the just hatched larva forms a shallow pit, on the ventral side of the head, immediately in front of the mouth. This pit rapidly deepens, and soon extends itself backwards nearly as far as the infundibulum (fig. 310, 0!}. By the development of the upper lip the opening of the olfactory pit is gradually carried to the dorsal surface of the head, and becomes at the same time narrowed and ciliated (fig. 47, ol). The whole organ forms an elongated sack, and in later stages becomes nearly divided by a median fold into two halves.

It is probable that the unpaired condition of the olfactory organ in the Lamprey has arisen from the fusion of two pits into one ; there is however no evidence of this in the early development ; but the division of the sack into two halves by a median fold may be regarded as an indication of such a paired character in the later stages.

In Myxine the olfactory organ communicates with the mouth through the palate, but the meaning of this communication, which does not appear to be of the same nature as the communication between the olfactory pits and the mouth by the posterior nares in the higher types, is not known.

The opening of the olfactory pit does not retain its embryonic characters. In Elasmobranchii and Chimaera it becomes enclosed by a wall of integument, often deficient on the side of the mouth, so that there is formed a groove leading from the nasal pit towards the angle of the mouth. This groove is


534


EXTERNAL AND INTERNAL NARES.


MB.


u



usually constricted in the middle, and the original single opening of the nasal sack thus becomes nearly divided into two. In Teleostei and Ganoids the division of the nasal opening into two parts becomes complete, but the ventral opening is generally carried off some distance from the mouth, and placed, by the growth of the snout, on the upper surface of the head (figs. 54 and 68). In all these instances it is

/ tftM

probable that the dorsal opening of the nasal sack is homologous with the external nares, and the ventral opening with the posterior nares of higher types. Thus the posterior nares would in fact seem to be represented in all Fishes by a ventral part of the opening of the original nasal pit which either adjoins the border of the mouth (many Elasmobranchii) or is quite separate from the mouth (Teleostei and Ganoidei). In the Dipnoi, Amphibia and all the higher types the oral region becomes extended so as to enclose the posterior nares, and then each nasal pit acquires two openings ; viz. one outside the mouth, the external nares, and one within the mouth, the internal or posterior nares. In the Dipnoi the two nasal openings are very similar to those in Ganoidei and Teleostei, but both are placed on the under surface of the head, the inner one being within the mouth, and the external one is so close to the outer border of the upper lip that it also has been considered by some anatomists to lie within the mouth.

In all the higher types the nasal pits have originally only a single opening, and the ontogenetic process by which the posterior nasal opening is formed has been studied in the Amniota and Amphibia. Amongst the Amniota we may take the Chick as representing the process in a very simple form. The general history of the process was first made out by Kolliker.


FIG. 308. SIDE VIEW OF THE HEAD OF AN EMBRYO CHICK OF THE THIRD DAY AS AN OPAQUE OBJECT. (Chromic acid preparation.)

C.H. cerebral hemispheres ; F.B. vesicle of third ventricle; M.B. mid-brain; Cb. cerebellum; H.B. medulla oblongata; N. nasal pit ; ot. auditory vesicle in the stage of a pit with the opening not yet closed up; op. optic vesicle, with /. lens and ch.f. choroidal fissure.

i F. The first visceral fold ; above it is seen the superior maxillary process.

2, 3, 4 F. Second, third and fourth visceral folds, with the visceral clefts between them.


OLFACTORY ORGANS.


535


The opening of the nasal pit becomes surrounded by a ridge except on its oral side. The deficiency of this ridge on the side of the mouth gives rise to a kind of shallow groove leading from



FIG. 309. SECTION THROUGH THE BRAIN AND OLFACTORY ORGAN OF AN EMBRYO OF SCYLLIUM. (Modified from figures by Marshall and myself.)

c.h. cerebral hemispheres; oLv. olfactory vesicle; olf, olfactory pit ; Seh. Schneiderian folds ; /. olfactory nerve. The reference line has been accidentally taken through the nerve to the brain.

the nasal pit to the mouth. The ridge enveloping the opening of the nasal pit next becomes prolonged along the sides of this groove, especially on its inner one; and at the same time the superior maxillary process grows forwards so as to bound the lower


ma



FIG. 310. DIAGRAMMATIC VERTICAL SECTION THROUGH THE HEAD OF A LARVA OF PETROMYZON.

The larva had been hatched three days, and was 4-8 mm. in length. The optic and auditory vesicles are supposed to be seen through the tissues.

c.h. cerebral hemisphere; th. optic thalamus; in. infundibulum ; pn. pineal gland; mb. mid-brain; cb. cerebellum; md. medulla oblongata; au.v. auditory vesicle; op. optic vesicle; ol. olfactory pit; m. mouth; br.c. branchial pouches; th. thyroid involution; v. ao. ventral aorta ; ht. ventricle of heart ; ch. notochord.


536 EXTERNAL AND INTERNAL NARES.


part of its outer side. The inner and outer ridges, together with the superior maxillary process, enclose a deep groove, connecting the original opening of the nasal pit with the mouth. The process just described is illustrated by fig. 311 A, and it may be seen that the ridge on the inner side of the groove forms the edge of the fronto-nasal process (k).

On the sixth day (Born, 394) the sides of this groove unite together in the middle, and convert it into a canal open at both ends the ventral openings of the canals of the two sides being placed just within the border of the mouth, and forming the posterior nares ; while the external openings form the anterior nares. The upper part of the canal, together with the original



FIG. 311. HEAD OF A CHICK FROM BELOW ON THE SIXTH AND SEVENTH DAYS OF INCUBATION. (From Huxley.)

/". cerebral vesicles ; a. eye, in which the remains of the choroid slit can still be seen in A ; g. nasal pits ; k. fronto-nasal process ; /. superior maxillary process ; i. inferior maxillary process or first visceral arch; 2. second visceral arch; x. first visceral cleft.

In A the cavity of the mouth is seen enclosed by the fronto-nasal process, the superior maxillary processes and the first pair of visceral arches. At the back of it is seen the opening leading into the throat. The nasal grooves leading from the nasal pits to the mouth are already closed over.

In B the external opening of the mouth has become much constricted, but it is still enclosed by the fronto-nasal process and superior maxillary processes above, and by the inferior maxillary processes (first pair of visceral arches) below.

The superior maxillary processes have united with the fronto nasal process, along nearly the whole length of the latter.

nasal pit, is alone lined by olfactory epithelium ; the remaining epithelium of the nasal cavity being indifferent epiblastic epi


OLFACTORY ORGANS.


537


thelium. Further changes subsequently take place in connection with the posterior nares, but these are described in the section dealing with the mouth.

In Mammalia the general formation of the anterior and posterior nares is the same as in Birds ; but, as shewn by Dursy and Kolliker, an outgrowth from the inner side of the canal between the two openings arises at an early period ; and becoming separate from the posterior nares and provided with a special opening into the mouth, forms the organ of Jacobson. The general relations of this organ when fully formed are shewn in fig. 312.

In Lacertilia the formation of the posterior nares differs in some particulars from that in Birds (Born). A groove is formed leading from the primitive nasal pit to the mouth, bordered on its inner side by the swollen edge of the fronto-nasal process, and on its outer by an outernasal process ; while the superior maxillary process does not assist in bounding it. On the inner side of the narrowest part of this groove there is formed a large lateral diverticulum, which is lined by a continuation of the Schneiderian epithelium, and forms the rudiment of Jacobson's organ. The nasal groove continues to grow in length, but soon becomes converted into a canal by the junction of the outer-nasal process with the fronto-nasal process. This canal is open at both ends : at its dorsal end is placed the original opening of the nasal pit, and its ventral opening is situated within the cavity of the mouth. The latter forms the primitive posterior nares. The superior maxillary process soon grows inwards on the under side of the posterior part of the nasal passage, and assists in forming its under wall. This ingrowth of the superior maxillary process is the rudiment of the hard palate.

On the conversion of the nasal groove into a closed passage, the opening of Jacobson's organ into the groove becomes concealed ; and at a later period Jacobson's organ becomes completely shut off from the nasal cavity, and opens into the mouth at the front end of an elongated groove leading back to the posterior nares.

In Amphibia the posterior nares are formed in a manner very different from that of the Amniota. At an early stage a shallow groove is formed leading from the nasal pit to the mouth ; but this groove instead



J


FIG. 312. SECTION THROUGH

THE NASAL CAVITY AND JA COBSON'S ORGAN. (From Gegenbaur.)

sn. septum nasi ; en. nasal cavity ; y. Jacobson's organ ; d, edge of upper jaw.


538 ORGANS OF THE LATERAL LINE.

of forming the posterior nares soon vanishes, and by the growth of the front of the head the nasal pits are carried farther away from the mouth.

The actual posterior nares are formed by a perforation in the palate, opening into the blind end of the original nasal pit.

Considering that the various stages in the formation of the posterior nares of the Amniota are so many repetitions of the adult states of lower forms, it may probably be assumed that the mode of formation of the posterior nares in Amphibia is secondary, as compared with that in the Amniota.

A diverticulum of the front part of the nasal cavity of the Anura is probably to be regarded as a rudimentary form of Jacobson's organ.

BIBLIOGRAPHY.

(394) G. Born. "Die Nasenhohlen u. d. Thranennasengang d. amnioten Wirbelthiere." Parts I. and II. Morphologisches Jahrbuch, Bd. V., 1879.

(395) A. Kollicker. " Ueber die Jacobson'schen Organe des Menschen." Festschrift f. Rienecker, 1877.

(396) A. M. Marshall. "Morphology of the Vertebrate Olfactory Organ." Quart. Journ. of Micr. Science, Vol. xix., 1879.

Sense organs of the lateral line.

Although I do not propose dealing with the general development of various sense organs of the skin, there is one set of organs, viz. that of the lateral line, which, both from its wide extension amongst the Ichthyopsida and from the similarity of some of its parts to certain organs found amongst the Chastopoda 1 , has a great morphological importance.

The organs of the lateral line consist as a rule of canals, partly situated in the head, and partly in the trunk. These canals open at intervals on the surface, and their walls contain a series of nerve-endings. The branches of the canal in the head are innervated for the most part by the fifth pair, and those of the trunk by the nervus lateralis of the vagus nerve. There is typically but a single canal in the trunk, the openings and nerve-endings of which are segmentally arranged.

Two types of development of these organs have been found. One of these is characteristic of Teleostei ; the other of Elasmobranchii.

In just hatched Teleostei, Schulze (No. 402) found that instead of the normal canals there was present a series of sense bulbs, projecting freely on the surface and partly composed of cells with stiff hairs. In most

1 The organs which resemble those of the lateral line are the remarkable sense organs found by Eisig in the Capitellidse (Mittheil. a. d. ZooL Station zu Neapel, Vol. I.) ; but I am not inclined to think that there is a true homology between these organs and the lateral line of Vertebrata. It seems to me probable that the segmentally arranged optic organs of Polyophthalmus are a special modification of the more indifferent sense organs of the Capitellidse. The close affinity of these two types of Chsetopods is favourable to this view.


SENSE ORGANS. 539


cases each bulb is enclosed in a delicate tube open at its free extremity ; while the bulbs correspond in number with the myotomes. In some Teleostei (Gobius, Esox, etc.) such sense organs persist through life ; in most forms however each organ becomes covered by a pair of lobes of the adjacent tissue, one formed above and the other below it. The two lobes of each pair then unite and form a tube open at both ends. The linear series of tubes so formed is the commencement of the adult canal ; while the primitive sense bulbs form the sensory organs of the tubes. The adjacent tubes partially unite into a continuous canal, but at their points of apposition pores are left, which place the canal in communication with the exterior.

Besides these parts, I have found that there is present in the just hatched Salmon a linear streak of modified epidermis on the level of the lateral nerve, and from the analogy of the process described below for Elasmobranchii it appears to me probable that these streaks play some part in the formation of the canal of the lateral line.

In Elasmobranchii (Scyllium) the lateral line is formed as a linear thickening of the mucous layer of the epidermis. This thickening is at first very short, but gradually grows backwards, its hinder end forming a kind of enlarged growing point. The lateral nerve is formed shortly after the lateral line, and by the time that the lateral line has reached the level of the anus the lateral nerve has grown back for about two-thirds of that distance. The lateral nerve would seem to be formed as a branch of the vagus, but is at first half enclosed in the modified cells of the lateral line (fig. 275, nl) 1 , though it soon assumes a deeper position.

A permanent stage, more or less corresponding to the stage just described in Elasmobranchii, is retained in Chimasra, and Echinorhinus spinosus, where the lateral line has the form of an open groove (Solger, No. 404).

The epidermic thickening, which forms the lateral line, is converted into a canal, not as in Teleostei by the folding over of the sides, but by the formation of a cavity between the mucous and epidermic layers of the epiblast, and the subsequent enclosure of this cavity by the modified cells of the mucous layer of the epiblast which constitute the lateral line. The cavity first appears at the hind end of the organ, and thence extends forwards.

After its conversion into a canal the lateral line gradually recedes from the surface ; remaining however connected with the epidermis at a series of points corresponding with the segments, and at these points perforations are eventually formed to constitute the segmental apertures of the system.

The manner in which the lumen of the canal is formed in Elasmobranchs bears the same relation to the ordinary process of conversion of a groove into a canal that the formation of the auditory involution

1 Gotte and Semper both hold that the lateral nerve, instead of growing in a centrifugal manner like other nerves, is directly derived from the epiblast of the lateral line. For the reasons which prevent me accepting this view I must refer the reader to my Monograph on Elasmobranch Fishes, pp. 141 146.


540 ORGANS OF THE LATERAL LINE.

in Amphibia does to the same process in Birds. In both Elasmobranchii and Amphibia the mucous layer of the epiblast behaves exactly as does the whole epiblast in the other types, but is shut off from the surface by the passive epidermic layer of the epiblast.

The mucous canals of the head and the ampullae are formed from the mucous layer of the epidermis in a manner very similar to the lateral line ; but the nerves to them arise as simple branches of the fifth and seventh nerves, which unite with them at a series of points, but do not follow their course like the lateral nerve.

It is clear that the canal of the lateral line is secondary, as compared with the open groove of Chimaera or the segmentally arranged sense bulbs of young Teleostei ; and it is also clear that the phylogenetic mode of formation of the canal consisted in the closure of a primitively open groove. The abbreviation of this process in Elasmobranchii was probably acquired after the appearance of food-yolk in the egg, and the consequent disappearance of a free larval stage.

While the above points are fairly obvious it does not seem easy to decide a priori whether a continuous sense groove or isolated sense bulbs were the primitive structures from which the canals of the lateral line took their origin. It is equally easy to picture the evolution of the canal of the lateral line either from (i) a continuous unsegmented sense line, certain points of which became segmentally differentiated into special sense bulbs, while the whole subsequently formed a groove and then a canal ; or from (2) a series of isolated sense bulbs, for each of which a protective groove was developed ; and from the linear fusion of which a continuous canal became formed.

From the presence however of a linear streak of modified epidermis in larval Teleostei, as well as in Elasmobranchii, it appears to me more probable that a linear sense streak was the primitive structure from which all the modifications of the lateral line took their origin, and that the segmentally arranged sense bulbs of Teleostei are secondary differentiations of this primitive structure.

The, at first sight remarkable, distribution of the vagus nerve to the lateral line is probably to be explained in connection with the evolution of this organ. As is indicated both by its innervation from the vagus, as also from the region where it first becomes developed, the lateral line was probably originally restricted to the anterior part of the body. As it became prolonged backwards it naturally carried with it the vagus nerve, and thus a sensory branch of this nerve has come to innervate a region which is far beyond the limits of its original distribution.

BIBLIOGRAPHY.

(397) F. M. Balfour. A Monograph onthe development of Elasnwbranch Fishes, pp. 141 146. London, 1878.

(398) H. Eisig. "Die Segmentalorgane cl. Capitelliden." Mitthcil. a. d. zool. Station zu Neapel> Vol. I. 1879.


BIBLIOGRAPHY. 541


(399) A. Gotte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.

(400) Fr. Leydig. Lehrbuch d. Histologie des Memchen u. d. Thiere. Hamm.

1857 (401) Fr. Leydig. Neue Beitrdge z. anat. Kenntniss d. Hautdecke u. Hautsinnesorgane d. Fische. Halle, 1879.

(402) F. E. Schulze. " Ueb. d. Sinnesorgane d. Seitenlinie bei Fischen und Amphibien." Archiv f. mikr. Anat., Vol. vi. 1870.

(403) C. Semper. "Das Urogenitalsy stem d. Selachier." Arbeit, a. d. zoo!.zoot. Instil. Wiirzburg, Vol. II.

(404) B. Solger. "Neue Untersuchungen zur Anat. d. Seitenorgane d. Fische." Archiv f. mikr. Anat., Vol. xvn. and xvm. 1879 an< * !88o.


CHAPTER XVIII.


THE NOTOCHORD, THE VERTEBRAL COLUMN, THE RIBS AND THE STERNUM.


INTRODUCTION.

AMONGST the products of that part of the mesoblast which constitutes the connective tissue of the body special prominence must be given to the skeleton of the Vertebrata, from its importance in relation to numerous phylogenetic and morphological problems.

The development of the skeleton is however so large a subject that it cannot be satisfactorily dealt with except in a special treatise devoted to it ; and the following description must be regarded as a mere sketch, from which detail has been as far as possible excluded.

In the lowest Chordata the sole structure present, which deserves to be called a skeleton, is the notochord. Although the notochord often persists as an important organ in the true Vertebrata, yet there are always added to it various skeletal structures developed in the mesoblast. Before entering into a systematic description of these, it will be convenient to say a few words as to the general characters of the skeleton.

Two elements, distinct both in their genesis and structure, are to be recognized in the skeleton. The one, forming the true primitive internal skeleton or endoskeleton, is imbedded within the muscles and is originally formed in cartilage. In many instances it retains a cartilaginous consistency through life, but in the majority of cases it becomes gradually ossified, and


NOTOCHORD AND VERTEBRAL COLUMN. 543

converted into true bone. Bones so formed are known as cartilage bones.

The other element is originally formed by the fusion of the ossified bases of the dermal placoid scales already described in Chapter xiv., or by the fusion of the ossified bases of teeth situated in the mucous membrane of the mouth. In both instances the plates of bone so formed may lose the teeth or spines with which they were in the first instance covered, either by absorption in the individual, or phylogenetically by their gradually ceasing to be developed. The plates of bone, which originated by the above process, become in higher types directly developed in the connective tissue beneath the skin ; and gradually acquire a deeper situation, and are finally so intimately interlocked with parts of the true internal skeleton, that the two sets of elements can only be distinguished by the fact of the one set ossifying in cartilage and the other in membrane.

It seems probable that in the Reptilia, and possibly the extinct Amphibia, dermal bones have originated in the skin without the intervention of superjacent spinous structures.

In cases where a membra nebone, as the dermal ossifications are usually called, overlies a part of the cartilage, it may set up ossification in the latter, and the cartilage bone and membrane bone may become so intimately fused as to be quite inseparable. It seems probable that in cases of this kind the compound bone may in the course of further evolution entirely lose either its cartilaginous element or its membranous element ; so that cases occasionally occur where the development of a bone ceases to be an absolutely safe guide to its evolution.

As to the processes which take place in the ossification of cartilage there is still much to be made out. Two processes are often distinguished, viz. (i) a process known as ectostosis, in which the ossification takes place in the perichondrium, and either simply surrounds or gradually replaces the cartilage, and (2) a process known as endostosis, where the ossification actually takes place between the cartilage cells. It seems probable however (Gegenbaur, Vrolik) that there is no sharp line to be drawn between these two processes ; but that the ossification almost always starts from the perichondrium. In the higher types, as a rule, the vessels of the perichondrium extend into


544 MEMBRANE BONES AND CARTILAGE BONES.

the cartilage, and the ossification takes place around these vessels within the cartilage; but in the lower types (Pisces, Amphibia) ossification is often entirely confined to the perichondrium ; and the cartilage is simply absorbed.

The regions where ossification first sets in are known as centres of ossification; and from these centres the ossification spreads outwards. There may be one or more centres for a bone.

The actual causes which in the first instance gave rise to particular centres of ossification, or to the ossification of particular parts of the cartilage, are but little understood ; nor have we as yet any satisfactory criterion for determining the value to be attached to the number and position of centres of ossification. In some instances such centres appear to have an important morphological significance, and in other instances they would seem to be determined by the size of the cartilage about to be ossified.

There is no doubt that the membrane bones and cartilage bones can as a rule be easily distinguished by their mode of development ; but it is by no means certain that this is always the case. It is necessarily very difficult to establish the homology between bones, which develop in one type from membrane and in another type from cartilage ; but there are without doubt certain instances in. which the homology between two bones would be unhesitatingly admitted were it not for the difference in their development. The most difficult cases of this kind are connected with the shoulder-girdle.

The possible sources of confusion in the development of bones are obviously two. (i) A cartilage bone by origin may directly ossify in membrane, without the previous development of cartilage, and (2) a membrane bone may in the first instance be formed in cartilage.

The occurrence of the first of these is much more easy to admit than that of the second ; and there can be little doubt that it sometimes takes place. In a large number of cases it would moreover cause no serious difficulty to the morphologist.

BIBLIOGRAPHY of the origin of the Skeleton.

(405) C. Gegenbaur. " Ueb. primare u. secundare Knochenbildung mit besonderer Beziehung auf d. Lehre von dem Primordialcranium." Jcnaischc Zcitschrifl, Vol. III. 1867.

(406) O. Hertwig. " Ueber Ban u. Entwicklung d. Placoidschuppen u. d. Ziihne d. Selachicr." Jenaische Zeitsckrift, Vol. viu. 1874.


NOTOCHORD AND VERTEBRAL COLUMN.


545


(407) O. Hertwig. " Ueb. cl. Zahnsystem d. Amphibien u. seine Bedeutung f. d. Genese d. Skelets d. Mundhohle." Archiv f. mikr. Anat., Vol. xi. Supplementheft, 1874.

(408) O. Hertwig. " Ueber d. Hautskelet cl. Fische." Morphol. Jahrbmh, Vol. II. 1876. (Siluroiden u. Acipenseriden.)

(409) O. Hertwig. "Ueber d. Hautskelet d. Fische (Lepidosteus u. Polypterus)." Morph. Jahrbnch, Vol. v. 1879.

(410) A. Kolliker. " Allgemeine Betrachtungen iib. die Entstehung d. knochernen Schadels d. Wirbelthiere. " Berichte r. d. kijnigl. zoot. Anstalt z. Wiirzburg, 1849.

(411) Fr. Leydig. " Histologische Bemerkungen lib. d. Polypterus bichir." Zeit.f. wiss. Zool., Vol. v. 1858.

(412) H. Miiller. " Ueber d. Entwick. d. Knochensubstanz nebst Bemerkungen, etc." Zeit. f. wiss. ZooL, Vol. ix. 1859.

(413) Williamson. "On the structure and development of the Scales and Bones of Fishes." Phil. Trans., 1851.

(414) Vrolik. " Studien lib. d. Verknocherung u. die Knochen d. Schadels d. Teleostier. " Niederliindisches Archiv f. Zoologie, Vol. I.


NotocJtord and Vertebral column.

The primitive axial skeleton of the Chordata consists of the notochord and its sheath. It persists as such in the adult in Amphioxus, and constitutes, in embryos of all Vertebrata, for a considerable period of their early embryonic life, the sole representative of the axial skeleton.

The Notochord. The early formation of the notochord has already been described in detail (pp. 292 300). It is developed, in most if not all cases, as an axial differentiation of the hypoblast, and forms at first a solid cord of cells, without a sheath, placed between the nervous system and the dorsal wall of the alimentary tract, and extending from the base of the front of the



mid-brain to the end of the tail. The section in the region of the brain will be dealt with by itself. That H. HI.


FIG. 313. HORIZONTAL SECTION THROUGH THE TRUNK OF AN EMBRYO OF SCYLLIUM CONSIDERABLY YOUNGER THAN F IN FIG. 28.

The section is taken at the level of the notochord, and shews the separation of the cells to form the vertebral bodies from the muscle-plates.

ch. notochord ; ep. epiblast ; Vr. rudiment of vertebral body; ;;//. muscle-plate; mp'. portion of muscle-plate already differentiated into longitudinal muscles.

35


546


NOTOCHORD.


in the trunk forms the basis round which the vertebral column is moulded.

The early histological changes in the cells of the notochord are approximately the same in all the Craniata. There is formed by the superficial cells of the notochord a delicate sheath, which soon thickens, and becomes a welldefined structure. Vacuoles (one or more to each cell) are formed in the cells of the notochord, which enlarge till the whole notochord becomes almost entirely formed of large vacuoles separated by membranous septa which form a complete sponge-like reticulum 'fig. 313). In the Ichthyopsida most of the protoplasm with the nuclei is carried to the periphery, where it forms a special nucleated layer sometimes divided into definite epithelial-like cells (fig. 314), while in the meshes of the reticulum a few nuclei surrounded by a little protoplasm still remain. In the Amniotic Vertebrata, probably owing to the early atrophy of the notochord, the distribution of the nuclei in the spaces of the mesh-work remains fairly uniform.



FIG. 314. SECTION THROUGH THE SPINAL COLUMN OF A YOUNG SALMON. (From Gegenbaur.)

cs. sheath of notochord ; k. neural arch ; k'. haemal arch; m. spinal cord; a. dorsal aorta ; z'. cardinal veins.


In the early stages of development the spaces in the notochordal spongework, each containing a nucleus and protoplasm, probably represent cells. In the types in which the notochord persists in the adult the mesh-work becomes highly complicated, and then forms a peculiar reticulum filled with gelatinous material, the spaces in which do not indicate the outlines of definite cells (figs. 315 and 318).

Around the sheath of the notochord there is formed in the Cyclostomata, Ganoidei, Elasmobranchii and Teleostei an elastic membrane usually known as the membrana elastica externa.

In most Vertebrates the notochord and its sheath either atrophy completely or become a relatively unimportant part of the axial skeleton; but in the Cyclostomata (fig. 315) and in the Selachioidean Ganoids (Acipenser, etc.) they persist as the sole representative of the true vertebral axis. The sheath becomes very much thickened; and on the membrana elastica covering


NOTOCHORD AND VERTEBRAL COLUMN.


547


Ch


it the vertebral arches directly rest. In Klasmobranchii the sheath of the notochord undergoes a more complicated series of changes, which result first of all in the formation of a definite unsegmented cartilaginous tube 1 round the notochord, and subsequently (in most forms) in the formation of true vertebral bodies. Between the membrana elastica externa and the sheath of the notochord a layer of cells becomes interposed (fig. 316, n}, which lie in a matrix not sharply separated from the sheath of the notochord. The cells which form this layer appear to be derived from a special investment of the notochord, and to have penetrated through the membrana elastica externa to reach their final situation. The layer with these cells soon increases 7/> cardmal vems in thickness, and forms a continuous unsegmented tube of fibrous tissue with flattened concentrically arranged nuclei (fig. 317, Vb}. Externally is placed c f, the membrana elastica externa (met}, while within is the cuticular sheath of the notochord. This tube is the cartilaginous tube spoken of above and is known as the cartilaginous sheath of the notochord.



FIG. 315. SECTION THROUGH THE VERTEBRAL COLUMN OF AMMOCCETES. (From Gegenbaur.)

Ch. notochord ; c s. notochordal sheath ; m. spinal cord ; a. aorta ;


^ \


FIG. 316. LONGITUDINAL SECTION THROUGH A SMALL PART OF THE NOTOCHORD AND ADJOINING PARTS OF A SCYLLIUM EMBRYO, AT THE TIME OF THE FIRST FORMATION OF THE CARTILAGINOUS SHEATH.

ch. notochord; sc. sheath of notochord; n. nuclei of cartilaginous sheath; me.e. membrana elastica externa.


The exact origin of the cartilaginous tube just described is a question of fundamental importance with reference to the origin of the vertebral column and the homologies of its constituent parts ; but is by no means easy to settle. In the account of the subject in my memoir on Elasmobranch Fishes I held with Gegenbaur that it arose from

1 This tube consists of a peculiar form of fibrous tissue rather than true cartilage, though part of it subsequently becomes hyaline cartilage.

352


548


SHEATH OF THE NOTOCHORD.


a layer of cells outside the sheath of the notochord, on the exterior of which the membrana elastica externa was subsequently formed. To this view Gotte (No. 419) also gave his adhesion. Schneider has since (No. 429) stated that this is not the case, but that, as described above, the membrana elastica externa is formed before the layer of cartilage. I have since worked over this subject again, and am on the whole inclined to adopt Schneider's correction.

It follows from the above description that the cartilaginous tube in question is an essential part of the sheath of the notochord, and that it is to some extent homologous with the notochordal sheath of the Sturgeon and the Lamprey, and not an entirely new formation.

This sheath forms the basis of the centra of the future vertebrae. In a few adult forms, i.e. Chimaera and the Dipnoi, it



FIG. 317. TRANSVERSE SECTION THROUGH THE VENTRAL PART OF THE NOTOCHORD AND ADJOINING STRUCTURES OF AN ADVANCED SCYLLIUM EMBRYO AT THE ROOT OF THE TAIL.

Vb. cartilaginous sheath of the notochord ; ha. hasmal arch ; vp. process to which the rib is articulated ; mcl. membrana elastica externa ; ch. notochord ; ao. aorta ; . caudal vein.


retains its primitive condition, except that in Chimaera there are present delicate ossified rings more numerous than the arches ; while in the Notidani, Laemargi and Echinorhini the


NOTOCHORD AND VERTEBRAL COLUMN. 549

indications of vertebrae are imperfectly marked out. The further history of this sheath in the forms in which true vertebrae are formed can only be dealt with in connection with the formation of the vertebral arches.

In Teleostei there is present, as in Elasmobranchii, an elastica externa, and an inner notochordal sheath. The elastica externa contains, according to Gotte, cells. These cells, if present, are however very difficult to make out, but in any case the so-called elastica externa appears to correspond with the cartilaginous sheath of Elasmobranchii together with its enveloping elastica, since ossification, when it sets in, occurs in this layer. The sheath within becomes unusually thick.

In the Amphibia and in the Amniota no membrane is present which can be identified with the membrana elastica externa of the Elasmobranchii, Teleostei, etc. In Amphibia (Gotte) there is formed round the notochord a cellular sheath, which has very much the relations of the cartilaginous tube around the notochord of Elasmobranchii, and is developed in the same way from the perichordal connective tissue cells. It is only necessary to suppose that the rnembrana elastica externa has ceased to be developed (which in view of its extreme delicacy and unimportant function in Elasmobranchii is not difficult to do) and this cellular sheath would then obviously be homologous with the cartilaginous tube in question. In the Amniota an external sheath of the notochord cannot be traced as a distinct structure, but the connective tissue surrounding the notochord and spinal cord is simply differentiated into the vertebral bodies and vertebral arches.

Vertebral arches and Vertebral bodies.

Cyclostomata. The Cyclostomata are the most primitive forms in which true vertebral arches are present. Their ontogeny in this group has not been satisfactorily worked out. It is however noticeable in connection with them that they form for the most part isolated pieces of cartilage, the segmental arrangement of which is only imperfect.

Elasmobranchii. In the Elasmobranchii the cells forming the vertebral arches are derived from the splanchnic layer of the mesoblastic somites. They have at first the same segmentation


55O NEURAL AND H^MAL ARCHES.

as the somites (fig. 313, Vr), but this segmentation is soon lost, and there is formed round the notochord a continuous sheath of embryonic connective tissue cells, which gives rise to the arches of the vertebrae, the tissue forming the dura mater, the perichondrium, and the general investing connective tissue.

The changes which next follow result in what has been known since Remak as the secondary segmentation of the vertebral column. This segmentation, which occurs in all Vertebrata with true vertebrae, is essentially the segmentation of the continuous investment of the notochord and spinal cord into vertebral bodies and vertebral arches. It does not however follow the lines of the segmentation of the muscle-plates, but is so effected that the centres of the vertebral bodies are opposite the septa between the muscle-plates.

The explanation of this character in the segmentation is not difficult to find. The primary segmentation of the body is that of the muscle-plates, which were present in the primitive forms in which vertebrae had not appeared. As soon however as the notochordal sheath was required to be strong as well as flexible, it necessarily became divided into a series of segments.

The condition under which the lateral muscles can best cause the flexure of the vertebral column is clearly that each myotome shall be capable of acting on two vertebrae ; and this condition can only be fulfilled when the myotomes are opposite the intervals between the vertebrae. For this reason, when the vertebrae became formed, their centres were opposite not the middle of the myotomes but the inter-muscular septa.

These considerations fully explain the characters of the secondary segmentation of the vertebral column. On the other hand the primary segmentation (fig. 313) of the vertebral rudiments is clearly a remnant of a condition when no vertebral bodies were present ; and has no greater morphological significance than the fact that the cells of the vertebrae were derived from the segmented muscle-plates, and then became fused into a continuous sheath around the notochord and nervous axis ; till finally they became in still higher forms differentiated into vertebrae and their arches.

During the stage represented in fig. 28 g, and somewhat before the cartilaginous sheath of the notochord is formed, there appear four special concentrations of the mesoblastic tissue adjoining the notochord, two of them dorsal (neural) and two of them ventral (haemal). They are not segmented, and form four ridges, seated on the sides of the notochord. They are united


NOTOCHORD AND VERTEBRAL COLUMN.


551


with each other by a delicate layer of tissue, and constitute the substance in which the neural and haemal arches subsequently become differentiated.

At about the time when the first traces of the cartilaginous sheath of the notochord arise, differentiations take place in the neural and haemal ridges. In the neural ridge two sets of arches are formed for each myotome, one resting on the cartilaginous sheath of the notochord in the region which will afterwards form the centrum of a vertebra, and constituting a true neural arch ; and a second separate from the cartilaginous sheath, forming an intercalated piece 1 . Both of them soon become hyaline cartilage.

There is a considerable portion of the original tissue of the neural ridge, especially in the immediate neighbourhood of the notochord, which is not employed in the formation of the neural arches. This tissue has a fibrous character and becomes converted into the perichondrium and other parts.

The haemal arches are formed from the haemal ridge in precisely the same way as the neural arches, but interhsemal intercalated pieces are often present. In the region of the tail the haemal arches are continued into ventral processes which meet below, enclosing the aorta and caudal veins.

1 The presence of intercalated pieces in the neural arch system of Elasmobranchii, Chimaera, etc. is probably not the indication of an highly differentiated type of neural arch, but of a transitional type between an imperfect investment of the spinal cord by isolated cartilaginous bars, and a complete system of neural arches like that in the higher Vertebrata.



FIG. 318. SECTION THROUGH THE VERTEBRAL COLUMN OF AN ADVANCED EMBRYO OF SCYLLIUM IN THE REGION OF THE TAIL.

na. neural arch ; ha. haemal arch ; ch. notochord ; sh. inner sheath of notochord ; ne. membrana elastica externa.


552 NEURAL AND H^iMAL ARCIIKS.

Since primitively the postanal gut was placed between the aorta and the caudal vein, the haemal arches potentially invest a caudal section of the body cavity. In the trunk region they do not meet ventrally, but give support to the ribs. The structures just described are shewn in section in fig. 318, in which the neural (110) and haemal (ha) arches are shewn resting upon the cartilaginous sheath of the notochord.

While these changes are being effected in the arches the cartilaginous sheath of the notochord undergoes important differentiations. In the vertebral regions opposite the origin of the neural and haemal arches (fig. 318) its outer part becomes hyaline cartilage, while the inner parts adjoining the notochord undergo a somewhat different development, the notochord in this part becomes at the same time somewhat constricted. In the intervertebral regions the cartilaginous sheath of the notochord becomes more definitely fibrous, while the notochord is in no way constricted. A diagrammatic longitudinal section through the vertebral column, while these changes are being effected, is shewn in fig. 320 B.

These processes are soon carried further. The notochord within the vertebral body becomes gradually constricted, especially in the median plane, till it is here reduced to a fibrous band, which gradually enlarges in either direction till it reaches its maximum thickness in the median plane of the intervertebral region. The hyaline cartilage of the vertebral region forms a vertebral body in which calcification may to some extent take place. The cartilage of the base of the arches gradually spreads over it, and on the absorption of the membrana elastica externa, which usually takes place long before the adult state is reached, the arch tissue becomes indistinguishably fused with that of the vertebral bodies, so that the latter are compound structures, partly formed of the primitive cartilaginous sheath, and partly of the tissue of the bases of the neural and haemal arches. Owing to the beaded structure of the notochord the vertebral bodies take of necessity a biconcave hourglass-shaped form.

The intervertebral regions of the primitive sheath of the notochord form fibrous intervertebral ligaments enclosing the unconstricted intervertebral sections of the notochord.


NOTOCHORD AND VERTKBKAL COLUMN. 553

A peculiar fact may here be noticed with reference to the formation of the vertebral bodies in the tail of Scyllium, Raja, and possibly other forms, viz. that there are double as many -vertebral bodies as there are myotomes and spinal nerves. This is not due to a secondary segmentation of the vertebras but, as I have satisfied myself by a study of the development, takes place when the vertebral bodies first become differentiated. The possibility of such a relation of parts is probably to be explained by the fact that the segmentation of the vertebral column arose subsequently to that of the nerves and myotomes.

Ganoidei. In Acipenser and other cartilaginous Ganoids the haemal and neural arches are formed as in Elasmobranchii, and rest upon the outer sheath of the notochord. Since however the sheath of the notochord is never differentiated into distinct vertebrae, this primitive condition is retained through life.

Teleostei. In Teleostei the formation of the vertebral arches and bodies takes place in a manner, which can be reduced, except in certain minor points, to the same type as that of Elasmobranchii.

There are early formed (fig. 314 k and k] neural and haemal arches resting upon the outer sheath of the notochord. The latter structure, which, as mentioned on p. 549, corresponds to the cartilaginous sheath of the notochord of Elasmobranchii, soon becomes divided into vertebral and intervertebral regions. In the former ossification directly sets in without the sheath acquiring the character of hyaline cartilage (Gotte, 419). The latter forms the fibrous intervertebral ligaments. The notochord exhibits vertebral constrictions.

The ossified outer sheath of the notochord forms but a small part of the permanent vertebrae. The remainder is derived partly from an ossification of the connective tissue surrounding the sheath, and partly from the bases of the arches, which do not spread round the primitive vertebral bodies as in Elasmobranchii. The ossifications in the tissue surrounding the sheath usually (fig. 319) take the form of a cross, while the bases of the arches (k and k'} remain as four cartilaginous radii between the limbs of the osseous cross. In some instances the bases of the arches also become ossified, and are then with difficulty distinguishable from the other parts of the secondary vertebral body. The parts of the arches outside the vertebral bodies are for the most part ossified (fig. 319). In correlation with the vertebral constrictions of the notochord the vertebral bodies are biconcave.

Amphibia. Of the forms of Amphibia so far studied embryologically the Salamandridae present the most primitive type of formation of the vertebral column.

It has already been stated that in Amphibia there is present


554


VERTEBRAL COLUMN OF AMPHIBIA.


around the notochord a cellular sheath, equivalent to the cartilaginous sheath of Elasmobranchii. In the tissue on the dorsal side of this sheath a series of cartilaginous processes becomes formed. These processes are the commencing neural arches ; and they rest on the cellular sheath of the notochord opposite the middle of the vertebral regions.

A superficial osseous layer becomes very early formed in each vertebral region of the cellular sheath ; while in each of the intervertebral regions, which are considerably shorter than the vertebral, there is developed a ring-like cartilaginous thickening of the sheath, which projects inwards so as to constrict the notochord. At a period before this thickening has attained considerable dimensions the notochord becomes sufficiently

constricted in the centre of each FlG - 319- VERTICAL SECTIONTHROUGH THE MIDDLE OF A VER vertebral region to give a biconcave TEBRA OF Esox LUCIUS (PIKE). form to the vertebrae for a very < From Gegenbaur.) short period of fcetal life.



The stage with biconcave vertebrae is retained through life in the Perennibranchiata and Gymnophiona.


ch. notochord ; cs. notochordal sheath; /. and K. cartilaginous tissue of the neural and haemal arches ; h. osseous hremal process ; n. spinal canal.


The chief peculiarity which distinguishes the later history of their vertebral column from that of fishes consists in the immense development of the intervertebral thickenings just mentioned, which increase to such an extent as to reduce the notochord, where it passes through them, to a mere band ; while the cartilage of which they are composed becomes differentiated into two regions, one belonging to the vertebra in front, the other to that behind, the hinder one being convex, and the anterior concave. The two parts are not however absolutely separated from each other.

By these changes each vertebra comes to be composed of (i) a thin osseous somewhat hourglass-shaped cylinder with a dilated portion of the notochord in its centre, and (2 and 3) of two


NOTOCHORD AND VERTEBRAL COLUMN.


555


halves of two intervertebral cartilages, viz. an anterior convex half and a posterior concave half. The vertebrae thus come to be opisthoccelous. A longitudinal section through the vertebral column at this stage is diagrammatically shewn in fig. 320 C.

To the centre of each of these vertebrae the neural arches, the origin of which was described above, become in the meantime firmly attached ; and grow obliquely upwards and A B CUE



FIG. 320. DIAGRAM REPRESENTING THE MODE OF DEVELOPMENT OK THE

VERTEBRA IN THE DIFFERENT TYPES. (From Gegenbaur.)

A. Ideal type in which distinct vertebrae are not established.

B. Type of Pisces with vertebral constrictions of the notochord.

C. Amphibian type, with intervertebral constrictions of the notochord by the intervertebral parts of the cellular sheath.

D. Intervertebral constriction of the notochord as effected in Reptilia and Aves.

E. Vertebral constriction of the notochord as effected in Mammalia, the intervertebral parts of the cartilaginous sheath being converted into intervertebral ligaments.

c . notochord ; cs. cuticular sheath of notochord ; s. cartilaginous sheath ; v. vertebral regions ; iv. intervertebral regions ; g, intervertebral joints.

backwards, so as to meet and unite above the spinal cord. The transverse processes of the vertebrae would seem (Pick) to be developed independently of the arches, though they very soon fuse with them. According to Gotte the transverse processes are double in the trunk, there being two pairs, one vertically above the other for each vertebra. The pair on each side eventually fuse together.

In the tail haemal arches are formed, which are similar in their mode of development to the neural arches.

The unconstricted portion of the notochord, which persists in each vertebra, becomes in part converted into cartilage.


556 VKRTKIJRAL COLUMN OF THE AMNIOTA.

Anura. In the Anura the process of formation of the vertebral column is essentially the same as that in the Salamandridte. Two types may however be observed. One of these occurs in the majority of the Anura, and mainly differs from that in Salamandra in (i) the earlier fusion of the arches with the cellular sheath of the notochord ; (2) the more rapid growth of the intervertebral thickenings of the cellular sheath, which results in the early and complete obliteration of the intervertebral parts of the notochord ; (3) the complete division of these intervertebral thickenings into anterior and posterior portions, which unite with and form the articular surfaces of two contiguous vertebras. The vertebrae are moreover proccelous instead of being opisthoccelous.

The unconstricted vertebral sections of the notochord always persist till the ossification of the vertebras has taken place. In some forms they remain through life (Rana), while in other cases they eventually either wholly or partially disappear.

The second type of vertebral development is found in Bombinator, Pseudis, Pipa, and Pelobates. In these genera the formation of the vertebra takes place almost entirely on the dorsal side of the notochord ; so that the latter forms a band on the ventral side of the vertebral column. In other respects the history of the vertebral column is the same in the two cases ; the vertebral unconstricted parts of the notochord appear however to become in part converted into cartilage. The type of formation of the vertebral column in these genera has been distinguished as epichordal in contradistinction to the more normal or perichordal type.

Amniota. In the Amniota all trace of a distinction between a cellular notochord sheath and an arch tissue is lost, and the two are developed together as a continuous whole forming an unsegmented tube round the notochord, with a neural ridge which does not at first nearly invest the neural cord. This tube becomes differentiated, in the manner already described for other types, into (i) vertebral regions with true arches, and (2) intervertebral regions.

Reptilia. In Reptilia (Gegenbaur, No. 416) a cartilaginous tube is formed round the notochord, which is continuous with the cartilaginous neural arches. The latter are placed in the vertebral regions, and in these regions ossification very early sets in, while the notochord remains relatively unconstricted. In the intervertebral regions the cartilage becomes thickened, as in Amphibia, and gradually constricts the notochord. The cartilage in each of the intervertebral regions soon becomes divided into two parts which form the articular faces of two contiguous vertebrae.


NOTOCHORD AND VERTEBRAL COLUMN. 557

The general character of the vertebral column on the completion of these changes is shewn in fig. 320 D. The later changes are relatively unimportant. The constricted intervertebral sections of the notochord rapidly disappear, while the vertebral sections become partially converted into cartilage, and only cease to be distinguishable at a considerably later period.

The ossification extends from the bodies of the vertebrae into the arches and into the articular surfaces, so that the whole vertebrae eventually become ossified.

The Ascalabotae (Geckos) present an exceptional type of vertebral column which has many of the characters of a developmental stage in other Lizards. The body of the vertebra is formed of a slightly hourglassshaped osseous tube, united with adjoining vertebras by a short intervertebral cartilage. There is a persistent and continuous notochord which, owing to the small development of the intervertebral cartilages, is narrower in the vertebral than in the intervertebral regions.

Aves. In Birds the cellular tube formed round the notochord is far thicker than in the Reptilia. It is continuous in the regions of the future vertebrae with neural arches, which do not at first nearly enclose the spinal cord.

On about the fifth day, in the case of the chick, it becomes differentiated into vertebral regions opposite the attachments of the neural arches, and intervertebral regions between them ; the two sets of regions being only distinguished by their histological characters. Very shortly afterwards each intervertebral region becomes segmented into two parts, which respectively attach themselves to the contiguous vertebral regions. A part of each intervertebral region, immediately adjoining the notochord, does not however undergo this division, and afterwards gives rise to the ligamentum suspensorium.

The notochord during these changes at first remains indifferent, but subsequently, on about the seventh day in the chick, a slight constriction of each vertebral region takes place ; so that the vertebrae have temporarily, as they have also in Amphibia, a biconcave form which repeats the permanent condition of most fishes. By the ninth and tenth days, however, this condition has completely disappeared, and in all the intervertebral portions the notochord has become distinctly constricted, and at the same time in each vertebral portion there


558


VERTEBRAL COLUMN OF MAMMALIA.


have also appeared two constrictions of the notochord giving rise to a central and to two terminal enlargements.

On the twelfth day the ossification of the cartilaginous centra commences.

The first vertebra to ossify is the second or third cervical, and the ossification gradually extends to those behind. It does not commence in the arches till somewhat later than in the bodies. For each arch there are two centres of ossification, one on each side.

The notochord persists for the greater part of foetal life and even into post-fcetal life. The larger vertebral portions are often the first completely to vanish. They would seem in many cases at any rate (Gegenbaur) to be converted into cartilage, and so form an integral part of the permanent vertebrae. Rudiments of the intervertebral portions of the notochord may long be detected in the ligamenta suspensoria.

Schwarck (No. 420) states that in both the intervertebral and the vertebral regions, though less conspicuously in the former, the cartilage is divided into two layers, an inner and an outer. He holds that the inner layer corresponds to the cartilaginous notochordal sheath of the lower types, and the outer to the arch tissue. Ossification (Gegenbaur) of the centra appears in a special inner layer of cartilage, which is probably the same as the inner layer of the earlier stage, though this point has not been definitely established.


FIG. 321. LONGITUDINAL SECTION THROUGH THE VERTEBRAL COLUMN OF AN EIGHT WEEKS' HUMAN EMBRYO IN THE THORACIC REGION. (From Kolliker.)

v. cartilaginous vertebral body ; //. intervertebral ligament; ch, notochord.


Mammalia. The early development of the perichordal cartilaginous tube and rudimentary neural arches is almost the same in Mammals as in Birds. The differentiation into vertebral and intervertebral regions is the same in both groups ; but instead of becoming divided as in Reptilia and Birds into two segments attached to two adjoining vertebrae, the intervertebral regions become in Mammals wholly converted into the intervertebral ligaments (fig. 322 /*'). There are three centres of ossifications for each vertebra, two in the arch and one in the centrum.


NOTOCHORD AND VERTEBRAL COLUMN.


559


The fate of the notochord is in important respects different from that in Birds. It is first constricted in the centre of the vertebra (figs. 320 E and 321) and disappears there shortly after the ossification ; while in the intervertebral regions it remains relatively unconstricted (figs. 320 E, 321 and 322 c] and after



FlG. 3-22. LONGITUDINAL SECTION THROUGH THE INTERVERTEBRAL LIGAMENT AND ADJACENT PARTS OF TWO VERTEBRA FROM THE THORACIC REGION OF AN ADVANCED EMBRYO OF A SHEEP. (From Kolliker.)

la. ligamentum longitudinale anterius ; lp. ligamentum long, posterius ; li. ligamentum intervertebrale ; k, k'. epiphysis of vertebra ; w. and iv' '. anterior and posterior vertebrae ; c. intervertebral dilatation of notochord ; c'. and c'. vertebral dilatation of notochord.

undergoing certain histological changes remains through life as part of the nucleus pulposus in the axis of the invertebral ligaments 1 . There is also a slight swelling of the notochord near the two extremities of each vertebra (fig. 322 c' and c"}. In the persistent vertebral constriction of the notochord Mammals retain a more primitive and piscine mode of formation of the vertebral column than the majority either of the Reptilia or Amphibia.

1 This view was first put forward by Lushka, and his surmises have been confirmed by Kolliker and other embryologists. Leboucq (No. 424) however holds that_ the cells of the notochord in the intervertebral regions fuse with those of the adjoining tissue ; and Dursy and others deny that the nucleus pulposus is derived from the notochord.


560 BIBLIOGRAPHY.


BIBLIOGRAPHY of Notochord and Vertebral column.

(415) Cartier. "Beitrage zur Entwicklungsgeschichte der Wirbelsaule." Zeitschrift furwiss. ZooL, Bd. xxv. Suppl. 1875.

(416) C. Gegenbaur. Untersuchungen zur vergleichenden Anatomic der Wirbelsaule der Amphibien nnd Reptilien. Leipzig, 1862.

(417) C. Gegenbaur. " Ueber die Entwickelung der Wirbelsaule des Lepidosteus mil vergleichend anatomischen Bemerkungen." Jenaische Zeitschrift, Bd. in. 1863.

(418) C. Gegenbaur. " Ueb. d. Skeletgewebe d. Cyclostomen." Jenaische Zeitschrift, Vol. v. 1870.

(419) Al. Gotte. "Beitrage zur vergleich. Morphol. des Skeletsystems d. Wirbelthicre. " II. "Die Wirbelsaule u. ihre Anhange." Archiv f. mikr. Anat., Vol. xv. 1878 (Cyclostomen, Ganoiden, Plagiostomen, Chimaera), and Vol. xvi. 1879 (Teleostier).

(420) Hasse und Schwarck. "Studien zur vergleichenden Anatomic der Wirbelsaule u. s. w." Hasse, Anatomische Studien, 1872.

(421) C. Hasse. Das natiirliche System d. Elasmobranchier auf Grundlage d. Bau. u. d. Entwick. ihrer Wirbelsaule. Jena, 1879.

(422) A. Kolliker. " Ueber die Beziehungen der Chorda dorsalis zur Bildung der Wirbel der Selachier und einiger anderen Fische." Verhandlungen der physical, medic in. Gesellschaft in Wiirzburg, Bd. X.

(423) A. Kolliker. " Weitere Beobachtungen iiber die Wirbel der Selachier insbesondere iiber die Wirbel der Lamnoidei." Abhandlungen der senkenbergischen naturforschenden Gesellschaft in Frankfurt, Bd. v.

(424) H. Leboucq. " Recherches s. 1. mode de disparition de la corde dorsale chez les vertebres superieurs." Archives de Biologie, Vol. I. 1 880.

(425) Fr. Leydig. Anatomisch-histologische Untersuchungen iiber Fische nnd Reptilien. Berlin, 1853.

(426) Aug. Miiller. " Beobachtungen zur vergleichenden Anatomic der Wirbelsaule." Miiller's Archiv. 1853.

(427) J. Miiller. " Vergleichende Anatomic der Myxinoiden u. der Cyklostomen mil durchbohrtem Gaumen, I. Osteologie und Myologie." Abhandlungen der koniglichen Akademie der Wissenschaften zu Berlin. 1834.

(428) W. Miiller. "Beobachtungen des pathologischen Instituts zu Jena, I. Ueber den Bau der Chorda dorsalis." Jenaische Zeitschrift, Bd. VI. 1871.

(429) A. Schneider. Beitrage c. vergleich. Anat. u. Entwick. d. Wirbelthicre. Berlin, 1879.


Ribs and Sternum.

Ribs. Embryological evidence on the development of the ribs, though somewhat inadequate, indicates that they arise as cartilaginous bars in the connective tissue of the intermuscular septa, and that they are placed, in Elasmobranchii and


RIBS. 561

Amphibia, on the level of division between the dorso-lateral and ventro-lateral divisions of the muscle-plates. This does not appear to hold true for either Ganoidei or Teleostei. In Teleostei they are entirely below the muscles along the lines of the intermuscular septa, and this is partially true for Ganoidei, though not wholly so in Lepidosteus. They may be attached either to the haemal (Pisces) or neural (Amphibia and Amniota) arches. The connective tissue from which they are formed is continuous with the processes of the vertebrae to which they are attached ; but the conversion of the tissue into cartilage takes place more or less independently of that of the arches, although in many cases the cartilage of the two becomes continuous, the separation of the ribs being then effected by a subsequent process of segmentation (Pick, No. 431). It is possible that the ribs of Pisces may not be homologous with those of Amphibia and the Amniota, but till the reverse can be proved it is more convenient to assume that the ribs are homologous structures throughout the vertebrate series.

In Elasmobranchii the ribs are relatively of less importance in the adult than in the embryo. By a careful examination of their early development, I have satisfied myself that the differentiation of the ribs is independent of that of the haemal processes to which they are attached, although the differentiation proceeds in such a manner that, when both are converted into cartilage, they are quite continuous. Subsequently the ribs become segmented off from the haemal processes. At the junction of the tail and trunk, where the haemal processes commence to be ventrally prolonged, eventually to unite in the region of the tail below the caudal vein, the ribs are attached to short processes which spring from the sides of the haemal arches (fig. 317). The ventral haemal arches of these" fishes are therefore clearly in no part formed by the ribs.

In Ganoidei and Teleostei there is very great difficulty in determining the homologies of the ribs.

In the cartilaginous Ganoidei there are well developed rib-like structures, which might be regarded as homologous with Elasmobranch ribs, and indeed probably are so ; but at the same time their relations are in some respects very different from those of Elasmobranch ribs in the caudal region. In Ganoids the ribs, in approaching the tail, become shorter and then fuse with the ends of the haemal processes, and finally in the caudal region form together with the haemal arches a closed haemal canal which superficially resembles that in Elasmobranchii.

In Lepidosteus and Amia, especially the former, the same phenomenon is still more marked ; and in Lepidosteus it is easy, in passing backwards,

B. III. 36


562 STERNUM.


to trace the ribs bending ventral-wards, and uniting ventrally in the caudal region to form, with the haemal processes, a complete haemal canal.

It might have been anticipated that the Teleostean Ganoids would resemble the Teleostei, but, from an examination of adult Teleostei, it would seem to be clear that the relations of the parts are the same as in Elasmobranchii, i.e. that the ribs have no share in forming the haemal canal in the tail. Aug. Miiller and Gotte have however brought embryological evidence (though not of a conclusive character), to shew that in the embryo the ribs really fuse with the haemal processes in the tail, and so assist, as in the Ganoids, in forming the haemal canal. Gotte moreover holds that the ribs in Elasmobranchii are not homologous with those of Teleostei and Ganoids ; but that the haemal arches in the tail are homologous in the three groups.

Without necessarily following Gotte in these views it is worth pointing out that the undoubtedly close affinity between the bony Ganoids and the Teleostei is in favour of the view on the haemal arches of Teleostei at which he has arrived on embryological grounds.

In Amphibia the formation of the ribs from the connective tissue of the intermuscular septa, their secondary attachment to the transverse processes of the neural arches, and their subsequent separation was first clearly established by Pick (No. 431), whose statements have since been confirmed by Hasse, Born, &c., and in part by Gotte, who holds however that, though converted into cartilage independently of the transverse processes, they are formed in membrane as outgrowths of these processes.

In the Amniota the ribs are also independently established (Hasse and Born), though they subsequently become united to the transverse processes and to the bodies of the vertebrae, or to the transverse processes only. This junction is however stated by the majority of authorities, never to be effected by the fusion of the cartilage of the two parts, but always by fibrous tissue ; though Hoffmann (No. 435) takes a different view on this subject, holding that the ribs are at first continuous with the intervertebral regions of the primitive cartilaginous tube surrounding the notochord.

Sternum. In dealing with the development of the sternum it will be convenient to leave out of consideration the interclavicle or episternum which is, properly speaking, only part of the shoulder-girdle and to confine my statements to the sternum proper.

This structure is found in all the Amniota except the Ophidia, Chelonia, and some of the Amphisbaenae.

From the older researches of Rathke, and from the newer ones of Gotte, etc., it appears that the sternum is always formed from the fusion of the ventral extremities of a certain number of ribs. The extremities of the ribs unite with each other from


STERNUM. 563


before backwards, and thus give rise to two cartilaginous bands. These bands become segmented off from the ribs with which they are at first continuous, and subsequently fuse in the median ventral line to form an unpaired sternum. The Mammalian presternum (manubrium sterni) and xiphosternum have the same origin as the main body of the sternum (Ruge, No. 438).

In the Amphibia there is no structure which admits from its mode of development of a complete comparison with the sternum of the Amniota ; and it must for this reason be considered doubtful whether the median structure placed behind the coracoids in the Anura, which is usually known as the sternum, is really homologous with the sternum of the Amniota 1 .

The remaining Ichthyopsida are undoubtedly not provided with a sternum.

BIBLIOGRAPHY of Ribs and Sternum.

(430) C. Glaus. " Beitrage z. vergleich. Osteol. d. Vertebraten. I. Rippen u. unteres Bogensystem. " Sitz. d. kaiserl. Akad. Wiss. Wien, Vol. LXXIV. 1876.

(431) A. E. Fick. " Zur Entwicklungsgeschichte . d. Rippen und Querfortsatze." Archivf. Anat. und Physiol. 1879.

(432) C. Gegenbaur. "Zur Entwick. d. Wirbelsaule des Lepidosteus mil vergleich. anat. Bemerk." Jenaische Zeit., Vol. III. 1867.

(433) A. Gotte. " Beitrage z. vergleich. Morphol. d. Skeletsystems d. Wirbelthiere Brustbein u. Schultergiirtel." Archivf. mikr. Anat., Vol. xiv. 1877.

(434) C. Hasse u. G. Born. " Bemerkungen lib. d. Morphologic d. Rippen." Zoologischer A nzeiger, 1879.

(4S5) C. K. Hoffmann. "Beitrage z. vergl. Anat. d. Wirbelthiere." Niederland. Archiv Zool., Vol. IV. 1878.

(436) W. K. Parker. " A monograph on the structure and development of the shoulder-girdle and sternum." Ray Soc. 1867.

(437) H. Rathke. Ueb. d. Bau n. d. Entrmcklung d. Brustbeins d. Saurier.

i853 (438) G. Ruge. " Untersuch. lib. Entwick. am Brustbeine d. Menschen.

Morphol. Jahrbuch., Vol. VI. 1880.

1 The so-called sternum of the Amphibia develops in proximity with certain rudimentary abdominal ribs, and Ruge has with some force urged (against Gotte) that it may be for this reason a rudimentary structure of the same nature as the sternum of the higher types.


362


CHAPTER XIX. THE SKULL.

THREE distinct sets of elements may enter into the composition of the skull. These are (i) the cranium proper, composed of true endoskeletal elements originally formed in cartilage, to which are usually added exoskeletal osseous elements, formed in the manner already described p. 542, and known in the higher types as membrane bones. (2) The visceral arches formed primitively as cartilaginous bars, but in the higher types largely supplemented or even replaced by exoskeletal elements. (3) The labial cartilages.

These parts present themselves in the most various forms, and their study constitutes one of the most important departments of vertebrate morphology, and one which has always been a favourite subject of study with anatomists. At the end of the last century and during the first half of the present century the morphology of the skull was handled from the point of view of the adult anatomy by Goethe, Oken, Cuvier, Owen, and many other anatomists, while Duges and, nearer to our own time, Rathke, laid the foundation of an embryological study of its morphology. A new era in the study of the skull was inaugurated by Huxley in his Croonian lecture in 1858, and in his lectures on Comparative Anatomy subsequently delivered before the Royal College of Surgeons. In these lectures Huxley disproved the then widely accepted view that the skull was composed of four vertebrae ; and laid the foundation of a more satisfactory method of dealing with the homologies of its constituent parts. Since then the knowledge of the development of the skull has made great progress. In this country a number


THE SKULL.


565


of very interesting memoirs have been published on the subject by Parker, which together constitute a most striking contribution to our knowledge of the ontogeny of the skull in a series of types ; and in Germany Gegenbaur's monograph on the cephalic skeleton of Elasmobranchii has greatly promoted a scientific appreciation of the nature of the skull.

In the present chapter only the most important features in the development of the skull will be touched on.

It will be convenient to describe, in the first instance, the development of the cartilaginous elements of the skull.

The Cranium. The brain is at first enveloped in a continuous layer of mesoblast known as the membranous cranium, into the base of which the anterior part of the notochord is prolonged for some distance. The primitive cartilaginous cranium is formed by a differentiation within the membranous cranium, and is always composed of the following parts

(fig- 323) :

(1) A pair of cartilaginous plates on each side of the cephalic section of the notochord, known as the parachordals (pa. ck}. These plates together with the notochord (nc) enclosed between them form a floor for the hind- and midbrain. The continuous plate, formed by them and the notochord, is known as the basil ar plate.

(2) A pair of bars forming the floor for the fore-brain,


iff



Cl?


pa.ch.


CIA


FIG. 323. HEAD OK EMBRYO DOGFISH, SECOND STAGE ; BASAL VIEW OF CRANIUM FROM ABOVE, THE CONTENTS HAVING BEEN REMOVED. (From

Parker.)

ol. olfactory sacs ; an. auditory capsule; nc. notochord; py. pituitary body ; pa.ch. parachordal cartilage ; tr. trabecula ; inf. infundibulum ; C.ir. cornua trabeculse ; pn. prenasal element ; sp. spiracular cleft ; br. external branchiae; Cl. 2, 4. visceral clefts.


known as the trabeculae (tr). These bars are continued forward from the parachordals. They meet behind and embrace the front end of the notochord ; and after separating for some distance bend in again in such a way


566


THE PARACHORDALS AND NOTOCHORD.


as to enclose a space the pituitary space. In front of this space they remain in contact and generally unite. They extend forwards into the nasal region (pn}.

(3) The cartilaginous capsules of the sense organs. Of these the auditory (ait) and olfactory capsules (ol} unite more or less intimately with the cranial walls ; while the optic capsules, forming the usually cartilaginous sclerotics, remain distinct.

The parachordals and notochord. The first of these sets of elements, viz. the parachordals and notochord, forming together the basilar plate, is always an unsegmented continuation of the axial tissue of the vertebral column. It forms the floor for that section of the brain which belongs to the primitive postoral part of the head (vide p. 314), and its extension is roughly that of the basioccipital of the adult skull. Its mode of development is almost identical with that of the vertebral column, except that the notochord, even in many forms where it persists in the vertebral column, disappears in the basilar plate ; though in a certain number of cases remnants of it are found in the adult state.


It will be convenient to say a few words notochord in the head. It always extends along the floor of the mid- and hind-brains, but ends immediately behind the infundibulum. The limits of its anterior extension are clearly shewn in fig. 43. The front end of the notochord often becomes more or less ventrally flexed in correspondence with the cranial flexure ; its anterior end being in some instances (Elasmobranchii) almost bent backwards (fig. 324).

Kolliker has shewn that in the Rabbit 1 , and I believe that a more or less similar phenomenon may also be observed in Birds, the anterior end of the notochord is united to the hypoblast of the throat in immediate contiguity with the opening of the pituitary body ; but it is not clear whether this is to be looked upon as the remnant of a primitive attachment of the notochord to the hypoblast, or as a secondary attachment.


here with reference to the nib



FIG. 324. LONGITUDINAL SECTION THROUGH THE BRAIN OF A YOUNG PRISTIURUS EMBRYO.

cer. commencement of the cerebral hemisphere; pn. pineal gland ; ///.infundibulum ; //.ingrowth from mouth to form the pituitary body ; nib. mid-brain ; cb. cerebellum ; ch, notochord; al. alimentary tract; laa. artery of mandibular arch.


" Embryologische Mittheilungen." Festschrift d. Nattirfor. G^//., Halle, 1879.


THE SKULL.


567


Before the parachordals are formed the anterior end of the notochord has usually undergone a partial atrophy ; and its front end often becomes somewhat dorsally flexed. Within the basilar plate it often exhibits two or more dilatations, which have been regarded by Parker and Kolliker as indicative of a segmentation of this plate ; but they hardly appear to me to be capable of this interpretation.

In Elasmobranchs where, as shewn above, a very primitive type of development of the vertebral column is retained, we find that the basilar plate is at first formed of (i) the notochord invested by its cartilaginous sheath, and (2) of lateral masses of cartilage, the parachordals, homologous with the arch tissue of the vertebral column. This development probably indicates that the basilar plate contains in itself the same elements as those from which the neural arches and the centra of the vertebral column are formed ; but that it never passes beyond the unsegmented stage at first characteristic of the vertebral column. The hinder end of each parachordal forms a condyle articulating with the first vertebra ; so that in the cartilaginous skull there are always two occipital condyles. The basilar plate always grows up behind (fig. 326, so], and gives rise to a complete cartilaginous ring enveloping the medulla oblongata, in the same manner that the neural arches envelope the spinal cord. This ring forms an occipital cartilaginous ring ; in front of it the basilar plate becomes laterally continuous with the periotic cartilaginous capsules, and the occipital ring above usually spreads forward to form a roof for the part of the brain between these capsules. In the higher Vertebrates the periotic cartilages may be developed continuously with the basilar plate


The trabeculae. The trabeculae, so far as their mere anatomical relations are concerned, play the same part in forming the floor for the front cerebral vesicle as the parachordals for the mid- and hind-brains. They differ however from the parachordals in one important feature, viz. that, except at their hinder end (fig. 323), they do not embrace between them the notochord.

The notochord constitutes, as we have seen, the primitive axial skeleton of the body, and its absence in the greater part of the region of the trabeculae would probably seem to indicate, as


568


THE TRABECUL^i.


pointed out by Gegenbaur, that these parts, in spite of their similarity to the parachordals, have not the same morphological significance.


C V 1



FlG. 325. VIEW FROM ABOVE OF THE INVESTING MASS AND OF THE TRABECUL/E OF A CHICK ON THE FOURTH DAY OF INCUBATION. (After Parker.)

In order to shew this, the whole of the upper portion of the head has been sliced away. The cartilaginous portions of the skull are marked with the dark horizontal shading.

cv i. cerebral vesicle (sliced oft") ; e. eye ; nc. notochord ; iv. investing mass ; 9. foramen for the exit of the ninth nerve ; d. cochlea ; hsc. horizontal semicircular canal; q. quadrate; 5. notch for the passage of the fifth nerve; Ig. expanded anterior end of the investing mass ; pts. pituitary space ; tr. trabeculse. The reference line tr. has been accidentally made to end a little short of the cartilage.

The nature of the trabeculae has been much disputed by morphologists. The view that they cannot be regarded as the anterior section of the vertebral axis is supported by the consideration that the forward limit of the primitive skeletal axis, as marked by the notochord, coincides exactly with the distinction we have found it necessary to recognise, on entirely independent grounds, between the fore-brain, and the remainder of the nervous axis. But while this distinction between the parachordals and the trabeculas must . I think be admitted, I see no reason against supposing that the trabecuke may be plates developed to support the floor of the fore-brain, for the same physiological reasons that the parachordals have become formed at the sides of the notochord to support the floor of the hind-brain. By some anatomists the trabeculse have been held to be a pair of branchial bars ; but this view has now been generally given up. They have also been regarded as equivalent to a complete pair of neural arches enveloping the front end of the brain. The primitive extension of the base of the fore-brain through the pituitary


THE SKULL.


569


space is an argument, not without force, which has been appealed to in support of this view.

In the majority of the lower forms the trabeculys arise quite independently of the parachordals, though the two sets of elements soon unite ; while in Birds (fig. 325) and Mammals the parachordals and trabeculae are formed as a continuous whole. The junction between the trabeculae and parachordals becomes marked by a cartilaginous ridge known as the posterior clinoid.

The trabeculae are usually somewhat lyre-shaped, meeting in front and behind, and leaving a large pituitary space between their middle parts (figs. 323 and 325). Into this space there


so



f


bbr


cbr


FJG. 326. SIDE VIEW OF THE CARTILAGINOUS CRANIUM OF A FOWL ON THK

SEVENTH DAY OF INCUBATION. (After Parker.)

pn. prenasal cartilage ; aln. alinasal cartilage ; ale. aliethmoid ; immediately below this is the aliseptal cartilage, eth. ethmoid ; pp. pars plana ; ps. presphenoid or interorbital ; pa. palatine ; pg. pterygoid ; z. optic nerve ; as. alisphenoid ; q. quadrate ; st. stapes ; fr. fenestra rotunda ; hso. horizontal semicircular canal ; psc. posterior vertical semicircular canal : both the anterior and the posterior semicircular canals are seen shining through the cartilage, so. supraoccipital ; eo. exoccipital ; oc. occipital condyle ; nc. notochord ; mk. Meckel's cartilage ; ch. ceratohyal ; bh. basi-hyal ; cbr. and ebr. cerato-branchial ; bbr. basibranchial.

primitively projects the whole base of the fore-brain, but the space itself gradually becomes narrowed, till it usually contains only the pituitary body. The carotid arteries always pass through it in the embryo ; but in the higher forms it ceases to be perforated in the adult. The trabeculae soon unite together both in front and behind and form a complete plate underneath the fore-brain, and extending into the nasal region 1 . A special

1 In Man (Kolliker) the trabeculce form from the first a continuous plate in front of the pituitary space, and the latter very early acquires a cartilaginous floor.


5/0 THE TKAHECUL/E.


vertical growth of this plate in the region of the orbit forms the interorbital plate of Teleostei, Lacertilia and Aves (fig. 326, ps), on the upper surface of which the front part of the brain rests. The trabecular floor of the brain does not long remain simple. Its sides grow vertically upwards, forming a lateral wall for the brain, in which in the higher types two regions may be distinguished, viz. an alisphenoidal region (fig. 326, as) behind, growing out from what is known as the basisphenoidal region of the primitive trabeculae, and an orbitosphenoidal region in front growing out from the presphenoidal region of the trabecula,\ These plates form at first a continuous lateral wall of the cranium. At the front end of the brain they are continued inwards, and more or less completely separate the true cranial cavity from the nasal region in front. The region of the cartilage forming the anterior boundary of the cranial cavity is known as the lateral ethmoid region, and it is always perforated for the passage of the olfactory nerves.

The cartilaginous walls which grow up from the trabecular floor of the cranium generally extend upwards so as to form a roof, though almost always an imperfect roof, for the cranial cavity. In the higher types, in Mammals more especially, this roof can hardly be said to be formed at all. The region of the trabeculae in front of the brain is the ethmoid region. The basal part of this region forms an internasal plate, from which an internasal septum may grow up (fig. 326). To its sides the olfactory capsules are attached, and there are usually lateral outgrowths in front forming the trabecular cornua, while from the posterior part of the ethmoidal plate, forming the anterior boundary of the cranial cavity, there often grows out a prefrontal or lateral ethmoidal process.

These and other processes growing out from the trabeculse have occasionally been regarded as rudimentary praeoral branchial arches. I have already stated it as my view that the existence of branchial arches in this region is highly improbable, and I may add that the development of these structures as outgrowths of the skull is in itself to my mind a nearly conclusive argument against their being branchial arches, in that true branchial arches hardly ever or perhaps never arise in this way.

The sense capsules. The most important of these is the auditory capsule, which, as we have seen, fuses intimately with


THE SKULL.


the lateral walls of the skull. In front there is usually a cleft separating it from the alisphenoid region of the skull, through which the third division of the fifth nerve passes out. This cleft becomes narrowed to a small foramen (fig. 327, V). The sclerotic cartilage is always free, but profoundly modifies the region of the cranium near which it is placed. The nasal investment forms in Elasmobranchs (fig. 327, No) a capsule open



FIG. 327. SKULL OF ADULT DOGFISH, SIDE VIEW. (From Parker.) O. C, occipital condyle ; Au. periotic capsule; Pt.O. pterotic ridge ; Sp. 0. sphenotic process ; S. Or. supraorbital ridge ; Na. nasal capsule ; P.N. prenasal cartilage; 77. optic foramen ; V. trigeminal foramen ; PL TV., Qu. pterygo-quadrate arcade ; M.Pt. metapterygoid ligament (including a small cartilage) ; Pl.Tr, ethmo-palatine or palato-trabecular ligament ; Mck. lower jaw ; Sp. spiracle; H.M. hyomandibular; C.Hy, ceratohyal ; m.h.l. mandibulo-hyoid ligament; Ph.Br. pharyngobranchial ; E.Br. epibranchial ; C.br. ceratobranchial ; H.Br. hypobranchial ; B.Br. basibranchial ; Ex.Br. extrabranchial ; l\ 2 , 3 , 4 , 5 . labial cartilages ; the dotted lines within Mck. indicate the basihyal.

below, and continuous with the ethmoid region of the trabeculse. In most types however it becomes more closely united with the ethmoid region and the accessory parts belonging to it.

The cartilaginous cranium, the development of which has been thus briefly traced, persists in the adult without even the addition of membrane bones in the Cyclostomata, Elasmobranchii (fig. 327) and Holocephali. In the Selachioid Ganoids it is also found in the adult, but is covered over by membrane bones. In all other types it is invariably present in the embryo, but becomes in the adult more or less replaced by osseous tissue.


572 THE BRANCHIAL BARS.


Branchial skeleton.

The most primitive type of branchial skeleton in any existing form would appear to be that of the Petromyzonidae, which is developed in a superficial subdermal tissue, and consists of a series of bars united by transverse pieces, so as to form a basketwork. It is known as an extra-branchial system, and an early stage of its development in the Lamprey is shewn in fig. 47. In the higher forms this system is replaced by a series of bars, known as the branchial bars, so situated as to afford support to the successive branchial pouches. Outside these bars there may be present in some primitive forms (Elasmobranchii) cartilaginous elements, which are supposed to be remnants of the extrabranchial system (fig. 327, Ex.Br] ; while a series of membrane bones is also usually added to them, which will be dealt with in a separate section. The branchial bars are developed as simple cartilaginous rods in the deeper parts of the mesoblast which constitutes the primitive branchial arches.

The position of the branchial bars in relation to the somatopleure and splanchnopleure can be determined from their relation to the so-called head cavities. These cavities atrophy before the formation of the cartilaginous branchial bars, but it will be observed (fig. 328), that the artery of each arch (aa) is placed on the inner side of the head cavity (//). The cartilaginous bar arises at a later period on the inner side of the artery, and therefore on the inner side of the section of the body cavity primitively present in the arches.

An anterior arch, known as the mandibular arch, placed in front of the hyo-mandibular cleft, and a second arch, known as the hyoid arch, placed in front of the hyo-branchial cleft, are developed in all types. The succeeding arches are known as the true branchial arches, and are only fully developed in the Ichthyopsida.

In some Sharks (Notidani) seven branchial arches may be present (not including the hyoid and mandibular). In other Ichthyopsida five are usually present, in the embryo at any rate, while in the Amniota there are usually two or three post-hyoid membranous arches, in the interior of which a cartilaginous bar is usually formed. The general form of these bars at an early


THE SKULL.


573




Fir


HORIZONTAL


stage of development is shewn in the dog-fish (Scyllium) in fig. 329.

The simple condition of these bars in the embryo renders it highly probable that forms existed at one time with a simple branchial skeleton of this kind : at the present day however

J SECTION THROUGH THE PEN such forms no longer exist. The first ULTIMATE VISCERAL ARCH arch has in all cases changed its F RUS AN EMHRYO < function and has become converted ^ epiblast; vc. pouch of

into a supporting skeleton for the hypoblast which will form the , , ,11 -1 1 ., i i i. walls of a visceral cleft ; pp.

mouth ; the hyoid arch, though retain- segme nt of body-cavity in vis ing in Some forms its branchial func- ceral arch ;aa. aortic arch.

tion, has in most acquired additional functions and has undergone in consequence various peculiar modifications. The true branchial arches retain their branchial functions in Pisces and some Amphibia, but are secondarily modified and largely aborted in the abranchiate forms. Since the changes undergone

c.a



Bnl


ffm


LrJt


Sn.f


FIG. 329. HEAD OF EMBRYO DOGFISH, n LINES LONG. (From Parker.) TV. trabecula ; Pl.Pt. pterygo-quadrate ; M.Pt. metapterygoid region; Mn. mandibular cartilage ; Hy. hyoid arch; Br. i. first branchial arch; Sp. mandilmlohyoid cleft; C/ 1 . hyo-branchial cleft; Lch. groove below the eye; Net. olfactory rudiment; E. eyeball; An. auditory mass; C i, 2, 3. cerebral vesicles; Hm. hemispheres; f.n.p. nasofrontal process.

by the true branchial bars are far less complicated than those of the hyoid and mandibular bars it will be convenient to treat of them in the first instance.

These bars are, as already mentioned, most numerous in certain very primitive forms (seven in Notidanus), while as we ascend the series there is a gradual tendency for the posterior of them to disappear. This tendency is the result of a gradual atrophy of the posterior branchial pouches, which commenced at


574


THE BRANCHIAL BARS.


a stage in the evolution of the Chordata long prior to the appearance of cartilaginous or osseous branchial bars, and reaches its climax in the Amniota.

In a fully developed branchial bar the primitively simple rod of cartilage becomes divided into a series of segments, usually four, articulated so as to be more or less mobile : and either remaining cartilaginous or becoming partially or wholly ossified. Each bar (fig. 327) forms a somewhat curved structure, embracing the pharynx. The dorsal and somewhat horizontally placed segment is known as the pharyngobranchial (Ph.Br), the next two as the epibranchial (E.Br) and ceratobranchial (C.Br), and the ventral segment as the hypobranchial (H.Br). There is also typically present a basal unpaired segment, uniting the bars of the two sides, known as the basibranchial (B.Br). The arches often bear cartilaginous rays which support the gill lamellae.

In Teleostei dental plates are usually developed as an exoskeletal covering on parts of the branchial arches.

In the Amphibia four or three branchial arches are present in the embryo. These parts are more or less completely retained in the Perennibranchiata and Caducibranchiata, but in the Myctodera and Anura they become largely reduced, and entirely connected with the hyoid.

In the Anura they never reach any considerable development, and are soon reduced to a plate (fig. 330) the coalesced basihyal and basibranchial plate the posterior processes of which represent the remnants of the branchial arches.


According to Parker the posterior process of this plate in the adult is a remnant of the fourth branchial bar ; the next one is the third branchial bar, while the anterior lamina behind the hyoid is stated by him (though this is somewhat doubtful) to be a remnant of the first two bars.

In the Amniota, the branchial arches become still more



Pmx


FIG. 330. YOUNG FROG, WITH TAIL JUST ABSORBED ; SIDE VIEW OF SKULL. (From Parker.)

An. auditory capsule; in front of it is the cranial side wall ; A.N. external nostril ; St. stapes; Mck. Meckelian cartilage; B.Hy. basihyobranchial plate; St.Hy. stylohyal or ceratohyal; Br.i. first branchial arch.

Bones: E-0. exoccipital; Pr.O. prootic ; Pa. parietal ; Fr. frontal ; Na. nasal ; Pmx. premaxillary ; MX. maxillary; Pt. pterygoid; Sq. squamosal; Qn-J't. quadra tojugal; Art. articular; D. dentary.


THE SKULL. 575


degenerated, in correlation with the total disappearance of a branchial respiration at all periods of life. Their remnants become more or less important parts of the hyoid bone, and are solely employed in support of the tongue. Their basal portions are best preserved, forming parts of the body of the hyoid. The posterior (thyroid) cornua of the hyoid are remnants of the true arches. Of these there are two in the Chelonia and Lacertilia, and one in the Aves and Mammalia. In Aves the cornu formed from the first branchial arch (fig. 331, cbr) is always larger than that of the true hyoid arch (cJi).

Mandibular and Hyoid arches. The adaptations of both the mandibular and hyoid bars, to functions entirely distinct from



FlG. 331. VIEW FROM BELOW OF THE BRANCHIAL SKELETON OF THE SKULL

OF A FOWL ON THE FOURTH DAY OF INCUBATION. (After Parker.) cv i. cerebral vesicles ; e. eye ; fn. frontonasal process; n. nasal pit; tr. trabeculre ; pts. pituitary space ; mr. superior maxillary process ; pg. pterygoid ; pa. palatine ; q. quadrate; mk. Meckel's cartilage; ch. cerato-hyal ; bh. basihyal ; cbr. ceratobranchial ; ebr. proximal portion of the cartilage in the third visceral (first branchial) arch; bbr. basibranchial ; i. first visceral cleft; 2. second visceral cleft; 3. third visceral arch.

those which they primitively served, are most remarkable ; and the adaptations of the two bars are in many cases so intimately bound together, that it is not possible to treat them separately.

The most important change of function is undoubtedly that of the mandibular arch, which becomes entirely converted into a skeleton for the jaws. It may be noted as a peculiarity of the


576 MAND1BULAR AND HYOID BARS.

mandibular arch that it is never provided with an unpaired basal element.

The simplest forms of metamorphosis are those undergone by Elasmobranchii, of which the Dog-fish (Scyllium) and Skate (Raja) have been studied (Parker, No. 456). In some of these forms, e.g. the Skate, part of the mandibular bar is still related to the hyo-mandibular cleft (the spiracle).

Elasmobranchii. In Scyllium the hyoid and mandibular arches are at first very similar to those which follow. Soon however each of them sends an anteriorly directed dorsal process (fig. 329). The regions which may be distinguished owing to the growth of these processes have received names from ossifications in them which are found in other types. The anterior process of the mandibular arch is known as the pterygo-quadrate bar (Pl.Pt) ; the dorsal end of the primitive bar from which it starts (M.Pt] is known as the metapterygoid process; while the ventral end of the bar forms the Meckelian cartilage. The upper end of the hyoid arch is known as the hyomandibular.

In a somewhat later stage changes take place which cause these parts practically to assume the adult form (fig. 327). The mandibular arch becomes segmented at its bend into (i) a pterygo-quadrate bar (Pl.Pf) which grows forwards in front of the mouth, and forms an upper jaw, and (2) a Meckelian cartilage (Mck} which is placed behind the mouth, and forms a lower jaw. The two jaws are articulated together, and the cartilages of the two sides composing them meet each other distally.

At the articulation of the Meckelian cartilage with the quadrate part of the pterygo-quadrate is situated a ligament (M.Pf), which takes the place of the metapterygoid process of the previous stage, and passes up on the anterior side of the spiracle, to be attached to the cranium in the front part of the auditory region. This ligament, which is supplemented by a second ligament, the ethmopalatine ligament, passing from the pterygo-quadrate bar to the antorbital region of the skull, is not the most important support of the jaw. The main support is, on the contrary, given by the hyoid arch ; the hyomandibular segment of which (H.M) as well as the adjoining segment (ceratohyoid C.Hy) are firmly attached by ligament to the mandibular


THE SKULL.


577


arch. The hyomandibular is articulated with the cranium beneath the pterotic ridge (Pt.O),

In the type just described, the hyoid and mandibular arches undergo less modification than in almost any other case. The hyoid arch has altered its form, but retains its respiratory function. It has however acquired the secondary function of supporting the mandibular arch. The mandibular arch is divided into two elements, which form respectively the upper and lower jaws. It is not directly articulated with the skull, and its mode of support by the hyoid arch has been called by Huxley (No. 445) hyostylic.

The development of the hyoid and mandibular arches in the Skate is characterised by a few important features (fig. 333). The anterior element of the hyoid

arch, which forms the hyo- \ ^ Sp

mandibular (H.M], becomes entirely separate from the posterior part of the arch, and only serves to support the jaws. The posterior part of the arch (Hy} carries on the respiratory functions of the hyoid, and is closely connected with the first branchial arch. The upper or metapterygoidelementof the mandibular arch (M.Pt} has a considerable development,



FIG. 333. HEAD OF EMBRYO SKATE, i\ IN. LONG. (From Parker.)

Tr. trabecula ; Pl.Pt. pterygo- quadrate bar ; Mn. mandibular bar ; M.Pt. metapterygoid cartilage ; H.M. hyomandibular ; Hy. remainder of hyoid arch ; Br. \. first branchial arch ; Sp. mandibulo-hyoid cleft or spiracle ; Pn. pineal gland ; Au. au ditory vesicle ; C. i, C. 2, and C. 3. vesicles of the brain.


and, becoming separated from the remainder of the arch, forms a mass of cartilage with one or two branchial rays, in the front wall of the spiracle, and constitutes a section of the mandibular arch still retaining traces of its primitive function in supporting the wall of a branchial pouch.

Although the development of other Elasmobranch types is not known, it is necessary to call attention to the mode of support of the mandibular arch in certain forms, notably Notidanus, Hexanchus and Cestracion, where the pterygo-quadrate region of the mandibular arch is directly articulated to the B. in. 37


578 MANDIKULAR AND HYOID BARS.

cranium between the optic and trigeminal foramina. In the two former genera the metapterygoid region of the arch is moreover continuous with the pterygo-quadrate, and articulates with the post-orbital process of the auditory region of the skull. In spite of these attachments the mandibular arch continues to be partially supported by the hyomandibular. The skulls in which the mandibular arch has this double form of support have been called by Huxley amphistylic.

Considering the in many respects primitive characters of the forms with amphistylic skulls it seems not improbable that they


SOr


l } a.ch.



Gtly


FIG. 334. CRANIAL SKELETON OF A SALMON FRY, SECOND WEEK AFTER HATCHING; MEMBRANE BONES, EYEBALLS, AND NASAL SACS REMOVED. (From Parker.)

T.Cr. tegrnen cranii; 'S. Or. supraorbital band; Fo. superior fontanelle; Au. auditory capsule ; Pa.ch. parachordal cartilage; Ch. notochord; 7>. trabecula; above the trabecula, the interorbital septum is seen, passing into the cranial wall above and reaching the supraorbital band; //. optic foramen; V. trigeminal foramen; /', I". labial cartilages ; PI. Ft. palatopterygoid bar ; M. Pt. metapterygoid tract ; Qu. quadrate region; Mck. Meckelian cartilage; H.M. hyomandibular cartilage; Sy. symplectic tract; I.Hy. interhyal; C.Hy. ceratohyal; II. fly. hypohyal; G.ffy. glossohyal; Br.\. first branchial arch.

preserve the original mode of support of the mandibular arch ; from which differentiations in two directions have taken place, viz. differentiations in the direction of a complete support of the mandibular arch by the hyoid, which is characteristic of most Elasmobranchii and, as will be shewn below, of Ganoidei and Tclcostei ; and differentiations towards a direct articulation or attachment of the mandibular arch to the cranium, without the


THE SKULL. 579


intervention of the hyoid. The latter mode of attachment is called by Huxley autostylic. It is found in Holocephala, Dipnoi, Amphibia and the Amniota.

Teleostei. In addition to that of Elasmobranchii, the skull of the Salmon is the only hyostylic skull in which, by the admirable investigation of Parker (No. 451), the ontogeny of the hyoid and mandibular bars has been satisfactorily worked out. Apart from the presence of a series of membrane bones, the development of these bars agrees on the whole with the types already described.

The hyoid arch, though largely ossified, undergoes a process of development very similar to that in Raja. It is formed as a simple cartilaginous bar, which soon becomes segmented longi ft 1.3 Sp.



FIG. 335. YOUNG SALMON OF THE FIRST SUMMER, AKOUT 2 INCHES LONG;

SIDE VIEW OF SKULL, EXCLUDING BRANCHIAL ARCHES. (From Parker.)

The palato-mandibular and hyoid tracts are detached from their proper situations,

a line indicating the position where the hyomandibular is articulated beneath the

pterotic ridge.

oL olfactory fossa; c.tr. trabecular cornu; /*. /. upper labial cartilages ; p.s.

presphenoid tract ; t.cr. tegmen cranii ; s.o.b. supraorbital band; fo. superior fonta nelle; n.c. notochord; b.o. basilar cartilage; //'. trabecula; p.c. condyle for palatine

cartilage; 5. trigeminal foramen ; fa. facial foramen; 8. foramen for glossopharyngeal

and vagus nerves; mk. Meckelian cartilage; op.c. opercular condyle.

Bones: e.o. exoccipital; s.o. supraoccipital; e.p. epiotic; pt.o. pterotic; sp.o.

sphenotic ; op. opisthotic; pro. prootic; I'.s. basisphenoid ; al.s. alisphenoid; o.s.

orbitosphenoid ; I.e. ectethmoid or lateral ethmoid ; pa. palatine ; pg. pterygoid ;

m.pg. mesopterygoid ; mt.pg. metapterygoid ; qu. quadrate; ar. articular; h.m.

hyomandibular; sy. symplectic ; i.h. interhyal ; ep.h. epiceratohyal ; c.h. ceratohyal ;

h.h. hypohyal; g.h. glosso- or basihyal.

372


580 MANDIBULAR AND HYOID BARS.

tudinally into an anterior and a posterior part (fig. 334). The former constitutes the hyomandibular (H.M], while the latter, becoming more and more separated from the hyomandibular, constitutes the hyoid arch proper ; owing to the disappearance of the hyobranchial cleft, it loses its primitive function, and serves on the one hand to support the operculum covering the gills, and on the other to support the tongue. It becomes segmented into a series of parts which are ossified (fig. 335) as the epiceratohyal (ep./t) above, then a large ceratohyal (c/t), followed by a hypohyal (JiJi), while the median ventral element forms the basi- or glossohyal (gJi).

The hyomandibular itself is articulated with the skull below the pterotic process (fig. 334, H.M}. Its upper element ossifies as the hyomandibular (fig. 335, fun.}, while its lower part (fig. 334, Sy), which is firmly connected with the mandibular arch, ossifies as the symplectic (fig. 335, sy). A connecting element between the two parts of the hyoid bar forms an interhyal (i/i).

There are more important differences in the development of the mandibular arch in Elasmobranchii and the Salmon than in that of the hyoid arch, in that, instead of the whole arcade of the upper jaw being formed from the mandibular arch, a fresh element, in the form of an independently developed bar of cartilage, completes the upper arcade in front ; but even with this bar the two halves of the upper branch of the arch do not meet anteriorly, but are separated by the ends of the trabeculae.

The anterior bar of the upper arcade is known as the palatine ; but it appears to me as yet uncertain how far it is to be regarded as an element, primitively belonging to the upper arcade of the mandibular arch, which has become secondarily independent in its development ; or as an entirely distinct structure which has no counterpart in the Elasmobranch upper jaw. The latter view is adopted by Parker and Bridge, and a cartilage attached to the hinder wall of the nasal capsule of many Elasmobranchii is identified by them with the palatine rod of the Teleostei.

The arch itself is at first very similar to the succeeding arches ; its dorsal extremity soon however becomes broadened, and provided with an anteriorly directed process. This part (fig. 334, M.Pt and Qii] is then segmented from the lower region,


THE SKULL. 581


and forms what may be called the pterygo-quadrate cartilage, though not completely homologous with the similarly named cartilage in Elasmobranchs ; while the lower region forms the Meckelian cartilage (Mck], which has already grown inwards, so as to meet its fellow ventrally below the mouth. The whole arch becomes at the same time widely separated from the axial parts of the skull.

Nearly simultaneously with the first differentiation of the mandibular arch, a bar of cartilage the palatine bar already spoken of is formed on each side, below the eye, in front of the mouth. The dilated anterior extremity of this bar soon comes in contact with an anterior process of the trabeculse, known as the ethmopalatine process.

In a later stage the pterygoid end of the pterygo-quadrate cartilage unites with the distal end of the palatine bar (fig. 334, Pl.Pt], and there is then formed a continuous cartilaginous arcade for the upper jaw, which is strikingly similar to the cartilaginous upper jaw of Elasmobranchii.

A large dorsal process of the primitive pterygo-quadrate now forms a large metapterygoid tract (M.Pt] ; while the whole arch becomes firmly bound to the hyomandibular (H.M}.

In the later stages the parts formed in cartilage become ossified (fig. 335). The palatine is first ossified, the pterygoid region of the pterygo-quadrate is next ossified as a dorsal mesopterygoid (m.pg] and a ventral pterygoid proper (pg). The quadrate region, articulating with the Meckelian cartilage, becomes ossified as a distinct quadrate (qu\ while the dorsal region becomes also ossified as a metapterygoid (int.pg).

In the Meckelian cartilage a superficial ossification of the ventral edge and inner surface forms an articulare (ar) ; but the greater part of the cartilage persists through life.

Some of the above ossifications, at any rate those of the palatine and pterygoid, seem to be started by dental osseous plates adjoining the cartilage. They will be spoken of further in the section dealing with the membrane bones.

Amphibia. The development of the autostylic piscine skulls has unfortunately not yet been studied ; and the most primitive autostylic types whose development we are acquainted with are


582 MANDIBULAR AND HYOID BARS.

those of the Amphibia ; on which a large amount of light has been shed by the researches of Huxley and Parker.

The modifications of the hyoid arch are comparatively simple and uniform. It forms a rod of cartilage, which soon articulates in front with the quadrate element of the mandibular arch, and is subsequently attached by ligaments both to the quadrate and to the cranium. In those Amphibia in which external gills and gill clefts are lost, it fuses with the basal element of the hyoid (fig. 330), which, together with the basal portions of the following arches, forms a continuous cartilaginous plate. On the completion of these changes the paired parts of the hyoid arch have the form of two elongated rods, known as the anterior cornua of the hyoid, which attach the basihyal plate to the cranium behind the auditory capsule.

It is still uncertain whether there is any distinct element corresponding to the hyomandibular of fishes.

Parker holds that the columella auris of the Anura is the homologue of the hyomandibular. The columella develops comparatively late and independently of the remainder of the hyoid arch, but the similarity between its relations to the nerves and those of the hyomandibular is put forward by Parker as an argument in favour of his view. The early ligamentous connection between the quadrate and the upper end of the primitive hyoid is however an argument in favour of regarding the upper end of the primitive hyoid as the hyomandibular element, not separated from the remainder of the arch.

The history of the mandibular arch is more complicated than that of the hyoid. The part of it which corresponds with the upper jaw of Elasmobranchii exhibits most striking variations in development ; so striking indeed as to suggest that the secondary modifications it has undergone are sufficiently considerable to render great caution necessary in drawing morphological conclusions from the processes which are in some instances observable. A more satisfactory judgment on this point will be . possible after the publication of a memoir with which Parker is now engaged on the skulls of the different Anura.

The membrane bones applying themselves to the sides of the mandibular arch are relatively far more important than in the lower types. This is especially the case with the upper jaw where the maxillary and premaxillary bones functionally replace the primitive cartilaginous jaw ; while membranous pterygoids


THE SKULL.


583


and palatines apply themselves to, and largely take the place of, the cartilaginous palatine and pterygoid bars.

Two types worked out by Parker, viz. the Axolotl and the common Frog, may be selected to illustrate the development of the mandibular arch.

In the Axolotl, which may be taken as the type for the Urodela, the mandibular arch is constituted at a very early stage of (i) an enlarged dorsal element, corresponding with the pterygo-quadrate of the lower types, but usually known as the quadrate ; and (2) a ventral or Meckelian element. The Meckelian bar very early acquires its investing bones, while the dorsal part of the quadrate becomes divided into two characteristic



FIG. 336. YOUNG AXOLOTL, i\ INCHES LONG ; UNDER VIEW OF SKULL,

DISSECTED, THE LOWER JAW AND GILL ARCHES HAVING BEEN REMOVED.

(From Parker.)

nc. notochord ; oc.c. occipital condyle; f.o. fenestra ovalis; si. stapes; tr. trabecular cartilage; i.n. internal nares; c.tr. cornu trabeculse; pd. pedicle of quadrate; (/. quadrate; pg. outline of pterygoid cartilage; 5'. orbito-nasal nerve; 7. facial nerve.

BonCS I pa.s. parasphenoid ; e.o. exoccipital ; v. vomer; px. premaxillary ; mx. maxillary; pa. palatine; pg. pterygoid.

processes, viz. an anterior dorsal process which grows towards and soon permanently fuses with the trabecular crest, and a posterior process known as the otic process, which applies itself to the outer side of the auditory region. The anterior of these processes, as pointed out by Huxley, is probably homologous with the anterior process of the pterygo-quadrate bar in Notidanus, which articulates with the trabecular region of the cranium, while the otic process is homologous with the meta


584 MANDIBULAR AND HYOID BARS.

pterygoid process. Hardly any trace is present of an anterior process to form a pterygoid bar, but dentigerous plates forming a dermal palato-pterygoid bar have already appeared.

At a somewhat later stage a fresh process, called by Huxley the pedicle, grows out from the quadrate, and articulates with the ventral side of the auditory region (fig. 336, pd). Shortly afterwards a rod of cartilage grows forward from the quadrate under the membranous pterygoid (pg), which corresponds with the cartilaginous pterygoid bar of other types (fig. 336), and an independent palatine bar, arising even before the pterygoid process, is formed immediately dorsal to the dentigerous palatine plate (pa\ and is attached to the trabecula. These two bars eventually meet, but never become firmly united to the more important membrane bones placed superficially to them.

The mandibular arch in the Frog stands, so far as development is concerned, in striking contrast to the mandibular arch of the Axolotl, in spite of the obvious similarity in the arrangement of the adult parts in the two types. FlG . 33? . EMBRYO FROG, JUST BE In the earliest stage it FORE HATCHING ; SIDE VIEW OF HEAD,

WITH SKIN REMOVED. (From Parker.) forms a simple bar in the ,, lf , , - . , .. ,

Na. olfactory sack; E. involution for

membranous mandibular arch, eyeball; Ati. auditory sack; 7>. trabe11 i , .1 cula; Mn. mandibular : Hy. hyoid ; Br.I.

parallel to and very similar to first branchial arch . ' th / gili.buds are



are

the hyoid bar behind (figf 337, seen on the first two branchial arches; /. M \ T u, * u labial cartilages.

Mn). In the next stage ob served, that is to say in Tadpoles of four, five, to six lines long, an astonishing transformation has taken place. The mandibular arch (fig. 338) is turned directly forwards parallel to the trabecula, to which it is attached in front (p.pg) and behind (pd}. The proximal part of the arch thus forms a subocular bar, and the space between it and the trabecula a subocular fenestra. In front of the anterior attachment it is continued forwards for a short distance, and to the free end of this projecting part is articulated a small Meckelian cartilage directed upwards (mk}. The Meckelian cartilage is at this stage placed in front of the nasal sacks, in the lower lip of the suctorial


THE SKULL.


585


mouth. The greater part of the arch, parallel with the trabeculae, is equivalent to what has been called in the Axolotl the


mJr



FIG. 338. TADPOLE OF COMMON TOAD, ONE-THIRD OF AN INCH LONG ; CRANIAL AND MANDIBULAR CARTILAGES SEEN FROM ABOVE ; THE PARACHORDAL

CARTILAGES ARE NOT YET DEFINITE. (From Parker.)

nc. notochord; ms. muscular segments; au. auditory capsule; py. region of pituitary body; tr. trabecula; c.tr, cornu trabeculae ; p-pg. palatopterygoid bar ; pd. pedicle; q. quadrate condyle; mk. Meckelian piece of mandibular arch; s.o.f. subocular fenestra ; u.l. upper labial cartilage. The dotted circle within the quadrate region indicates the position of the internal nostril.

quadrate, while its anterior attachment to the trabeculae is the rudiment of the palato-pterygoid cartilage. The posterior attachment is known as the pedicle.

The condition of the mandibular arch during this and the next stage (fig. 339) is very perplexing. Its structure appears adapted in some way to support the suctorial mouth of the Tadpole.

Reasons have been offered in a previous part of this volume for supposing that the suctorial mouth of the Tadpole is probably not simply a structure secondarily acquired by this larva, but is an organ inherited from an ancestor provided through life with a suctorial mouth.

The question thus arises, is the peculiar modification of the mandibular arch of the Tadpole an inherited or an acquired feature ?

If the first alternative is accepted we should have to admit that the mandibular arch became first of all modified in connection with the suctorial mouth, before it was converted into the jaws of the Gnathostomata ; and that the peculiar history of this arch in the Tadpole is a more or less true record of its phylogenetic development. In favour of this


586


MANDIBULAR AND HYOID BARS.


view is the striking similarity which Huxley has pointed out between the oral skeleton of the Lamprey and that of the Tadpole ; and certain peculiarities of the mandibular arch of Chimaera and the Dipnoi can perhaps best be explained on the supposition that the oral skeleton of these forms has arisen in a manner somewhat similar to that in the Frog ; though with reference to this point further developmental data are much required.

On the other hand the above suppositions would necessitate our admitting that a great abbreviation has occurred in the development of the mandibular arch of the otherwise more primitive Urodela ; and that the simple mode of growth of the jaws in Elasmobranchii, from the primitive mandibular arch, is phylogenetically a much abbreviated and modified process, instead of being, as usually supposed, a true record of ancestral history.

If the view is accepted that the characters of the mandibular arch of the Tadpole are secondary, it will be necessary to admit that the adaptation of the mandibular arch to the suctorial mouth took place after the suctorial mouth had come to be merely a larval organ.

In view of our imperfect knowledge of the development of most Piscine skulls I would refrain from expressing a decided opinion in favour of either of these alternatives.


or.p


eth



FIG. 339. TADPOLE WITH TAIL BEGINNING TO SHRINK; SIDE VIEW OF SKULL

WITHOUT THE BRANCHIAL ARCHES. (From Parker.)

n.c. notochord; au. auditory capsule; between it and eth. the low cranial side wall is seen; eth. ethmoidal region; st. stapes; 5. trigeminal foramen; 2. optic foramen; ol. olfactory capsules, both seen owing to slight tilting of the skull; c.tr. cornu trabeculae; ./. upper labial, in outline; su. suspensorium (quadrate); pd. its pedicle; ot.fr. its otic process; or.p. its orbitar process; t.m. temporal muscle, indicated by dotted lines passing beneath the orbitar process; pa.pg. palatopterygoid bar; ;;//. Meckelian cartilage; /./. lower labial, in outline; c.h. ceratohyal; b.h. basihyal. The upper outline of the head is shewn by dotted lines.

As the tail of the Tadpole gradually disappears, and the metamorphosis into the Frog becomes accomplished, the mandibular arch undergoes important changes (fig. 339): the


THE SKULL.


palato-pterygoid attachment (pa.pg) of the quadrate subocular bar becomes gradually elongated ; and, as it is so, the front end of the subocular bar (su) rotates outwards and backwards, and soon forms a very considerable angle with the trabeculae. The Meckelian cartilage (ink) at its free end becomes at the same time considerably elongated. These processes of growth continue till (fig. 330) the palato-pterygoid bar (Pf) forms a subocular bar, and is considerably longer than the original subocular region of the quadrate ; while the Meckelian cartilage (Mck] has assumed its permanent position on the hinder border of the no longer suctorial mouth, and has grown forwards so as nearly to meet its fellow in the median line.

The metapterygoid region of the quadrate gives rise to a posterior and dorsal process (fig. 339, ot.pr), the end of which is constricted off as the tympanic annulus (fig. 340, a.f) ; while


pmx



FIG. 340. YOUNG FROG, NEAR END OF FIRST SUMMER ; UPPER VIEW OF SKULL, WITH LEFT MANDIBLE REMOVED, AND THE RIGHT EXTENDED OUTWARDS. (From Parker.)

b.o. basioccipital tract; s.o. supraoccipital tract; fo. frontal fontanelle; e.n, external nostril; internal to it, internasal plate; a.t. tympanic annulus.

Bones : e.o. exoccipital; pr.o. prootic, partly overlapped by/, parietal; f. frontal ; eth. rudiment of sphenethmoid ; na. nasal ; pmx. premaxillary ; mx. maxillary; /-. pterygoid, partly ensheathing the reduced cartilage; q.j. quadratojugal ; s<j. squamosal; ar. articular; d. dentary; m.mk. mento-Meckelian.

the proximal part of the process remains as the otic (metapterygoid) process, articulating with the auditory cartilage.

The pedicle (pd} retains its original attachment to the skull.


588 MAND1BULAR AND IIYOID BARS.

The palato-pterygoid soon becomes segmented into a transversely placed palatine, and a longitudinally placed pterygoid (fig. 340). With the exception of a few ossifications, which present no features of special interest, the parts of the mandibular arch have now reached their final condition, which is not very different from that in the Axolotl.

Sauropsida. In the Sauropsida the modifications of the hyoid and mandibular arches are fairly uniform.

The lower part of the hyoid arch, including the basihyoid, unites with the remnants of the arches behind to form the hyoid bone, to which it contributes the anterior cornu and anterior part of the body.

The columella is believed by Huxley and Parker to represent, as in the Anura, the independently developed dorsal (hyomandibular) element of the hyoid, together with the stapes with which it has become united 1 .

The membranous mandibular arch gives off in the embryos of all the Sauropsida an obvious bud to form the superior maxillary process, and the formation of this bud appears to represent the growth forwards of the pterygoid process in Elasmobranchii, which is indeed accompanied by the formation of a similar bud ; but the skeletal rod, which appears in the axis of this bud, is as a rule independent of that in the true arch (fig- SS 1 ./^. PS}- The former is the pterygo-palatine bar; the latter the Meckelian and quadrate cartilages.

The pterygo-palatine bar is usually if not always ossified directly, without the intervention of cartilage.

Born has recently shewn that Parker was mistaken in supposing that the palato-pterygoid bone is cartilaginous in Birds. In the Turtle a short cartilaginous pterygoid process of the quadrate would seem to be present (Parker, No. 458).

The quadrate and Meckelian cartilages are either from the first separate, or very early become so.

1 The strongest evidence in favour of Huxley's and Parker's view of the nature of the columella is the fusion in the adult Sphenodon of the upper end of the hyoid with the columella (vide Huxley, No. 445). From an examination of a specimen in the Cambridge museum I do not feel satisfied that the fusion is not secondary, but have not been able to examine the junction of the hyoid and columella in section. For a different view to that of Huxley vide Peters, "Ueb. d. Gehorknochelchen u. ihr Verhaltniss zu. Zungenbeinbogen b. Sphenodon." Berlin MoHOtsbtnekU, 1874.


THE SKULL.


589


The quadrate cartilage ossifies as the quadrate bone, and supplies the permanent articulation for the lower jaw. Its upper end exhibits a tendency to divide into two processes, corresponding with the pedicle and otic processes of the Amphibia. The Meckelian cartilage becomes soon covered by investing bones, and its proximal end ossifies as the articulare. The remainder of the cartilage usually disappears.

Mammalia. The most extraordinary metamorphosis of the hyoid and mandibular arches occurs in the Mammalia, and has been in part known since the publication of the memoir of Reichert (No. 461).

Both the hyoid and mandibular arches develop at first more completely than in any of the other types above Fishes; and are



pn.ch nc


FIG. 341. EMBRYO PIG, TWO-THIRDS OF AN INCH LONG ; ELEMENTS OF THE

SKULL SEEN SOMEWHAT DIAGRAMMATICALLY FROM BELOW. (From Parker.) pa.ch. parachordal cartilage; nc. notochorcl; au. auditory capsule; py. pituitary body; tr. trabeculse; c.lr. trabecular cornu; pn. prenasal cartilage; e.n. external nasal opening; ol. nasal capsule; p-pg- palatopterygoid tract enclosed in the maxillopalatine process; mn. mandibular arch ; hy. hyoid arch; th.h. first branchial arch; ja. facial nerve; 8a. glossopharyngeal ; 86. vagus; 9. hypoglossal.

articulated to each other above, while the pterygo-palatine bar is quite distinct. The main features of the subsequent development are undisputed, with the exception of that of the upper end of the hyoid, which is still controverted. The following is Parker's (No. 452) account for the Pig, which confirms in the main the view originally put forward by Huxley (No. 445).

The mandibular and hyoid arches are at first very similar


5QO MANDIBULAR AND HYOID BARS.

(fig. 341 mn and hy), their dorsal ends being somewhat incurved, and articulating together.

In a somewhat later stage (fig. 342) the upper end of the mandibular bar (mb\ without becoming segmented from the ventral part, becomes distinctly swollen, and clearly corresponds to the quadrate region of other types. The ventral part of the bar constitutes the Meckelian cartilage (mk).

The hyoid arch has in the meantime become segmented into two parts, an upper part (z), which eventually becomes one of



FIG. 342. EMBRYO PIG, AN INCH AND A THIRD LONG; SIDE VIEW OF MANDIBULAR AND HYOID ARCHES. THE MAIN HYOID ARCH IS SEEN AS DISPLACED BACKWARDS AFTER SEGMENTATION FROM THE INCUS. (From Parker.)

tg. tongue; ink. Meckelian cartilage; ml. body of malleus; mb. manubrium or handle of the malleus; t.ty. tegmen tympani; i. incus; st. stapes; i.hy, interhyal ligament; st.h. stylohyal cartilage; h.h. hypohyal ; ^.//.basibranchial; th.h. rudiment of first branchial arch; -ja. facial nerve.

the small bones of the ear the incus and a lower part which remains permanently as the anterior cornu of the hyoid (st./i). The two parts continue to be connected by a ligament.

The incus is articulated with the quadrate end of the mandibular arch, and its rounded head comes in contact with the stapes (fig. 342, st) which is segmented from the fenestra ovalis. The main arch of the hyoid becomes divided into a hypohyal (h.h) below and a stylohyal (st. h] above, and also becomes articulated with the basal element of the arch behind (b/i).

In the course of further development the Meckelian part of the mandibular arch becomes enveloped in a superficial ossification forming the dentary. Its upper end, adjoining the quadrate region, becomes calcified and then absorbed, and its lower, with the exception of the extreme point, is ossified and subsequently incorporated in the dentary.

The quadrate region remains relatively stationary in growth


TIIK SKULL. 591


as compared with the adjacent parts of the skull, and finally ossifies to form the malleus bone of the ear. The processus gracilis of the malleus is the primitive continuation into Meckel's cartilage.

The malleus and incus are at first embedded in the connective tissue adjoining the tympanic cavity (hyomandibular cleft, vide p. 528) ; and externally to them a bone known as the tympanic bone becomes developed so that they become placed between the tympanic bone and the periotic capsule. In late fcetal life they become transported completely within the tympanic cavity, though covered by a reflection of the tympanic mucous membrane.

The dorsal end of the part of the hyoid separated from the incus becomes ossified as the tympano-hyal, and is anchylosed with the adjacent parts of the periotic capsule. The middle part of the bar just outside the skull forms the stylo-hyal (styloid process in Man) which is attached by ligament to the anterior cornu of the hyoid (cerato-hyal).

While the account of the formation of the malleus, incus, and stapes just given is that usually accepted in this country, a somewhat different view of the development of these parts has as a rule been adopted in Germany. Reichert (No. 461) held that both the malleus and the incus were derived from the mandibular bar ; and this view has been confirmed by Giinther, Kolliker and other observers, and has recently been adopted by Salensky (No. 462) after a careful research especially directed towards this point. Reichert also held that the stapes was derived from the hyoid bar ; but, though his observations on this point have been very widely accepted, they have not met with such universal recognition as his views on the origin of the malleus and incus. Salensky has recently arrived at a view, which is in accord with that of Parker, in so far as the independence of the stapes of both the hyoid and mandibular arches is concerned. Salensky however holds that it is formed from a mass of mesoblast surrounding the artery of the mandibular arch, and that the form of the stapes is due to its perforation by the mandibular artery. A product of this artery permanently perforates the stapes in a few Mammalia, though in the majority it atrophies.

In view of the different accounts of the origin of the incus the exact nature of this bone must still be considered as an open question, but should Reichert's view be confirmed the identification of the incus with the columella of the Amphibia and Sauropsida must be abandoned.


592 MEMBRANE BONES.


Membrane bones and ossifications of the cranium.

The membrane bones of the skull may be divided into two classes, viz. (i) those derived from dermal osseous plates, which as explained above (p. 542) are primitively formed by the coalescence of the osseous plates of scales ; and (2) those formed by the coalescence of the osseous plates of teeth lining the oral cavity. Some of the bones sheathing the edge of the mouth have been formed partly by the one process and partly by the other.

In the Fishes there are found all grades of transition between simple dermal scutes, and true subdermal osseous plates forming an integral part of the internal skeleton. Dermal scutes are best represented in Acipenser and some Siluroid Fishes.

Where the membrane bones still retain the character of dermal plates, those on the dorsal surface of the cranium are usually arranged in a series of longitudinal rows, continuing in the region of the head the rows of dermal scutes of the trunk ; while the remaining cranial scutes are connected with the visceral arches. The dermal bones on the dorsal surface of the head are very different in number, size, and arrangement in different types of Fishes ; but owing to their linear disposition it is usually possible to find a certain number both of the paired and unpaired bones which have a similar situation in the different forms. These usually receive the same names, but both from general considerations as to their origin, as well as from a comparison of different species, it appears to me probable that there is no real homology between these bones in different species, but only a kind of general correspondence 1 .

It is not in fact till we get to the types above the Fishes that we can find a series of homologous dorsal membrane bones covering the roof of the skull. In these types three paired sets of such bones are usually present, viz, from behind forwards the parietals, frontals and nasals, the latter bounding the posterior surface of the external nasal opening. Even in the higher

1 For some interesting remarks on the arrangement of these bones in Fishes, vide Bridge, "On the Osteology of Polyodon folium." Phil. Trans., 1878.


THE SKULL. 593


types these bones are liable to vary very greatly from the usual arrangement.

Besides these bones there is usually present in the higher forms a lacrymal bone on the anterior margin of the orbit derived from one of a series of periorbital membrane bones frequently found in Fishes. Various supraorbital and postorbital bones, etc. are also frequently found in Lacertilia, etc. which are not impossibly phylogenetically independent of the membrane bones inherited from Fishes; and may have been evolved as bony scutes in the subdermal tissue of the papillae of the sauropsidan scales.

The visceral arches of Fishes, especially of the Teleostei, are usually provided with a series of membrane bones. In the true branchial arches these take the form of dentigerous plates ; but no such plates are found in the Amphibia or Amniota.

The opercular flap attached to the hyoid arch is usually supported by a series of membrane bones, which attain their highest development in the Teleostei. One of these bones, the praeopercular, is very constant and is primitively attached along the outer edge of the hyomandibular. It seems to be retained in Amphibia as a membrane bone, overlapping the attachment of the quadrate and known as the squamosal ; though it is not impossible that this bone may be derived from a superficial membrane bone, widely distributed in Teleostei and Ganoids, which is known as the supra-temporal. In Dipnoi the bone which appears to be clearly homologous with the squamosal would seem from its position to belong to the series of dorsal plates, and therefore to be the supra-temporal ; but it is regarded by Huxley (No. 446) as the praeopercular 1 .

In the Amniota the squamosal forms an integral part, of the osseous roof of the skull ; but in the Sauropsida it continues, as in Amphibia, to be closely related to the quadrate.

A larger series of persistent membrane bones are related to the mandibular, and its palato-quadrate process.

Overlying the palato-quadrate process are two rows of bones,

1 It is not impossible that the solution of the difficulty about the praeopercular is to be found by supposing that the praeopercular as it exists in Teleostei is derived from a dorsal dermal plate, and that in the Dipnoi this plate retains more nearly than in Teleostei its primitive position.

B. III. 3 8


594 MEMBRANE BONES.


one row lying at the edge of the mouth, on the outer side of the pterygo-palatine process, and the other set on the roof of the mouth superficial to the pterygo-palatine process.

The outer row is formed of the praemaxilla, maxilla, jugal, and very often quadrato-jugal. Of these bones the maxilla and prsemaxilla, as is more especially demonstrated by their ontogeny in the Urodela, are partly derived from dentigerous plates and partly from membrane plates outside the mouth; while the jugal, and quadrato-jugal when present, are entirely extra-oral. In the Amphibia and Amniota the praemaxillae and maxillae are the most important bones in the facial region, and are quite independent of any cartilaginous substratum.

The second row of bones is clearly constituted in the Dipnoi and Amphibia by the vomer in front, then the palatine, and finally the pterygoid behind. Of these bones the vomer is never related to a cartilaginous tract below, while the palatines and pterygoids usually are so. The position and growth of the three bones in many Urodela (Axolotl) are especially striking (Hertwig. No. 442). In the Axolotl they form a continuous series, the vomer and palatine being covered by teeth, but the pterygoid being without teeth. The vomer and palatine originate from the united osseous plates of the bases of the teeth, while the pterygoid is in the first instance continuous with the palatine.

In Teleostei, Amia, etc., there are dentigerous plates forming a palatine and pterygoid, which in position, at any rate, closely correspond with the similarly named bones in Amphibia ; and there is also a dentigerous vomer which may fairly be considered as equivalent to that in Amphibia.

In the Amniota the three bones found in Amphibia are always present, but with a few exceptions amongst the Lacertilia and Ophidia, are no longer dentigerous. The cartilaginous bars, which in the lower types are placed below the palatine and pterygoid membrane bones, are usually imperfectly or not at all developed.

On Meckel's cartilage important membrane bones are almost always grafted. On the outside and distal part of the cartilage a dentary is usually developed, which may envelope and replace the cartilage to a larger or smaller extent. Its oral edge


THE SKULL. 595


is usually dentigerous. The splenial membrane bone is the most important bone on the inner side of Meckel's cartilage, but other elements known as the coronoid and angular may also be added. In Mammalia the dentary is the only element present (vide p. 590).

On the roof of the mouth a median bone, the parasphenoid, is very widely present in the Amphibia and Fishes, except the Elasmobranchii and Cyclostomata, and has no doubt the same phylogenetic origin as the vomer and membranous palatines and pterygoids.

It is less important in the Sauropsida, and becomes indistinguishably fused with the sphenoid in the adult, while in Mammalia it is no longer found.

Ossification of the Cartilaginous Cranium. In certain Fishes the cartilaginous cranium remains quite unossified, while completely enveloped in dermal bones. Such for instance is its condition in the Selachioid Ganoids. In most instances, however, the investment of the cartilaginous cranium by membrane bones is accompanied by a more or less complete ossification of the cartilage itself.

In the Dipnoi this occurs to the smallest extent, the only ossifications occurring in the lateral parts of the occipital region, and forming the exoccipitals.

In Teleostei and bony Ganoids, a considerably greater number of ossifications occur in the cartilage.

In the region of the occipital cartilaginous ring there appears a basioccipital and supraoccipital and two exoccipitals. The basioccipital is the only bone on the floor of the skull ossifying that part into which the notochord is primitively continued 1 .

In the region of the periotic cartilage a large number of bones may appear. In front there is the prootic, which often meets the exoccipital behind ; behind there is above and in close connection with the supraoccipital the epiotic, and below in close connection with the exoccipital the opisthotic. On the dorsal side of the cartilage there is a projecting ridge composed mainly of a bone known as the pterotic, sometimes erroneously

1 The notochord appears also to enter into the posterior part of the region which ossifies as the basisphenoid.

383


59 6 OSSIFICATIONS OF THE CARTILAGINOUS CRANIUM.

called the squamosal, and continued in front by the sphenotic. The pterotic, or the cartilaginous region corresponding to it, always supplies the articular surface for the hyomandibular.

In the floor of the skull, in the region of the pituitary body, there is formed a basisphenoid; while in the lateral parts of the wall of this part of the cranium, there is a bone known as the alisphenoid.

In front, parts of the lateral walls of the cranium ossify as the orbitosphenoids.

In view of the very imperfect ossification of the cartilaginous cranium of the Dipnoi, and of the fact that there is certainly no direct genetic connection between the Teleostei on the one hand, and the Amphibia and Amniota on the other, it is very difficult to believe that most of the ossifications of the cranium in the Amphibia and Amniota have more than a general correspondence with those in the Teleostei.

In the Amphibia the ossifications in the cartilage are comparatively few. In the occipital region there is a lateral ossification on each side of the exoccipital. the basioccipital region being unossified, and the supraoccipital at the utmost indurated by a calcareous deposit.

The periotic capsule is ossified by a prootic centre, which meets the exoccipital behind.

The front part of the cartilaginous cranium is ossified by a complete ring of bone the sphenethmoid bone which embraces part of the ethmoid region, and of the orbitosphenoid and presphenoid regions.

In the Amphibia the cartilaginous cranium, with its centres of ossification, is easily separable from the membranous investing bones.

In the Amniota the cartilaginous cranium, whose development in the embryo has already been described, becomes in the adult much more largely ossified, and the bones which replace the primitive cartilage unite with the membrane bones to form a continuous bony cranium.

The centres of ossification become again much more numerous. In the occipital segment analogous centres to those of Teleostei are again found ; and it is probable that the exoccipitals are homologous throughout the series, the supraoccipital and basioc


THE SKULL. 597


cipital bones of the higher types being merely identical in position with the similarly named bones in Fishes.

In the periotic there are usually three centres of ossification, first recognised by Huxley. These are the prootic, the epiotic and opisthotic, the situations of which have already been defined. Of these the prootic is the most constant.

In Reptiles, the prootic and opisthotic frequently remain distinct even in the adult.

In Birds, the epiotic and opisthotic are early united with the supra- and exoccipital ; and at a later period the prootic is also indistinguishably fused with the adjacent parts.

In Mammals the three ossifications fuse into a continuous whole the periotic bone which may be partially united with the adjacent parts.

In the pituitary region of the base of the cranium a pair of osseous centres or in the higher types a single centre (Parker 1 ) gives rise to the basisphenoid bone, and in front of this another basal or pair of basal ossifications forms the presphenoid, while laterally to these two centres there are formed centres of ossification in the alisphenoid and orbitosphenoid regions, which may be extremely reduced in various Sauropsida, leaving the side walls of the skull almost entirely formed of membrane or cartilage.

In the ethmoid region there may arise a median ossification forming the mesethmoid and lateral ossifications forming the lateral ethmoids or prefrontals ; which may assist in forming the front wall of the brain-case, or be situated quite externally to the brain-case and be only related to the olfactory capsules.

The labial cartilages. In most Fishes a series of skeletal structures, known as the labial cartilages, are developed at the front and sides of the mouth, and in connection with the olfactory capsules ; and these cartilages still persist in connection with the olfactory capsules, though in a reduced form, in the higher types. They are more developed in the Cyclostomata than in any other Vertebrate type.

The meaning of these cartilages is very obscure ; but, from their being in part employed to support the lips and horny teeth of the Cyclostomata and the Tadpole, I should be inclined to regard them as remnants of a primitive skeleton supporting the suctorial mouth, with which, on the grounds already stated (p. 317), I believe the ancestors of the present Vertebrata to have been provided.

1 According to Kblliker there are two centres in Man in both the basisphenoid and presphenoid.


598 BIBLIOGRAPHY.


BIBLIOGRAPHY.

(439) A. Duges. "Recherches sur 1'Osteologie et la myologie des Batraciens a leur differents ages." Paris, Mem. savans etrang. 1835, and An. Set. A 7 af. Vol. I. 1834.

(440) C. Gegenbaur. Untersuchwigen z. vergleich. Anat. d. Wirbelthiere, III. Heft. Das Kopfskelet d. Selachier. Leipzig, 1872.

(441) Giinther. Beob. iib. die Entwick. d. Gehororgans. Leipzig, 1842.

(442) O. Hertwig. " Ueb. d. Zahnsystem d. Amphibien u. seine Bedeutung f. d. Genese d. Skelets d. Mundhohle. " Archiv f. mikr. Anat., Vol. xi. 1874, suppl.

(443) T.H.Huxley. " On the theory of the vertebrate skull." Proc. Royal Soc., Vol. ix. 1858.

(444) T. H. Huxley. The Elements of Comparative Anatomy. London, 1869.

(445) T.H.Huxley. "On the Malleus and Incus." Proc. Zool. Soc., 1869.

(446) T.H.Huxley. "On Ceratodus Forsteri." Proc. Zool. Soc., 1876.

(447) T. H. Huxley. " The nature of the craniofacial apparatus of Petromyzon." Journ. of Anat. and Phys., Vol. X. 1876.

(448) T.H.Huxley. The Anatomy of Vertebrated Animals. London, 1871.

(449) W. K. Parker. "On the structure and development of the skull of the Common Fowl (Callus Domesticus)." Phil. Trans., 1869.

(450) W. K. Parker. "On the structure and development of the skull of the Common Frog (Rana temporaria)." Phil. Trans., 1871.

(451) W. K. Parker. "On the structure and development of the skull in the Salmon (Salmo salar)." Bakerian Lecture, Phil. Trans., 1873.

(452) W. K. Parker. "On the structure and development of the skull in the Pig (Sus scrofa). " Phil. Trans., 1874.

(453) W. K. Parker. "On the structure and development of the skull in the Batrachia." Part n. Phil. Trans., 1876.

(454) W. K. Parker. "On the structure and development of the skull in the Urodelous Amphibia." Part in. Phil. Trans., 1877.

(455) W. K. Parker. "On the structure and development of the skull in the Common Snake (Tropidonotus natrix)." Phil. Trans., 1878.

(456) W. K. Parker. " On the structure and development of the skull in Sharks and Skates." Trans. Zoolog. Soc., 1878. Vol. x. pt. iv.

(457) W. K. Parker. "On the structure and development of the skull in the Lacertilia." Pt. I. Lacerta agilis, L. viridis and Zootoca vivipara. Phil. Trans., 1879.

(458) W. K. Parker. "The development of the Green Turtle." The Zoology of the Voyage of H. M.S. Challenger. Vol. I. pt. V.

(459) W. K. Parker. "The structure and development of the skull in the Batrachia." Pt. in. Phil. Trans., 1880.

(460) W. K. Parker and G. T. Belt any. The Morphology of the Skull. London, 1877.

(460*) H. Rathke. Entwick. d. Natter. Konigsberg, 1839.

(461) C. B. Reichert. " Ueber die Visceralbogen d. Wirbelthiere." Miiller's Archiv, 1837.

(462) W. Saleusky. "Beitragez. Entwick. d. knorpeligen Gehorknochelchen." Morphol. Jahrbuch, Vol. VI. 1880.

Vide also Kolliker (No. 298), especially for the human and mammalian skull; Gotte (No. 296).


CHAPTER XX.


THE PECTORAL AND PELVIC GIRDLES AND THE SKELETON OF THE LIMBS.


TJie Pectoral girdle.

Pisces. Amongst Fishes the pectoral girdle presents itself in its simplest form in Elasmobranchii, where it consists of a bent band of cartilage on each side of the body, of somewhat variable form, meeting and generally uniting with its fellow ventrally. Its anterior border is in close proximity with the last visceral arch, and a transverse ridge on its outer and posterior border, forming the articular surface for the skeleton of the limb, divides it into a dorsal part, which may be called the scapula, and a ventral part which may be called the coracoid.

In all the remaining groups of Fishes there is added to the cartilaginous band, which may wholly or partially ossify, an osseous support composed of a series of membrane bones.

In the types with such membrane bones the cartilaginous parts do not continue to meet ventrally, except in the Dipnoi where there is a ventral piece of cartilage, distinct from that bearing the articulation of the limb. The cartilage is moreover produced into two ventral processes, an anterior and a posterior, below the articulation of the limb ; which may be called, in accordance with Gegenbaur's nomenclature, the praecoracoid and coracoid. Of these the praecoracoid is far the most


600 THE PECTORAL GIRDLE.

prominent, and in the majority of cases the coracoid can hardly be recognised. The coracoid process is however well developed in the Selachioid Ganoids, and the Siluroid Teleostei. In Teleostei the scapular region often ossifies in two parts, the smaller of which is named by Parker praecoracoid, though it is quite distinct from Gegenbaur's praecoracoid. The membrane bones, as they present themselves in their most primitive state in Acipenser and the Siluroids, are dermal scutes embracing the anterior edge of the cartilaginous girdle. In Acipenser there are three scutes on each side. A dorsal scute known as the supra-clavicle, connected above with the skull by the posttemporal ; a middle piece or clavicle, and a ventral or infraclavicle (inter-clavicle), which meets its fellow below.

In most Fishes the primitive dermal scutes have become subdermal membrane bones, and the infra-clavicle is usually not distinct, but the two clavicles form the most important part of the membranous elements of the girdle. Additional membrane bones (post-clavicles) are often present behind the main row.

The development of these parts in Fishes has been but little studied.

In Scyllium, amongst the Elasmobranchii, I find that each half of the pectoral girdle develops as a vertical bar of cartilage at the front border of the rudimentary fin, and externally to the muscle-plates.

Before the tissue forming the pectoral girdle has acquired the character of true cartilage, the bars of the two sides meet ventrally by a differentiation in situ of the mesoblastic cells, so that, when the girdle is converted into cartilage, it forms an undivided arc, girthing the ventral side of the body. There is developed in continuity with the posterior border of this arc on the level of the fin a horizontal bar of cartilage, which is continued backwards along the insertion of the fin, and, as will be shewn in the sequel, becomes the metapterygium of the adult (figs. 344, bp and 348, mp). With this bar the remaining skeletal elements of the fin are also continuous.

The foramina of the pectoral girdle are not in the first instance formed by absorption, but by the non-development of the cartilage in the region of pre-existing nerves and vessels.


THE PECTORAL GIRDLE. 6oi

The development of these parts in Teleostei has been recently investigated by 'Swirski (No. 472) who finds in the Pike (Esox) that the cartilaginous pectoral girdle is at first continuous with the skeleton of the fin. It forms a rod with a dorsal scapular and ventral coracoid process. An independent mass of cartilage gives rise to a prascoracoid, which unites with the main mass, forming a triradiate bar like that of Acipenser or the Siluroids. The coracoid process becomes in the course of development gradually reduced.

'Swirski concludes that the so-called praecoracoid bar is to some extent a secondary element, and that the coracoid bar corresponds to the whole of the ventral part of the girdle of Elasmobranchii, but his investigations do not appear to me to be as complete as is desirable.

Amphibia and Amniota. The pectoral girdle contains a more or less constant series of elements throughout the Amphibia and Amniota ; and the differences in structure between the shoulder girdle of these groups and that of Fishes are so great that it is only possible to make certain general statements respecting the homologies of the parts in the two sets of types.

The generally accepted view, founded on the researches of Parker, Huxley, and Gegenbaur, is to the effect that there is a primitively cartilaginous coraco-scapular plate, homologous with that in Fishes, and that the membrane bones in Fishes are represented by the clavicle and inter-clavicle in the Sauropsida and Mammalia, which are however usually admitted to be absent in Amphibia. These views have recently been challenged by Gotte (No. 466) and Hoffmann (No. 467), on the ground of a series of careful embryological observations ; and until the whole subject has been worked over by other observers it does not seem possible to decide satisfactorily between the conflicting views. It is on all hands admitted that the scapulo-coracoid elements of the shoulder girdle are formed as a pair of cartilaginous plates, one on each side of the body. The dorsal half of each plate becomes the scapula, which may subsequently become divided into a supra-scapula and scapula proper ; while the ventral half forms the coracoid, which is not always separated from the scapula, and is usually divided into a coracoid proper, a praecoracoid, and an epicoracoid. By the conversion of parts of the primitive cartilaginous plates into membranous tissue various fenestrae may be formed in the cartilage, and the bars


602 THE NATURE OF THE CLAVICLE.

bounding these fenestrae both in the scapula and coracoid regions have received special names ; the anterior bar of the coracoid region, forming the praecoracoid, being especially important. At the boundary between the scapula and the coracoid, on the hinder border of the plate, is placed the glenoid articular cavity to carry the head of the humerus.

The grounds of difference between Gotte and Hoffmann and other anatomists concern especially the clavicle and inter-clavicle. The clavicle is usually regarded as a membrane bone which may become to some extent cartilaginous. By. the above anatomists, and by Rathke also, it is held to be at first united with the coraco-scapular plate, of which it forms the anterior limb, free ventrally, but united dorsally with the main part of the plate ; and Gotte and Hoffmann hold that it is essentially a cartilage bone, which however in the majority of the Reptilia ossifies directly without passing through the condition of cartilage.

The interclavicle (episternum) is held by Gotte to be developed from a paired formation at the free ventral ends of the clavicles, but he holds views which are in many respects original as to its homologies in Mammalia and Amphibia. Even if Gotte's facts are admitted, it does not appear to me necessarily to follow that his deductions are correct. The most important of these is to the effect that the dermal clavicle of Pisces has no homologue in the higher types. Granting that the clavicle in these groups is in its first stage continuous with the coracoscapular plate, and that it may become in some forms cartilaginous before ossifying, yet it seems to me all the same quite possible that it is genetically derived from the clavicle of Pisces, but that it has to a great extent lost even in development its primitive characters, though these characters are still partially indicated in the fact that it usually ossifies very early and partially at least as a membrane bone 1 .

In treating the development of the pectoral girdle systematically it will be convenient to begin with the Amniota, which may be considered to fix the nomenclature of the elements of the shoulder girdle.

1 The fact of the clavicle going out of its way, so to speak, to become cartilaginous before being ossified, may perhaps be explained by supposing that its close connection with the other parts of the shoulder girdle has caused, by a kind of infection, a change in its histological characters.


II IK PECTORAL GIRDLE.


603


Lacertilia. The shoulder girdle is formed as two membranous plates, from the dorsal part of the anterior border of each of which a bar projects (Rathke, Gotte), which is free at its ventral end. This bar, which is usually (Gegenbaur, Parker) held to be independent of the remaining part of the shoulder girdle, gives rise to the clavicle and interclavicle. The scapulocoracoid plate soon becomes cartilaginous, while at the same time the clavicular bar ossifies directly from the membranous state. The ventral ends of the two clavicular bars enlarge to form two longitudinally placed plates, which unite together and ossify as the interclavicle.

Parker gives a very different account of the interclavicle in Anguis. He states that it is formed of two pairs of bones 'strapped on to the antero-inferior part of the prassternum,' which subsequently unite into one.

Chelonia. The shoulder girdle of the Chelonia is formed (Rathke) of a triradiate cartilage on each side, with one dorsal and two ventral limbs. It is admitted on all hands that the dorsal limb is the scapular element, and the posterior ventral limb the coracoid ; but, while the anterior ventral limb is usually held to be the praecoracoid, Gotte and Hoffmann maintain that, in spite of its being formed of cartilage, it is homologous with the anterior bar of the primitive shoulder-plates of Lacertilia, and therefore the homologue of the clavicle.

Parker and Huxley (doubtfully) hold that the three anterior elements of the ventral plastron (entoplastron and epiplastra) are homologous with the interclavicle and clavicles, but considering that these plates appear to belong to a secondary system of dermal ossifications peculiar to the Chelonia, this homology does not appear to me probable.

Aves. There are very great differences of view as to the development of the pectoral arch of Aves.

About the presence in typical forms of the coraco-scapular plate and two independent clavicular bars all authors are agreed. With reference to the clavicle and interclavicle Parker (No. 468) finds that the scapular end of the clavicle attaches itself to and ossifies a mass of cartilage, which he regards as the mesoscapula, while the interclavicle is formed of a mass of tissue between the ends of the clavicles where they meet ventrally, which becomes the dilated plate at their junction.

Gegenbaur holds that the two primitive clavicular bars are simply clavicles, without any element of the scapula ; and states that the clavicles are not entirely ossified from membrane, but that a delicate band of cartilage precedes the osseous bars. He finds no interclavicle.

Gotte and Rathke both state that the clavicle is at first continuous with the coraco-scapular plate, but becomes early separated, and ossifies entirely as a membrane bone. Gotte further states that the interclavicles are formed as outgrowths of the median ends of the clavicles, which extend themselves at an early period of development along the inner edges of the two halves of the sternum. They soon separate from the clavicles, which subsequently meet to form the furculum ; while the interclavicular rudiments give rise, on the junction of the two halves of the sternum, to its keel, and to the ligament


604 THK PECTORAL GIRDLE.

connecting the furculum with the sternum. The observations of Gotte, which tend to shew the keel of the sternum is really an interclavicle, appear to me of great importance.

A prascoracoid, partially separated from the coracoid by a space, is present in Struthio. It is formed by a fenestration of a primitively continuous cartilaginous coracoid plate (Hoffmann). In Dromaeus and Casuarius clavicles are present (fused with the scapula in the adult Dromaeus), though absent in other Ratitae (Parker, etc.).

Mammalia. The coracoid element of the coraco-scapular plate is much reduced in Mammalia, forming at most a simple process (except in the Ornithodelphia) which ossifies however separately 1 .

With reference to the clavicles the same divergencies of opinion met with in other types are found here also.

The clavicle is stated by Rathke to be at first continuous with the coracoscapular plate. It is however soon separated, and ossifies very early, in the human embryo before any other bone. Gegenbaur however shewed that the human clavicle is provided with a central axis of cartilage, and this observation has been confirmed by Kolliker, and extended to other Mammalia by Gotte. The mode of ossification is nevertheless in many respects intermediate between that of a true cartilage bone and a membrane bone. The ends of the clavicles remain for some time, or even permanently, cartilaginous, and have been interpreted by Parker, it appears to me on hardly sufficient grounds, as parts of the mesoscapula and praecoracoid. Parker's so-called mesoscapula may ossify separately. The homologies of the episternum are much disputed. Gotte, who has worked out the development of the parts more fully than any other anatomist, finds that paired interclavicular elements grow out backwards from the ventral ends of the clavicles, and uniting together form a somewhat T-shaped interclavicle overlying the front end of the sternum. This condition is permanent in the Ornithodelphia, except that the anterior part of the sternum undergoes atrophy. But in the higher forms the interclavicle becomes almost at once divided into three parts, of which the two lateral remain distinct, while the median element fuses with the subjacent part of the sternum and constitutes with it the presternum (manubrium sterni). If Gotte' s facts are to be trusted, and they have been to a large extent confirmed by Hoffmann, his homologies appear to be satisfactorily established. As mentioned on p. 563 Ruge (No. 438) holds that Gotte is mistaken as to the origin of the presternum.

Gegenbaur admits the lateral elements as parts of the interclavicle, while Parker holds that they are not parts of an interclavicle but are homologous with the omosternum of the Frog, which is however held by Gotte to be a true interclavicle.

1 This process, known as the coracoid process, is held by Sabatier to be the pnecoracoid ; while this author also holds that the upper third of the glenoid cavity, which ossifies by a special nucleus, is the true coracoid. The absence of a praecoracoid in the Ornithodelphia is to my mind a serious difficulty in the way of Sabatier's view.


THE PECTORAL GIRDLE. 605

Amphibia. In Amphibia the two halves of the shoulder girdle are each formed as a continuous plate, the ventral or coracoid part of which is forked, and is composed of a larger posterior and a smaller anterior bar-like process, united dorsally. In the Urodela the two remain permanently free at their ventral ends, but in the Anura they become united, and the space between them then forms a fenestra. The anterior process is usually (Gegenbaur, Parker) regarded as the praecoracoid, but Gotte has pointed out that in its mode of development it strongly resembles the clavicle of the higher forms, and behaves quite differently to the so-called praecoracoid of Lizards. It is however to be noticed that it differs from the clavicle in the fact that it is never segmented off from the coraco-scapular plate, a condition which has its only parallel in the equally doubtful case of the Chelonia. Parker holds that there is no clavicle present in the Amphibia, while Gegenbaur maintains that an ossification which appears in many of the Anura (though not in the Urodela) in the perichondrium on the anterior border of the cartilaginous bar above mentioned is the representative of the clavicle. Gotte's observations on the ossification of this bone throw doubt upon this view of Gegenbaur ; while the fact that the cartilaginous bar may be completely enclosed by the bone in question renders Gegenbaur's view, that there is present both a clavicle and prsecoracoid, highly improbable.

No interclavicle is present in Urodela, but in this group and in a number of the Anura, a process grows out from the end of each of the bars (praecoracoids) which Gotte holds to be the clavicles. The two processes unite in the median line, and give rise in front to the anterior unpaired element of the shoulder girdle (omosternum of Parker). They sometimes overlap the epicoracoids behind, and fusing with them bind them together in the median line. Parker who has described the paired origin of the so-called omosternum, holds that it is not homologous with the interclavicle, but compares it with his omosternum in Mammals.


BIBLIOGRAPHY.

(463) Bruch. " Ueber die Entwicklung der Clavicula und die Farbe des Blutes. " Zeit.f. wiss. Zool., \\. 1853.

(464) A. Duges. " Recherches sur 1'osteologie et la myologie des Batraciens a leurs differens ages." Memoires des savants etrang. Academic royale des sciences de Finstitut de France^ Vol. vi. 1835.

(465) C. Gegenbaur. Untersuchungen zur vergleichenden Anatomie der Wirbelthiere, 2 Heft. Schultergiirtel der Wirbelthiere. Bmstflosse der Fische. Leipzig, 1865.

(466) A. Gotte. "Beitrage z. vergleich. Morphol. d. Skeletsystems d. Wirbelthiere : Brustbien u. Schultergiirtel." Archivf. mikr, Anat. Vol. xiv. 1877.

(467) C. K. Hoffmann. "Beitrage z. vergleichenden Anatomic d. Wirbelthiere." Niederlandisches Archivf. ZooL,Vol.v. 1879.

(468) W. K. Parker. "A Monograph on the Structure and Development of the Shoulder-girdle and Sternum in the Vertebrata." Ray Society, 1868.


606 PELVIC GIRDLE.


(469) H. Rathke. Ueber die Entwicklung der Schildkrbten. Braunschweig, 1848.

(470) H. Rathke. Ueber den Bau und die Entwicklung des Brustbeins der Saurier, 1853.

(471) A. Sabatier. Comparaison des ceinfures et des membres antMeurs et posttrtturs d. la Serie d. Vertttrh. Montpellier, 1880.

(472) Georg 'Swirski. Untersuch. iib. d. Entwick. d. Schultergiirtels n. d. Skelets d. Brustflosse d. Hechts. Inaug. Diss. Dorpat, 1880.


Pelvic girdle.

Pisces. The pelvic girdle of Fishes is formed of a cartilaginous band, to the outer and posterior side of which the basal element of the pelvic fin is usually articulated. This articulation divides it into a dorsal iliac, and ventral pubic section. The iliac section never articulates with the vertebral column.

In Elasmobranchii the two girdles unite ventrally, but the iliac section is only slightly developed. In Chimaera there is a well developed iliac process, but the pubic parts of the girdle are only united by connective tissue.

In the cartilaginous Ganoids the pelvic girdle is hardly to be separated from the skeleton of the fin. It is not united with its fellow, and is represented by a plate with slightly developed pubic and iliac processes.

In the Dipnoi there is a simple median cartilage, articulated with the limb, but not provided with an iliac process. In bony Ganoids and Teleostei there is on each side a bone meeting its fellow in the ventral line, which is usually held to be the rudiment of the pelvic girdle ; while Davidoff attempts to shew that it is the basal element of the fin, and that, except in Polypterus, a true pelvic girdle is absent in these types.

From my own observations I find that the mode of development of the pelvic girdle in Scyllium is very similar to that of the pectoral girdle. There is a bar on each side, continuous on its posterior border with the basal element of the fin (figs. 345 and 347). This bar meets and unites with its fellow ventrally before becoming converted into true cartilage, and though the iliac process (il) is never very considerable, yet it is better developed in the embryo than in the adult, and is at first directed nearly horizontally forwards.

Amphibia and Amniota. The primitive cartilaginous pelvic


PELVIC GIRDLE. 607


girdle of the higher types exhibits the same division as that of Pisces into a dorsal and a ventral section, which meet to form the articular cavity for the femur, known as the acetabulum. The dorsal section is always single, and is attached by means of rudimentary ribs to the sacral region of the vertebral column, and sometimes to vertebrae of the adjoining lumbar or caudal regions. It always ossifies as the ilium.

The ventral section is usually formed of two more or less separated parts, an anterior which ossifies as the pubis, and a posterior which ossifies as the ischium. The space between them is known as the obturator foramen. In the Amphibia the two parts are not separated, and resemble in this respect the pelvic girdle of Fishes. They generally meet the corresponding elements of the opposite side ventrally, and form a symphysis with them. The symphysis pubis, and symphysis ischii may be continuous (Mammalia, Amphibia).

The observations on the development of the pelvic girdle in the Amphibia and Amniota are nearly as scanty as on those of Fishes.

Amphibia. In the Amphibia (Bunge, No. 473) the two halves of the pelvic girdle are formed as independent masses of cartilage, which subsequently unite in the ventral line.

In the Urodelous Amphibia (Triton) each mass is a simple plate of cartilage divided into a dorsal and ventral section by the acetabulum. The ventral parts, which are not divided into two regions, unite in a symphysis comparatively late.

The dorsal section ossifies as the ilium. The ventral usually contains a single ossification in its posterior part which forms the ischium ; while the anterior part, which may be considered as representing the pubis, usually remains cartilaginous ; though Huxley (No. 475) states that it has a separate centre of ossification in Salamander, which however does not appear to be always present (Bunge). There is a small obturator foramen between the ischium and pubis, which gives passage to the obturator nerve. It is formed by the part of the tissue where the nerve is placed not becoming converted into cartilage.

There is a peculiar cartilage in the ventral median line in front of the pubis, which is developed independently of and much later than the true parts of the pelvic girdle. It may be called the praepubic cartilage.

Reptilia. In Lacertilia the pelvic girdle is formed as a somewhat triradiate mass of cartilage on each side, with a dorsal (iliac) process, and two ventral (pubic and ischiad) processes. The acetabulum is placed on the outer side at the junction of the three processes, each of which may be


6o8 PECTORAL AND PELVIC GIRDLES.

considered to have a share in forming it. The distal ends of the pubis and ischium are close together when first formed, but subsequently separate. Each of them unites at a late stage with the corresponding process of the opposite side in a ventral symphysis. A centre of ossification appears in each of the three processes of the primitive cartilage.

Aves. In Birds the parts of the pelvic girdle no longer develop as a continuous cartilage (Bunge). Either the pubis may be distinct, or, as in the Uuck, all the elements. The ilium early exhibits a short anterior process, but the pubis and ischium are at first placed with their long axes at right angles to that of the ilium, but gradually become rotated so as to lie parallel with it, their distal ends pointing backwards, and not uniting ventrally excepting in one or two Struthious forms.

Mammalia. In Mammalia the pelvic girdle is formed in cartilage as in the lower forms, but in Man at any rate the pubic part of the cartilage is formed independently of the remainder (Rosenberg). There are the usual three centres of ossification, which unite eventually into a single bone the innominate bone. The pubis and ischium of each side unite with each other ventrally, so as completely to enclose the obturator foramen.

Huxley holds that the so-called marsupial bones of Monotremes and Marsupials, which as shewn by Gegenbaur (No. 474) are performed in cartilage, are homologous with the praepubis of the Urodela ; but considering the great gap between the Urodela and Mammalia this homology can only be regarded as tentative. He further holds that the anterior prolongations of the cartilaginous ventral ends of the pubis of Crocodilia are also structures of the same nature.


BIBLIOGRAPHY.

(473) A. Bunge. Untersuch. z, Entwick. d. Beckengiirtels d. Amphibien, Reptilien u. Vogel, Inaug. Diss. Dorpat, 1880.

(474) C. Gegenbaur. " Ueber d. Ausschluss des Schambeins von d. Pfanne d. Hiiftgelenkes." Morph. Jahrbuch, Vol. II. 1876.

(475) Th. H. Huxley. "The characters of the Pelvis in Mammalia, etc." Proc. of Roy. Soc., Vol. xxvm. 1879.

(476) A. Sabatier. Comparaison des ceintures et des membres anterieurs et posterieurs dans la Serie d. Vertebrcs. Montpellier, 1880.

Comparison of Pectoral and Pelvic girdles.

Throughout the Vertebrata a more or less complete serial homology may be observed between the pectoral and pelvic girdles.

In the cartilaginous Fishes each girdle consists of a continuous band, a dorsal and ventral part being indicated by the articulation of the fin ; the former being relatively undeveloped in the pelvic


LIMBS. 609

girdle, while in the pectoral it may articulate with the vertebral column. In the case of the pectoral girdle secondary membrane bones become added to the primitive cartilage in most Fishes, which are not developed in the case of the pelvic girdle.

In the Amphibia and Amniota the ventral section of each girdle becomes divided into an anterior and a posterior part, the former constituting the praecoracoid and pubis, and the latter the coracoid and ischium ; these parts are however very imperfectly differentiated in the pelvic girdle of the Urodela. The ventral portions of the pelvic girdle usually unite below in a symphysis. They also meet each other ventrally in the case of the pectoral girdle in Amphibia, but in most other types are separated by the sternum, which has no homologue in the pelvic region, unless the praepubic cartilage is to be regarded as such. The dorsal or scapular section of the pectoral girdle remains free ; but that of the pelvic girdle acquires a firm articulation with the vertebral column.

If the clavicle of the higher types is derived from the membrane bones of the pectoral girdle of Fishes, it has no homologue in the pelvic girdle ; but if, as Gotte and Hoffmann suppose, it is a part of the primitive cartilaginous girdle, the ordinary view as to the serial homologies of the ventral sections of the two girdles in the higher types will need to be reconsidered.

Limbs.

It will be convenient to describe in this place not only the development of the skeleton of the limbs but also that of the limbs themselves. The limbs of Fishes are moreover so different from those of the Amphibia and Amniota that the development of the two types of limb may advantageously be treated separately.

In Fishes the first rudiments of the limbs appear as slight longitudinal ridge-like thickenings of the epiblast, which closely resemble the first rudiments of the unpaired fins.

These ridges are two in number on each side, an anterior immediately behind the last visceral fold, and a posterior on the level of the cloaca. In most Fishes they are in no way connected, but in some Elasmobranch embryos, more especially in Torpedo, they are connected together at their first development B. in. 39


6io


PAIRED FINS OF ELASMOBRANCHII.


by a line of columnar epiblast cells 1 . This connecting line of columnar epiblast is a very transitory structure, and after its disappearance the rudimentary fins become more prominent, consisting (fig. 343, &) of a projecting ridge both of epiblast and mesoblast, at the outer edge of which is a fold of epiblast only, which soon reaches considerable dimensions. At a later stage the mesoblast penetrates into this fold and the fin becomes a simple ridge of mesoblast, covered by epiblast. The pectoral fins are usually considerably ahead of the pelvic fins in development.

For the remaining history it is necessary to confine ourselves to Scylliurn as the only type which has been adequately studied.

The direction of the original ridge which connects the two fins of each side is nearly though not quite longitudinal, sloping somewhat obliquely downwards. It thus comes about that the attachment of each pair of limbs is somewhat on a slant, and that the pelvic pair nearly meet each other in the median ventral line a little way behind the anus.

The elongated ridge, forming the rudiment of each fin, gradually projects more and more, and so becomes broader in proportion to its length, but at the same time its actual attachment to the side of the body becomes shortened from behind forwards, so that what was originally the attached border becomes in part converted into the posterior border. This process is much more completely carried out in the case of the pectoral fins than in that of the pelvic, and the changes of form undergone by the pectoral fin in its development may be gathered from figs. 344 and 348.



FIG. 343. SECTION THROUGH THE VENTRAL PART OF THE TRUNK OF A YOUNG EMBRYO OF SCYLLIUM AT THE LEVEL OF THE UMBILICAL CORD.

b. pectoral fin ; ao. dorsal aorta ; cav. cardinal vein ; ua. vitelline artery ; u.v, vitelline vein ; al. duodenum ; /. liver ; sd. opening of segmented duct into the body cavity ; mp. muscle plate ; ;. umbilical canal.


1 I. M. I'alfour. Monograph on Elasmobranfh l-'hhes, pp. 1012.



LIMBS. 6ll

Before proceeding to the development of the skeleton of the fin it may be pointed out that the connection of the two rudimentary fins by a continuous epithelial line suggests the hypothesis that they are the remnants of two continuous lateral fins 1 .

Shortly after the view that the paired fins were remnants of continuous lateral fins had been put forward in my memoir on Elasmobranch Fishes, two very interesting papers were published by Thacker (No. 489) and Mivart (No. 484) advocating this view on the entirely independent grounds of the adult structure of the skeleton of the paired fins in comparison with that of the unpaired fins 2 .

The development of the skeleton has unfortunately not been as yet very fully studied. I have however made some investigations on this subject on Scyllium, and 'Swirski has also made some on the Pike.

In Scyllium the development of both the pectoral and pelvic fins is very similar.

In both fins the skeleton in its earliest stage consists of a bar springing from the posterior side of the pectoral or pelvic girdle, and running backwards parallel to the long axis of the body. The outer side of this bar is continued into a plate which

1 Both Maclise arid Humphry {Journal of Anat. and Pkys., Vol. v.) had previously suggested that the paired fins were related to the unpaired fins.

2 Davidoff in a Memoir (No. 477) which forms an important contribution to our knowledge of the structure of the pelvic fins has attempted from his observations to deduce certain arguments against the lateral fin theory of the limbs. His main argument is based on the fact that a variable but often considerable number of the spinal nerves in front of the pelvic fin are united, by a longitudinal commissure, with the true plexus of the nerves supplying the fin. From this he concludes that the pelvic fin has shifted its position, and that it may once therefore have been situated close behind the visceral arches. If this is the strongest argument which can be brought against the theory advocated in the text, there is I trust a considerable chance of its being generally accepted. For even granting that Davidoff's deduction from the character of the pelvic plexus is correct, there is, so far as I see, no reason in the nature of the lateral fin theory why the pelvic fins should not have shifted, and on the other hand the longitudinal cord connecting some of the spinal nerves in front of the pelvic fin may have another explanation. It might for instance be a remnant of the time when the pelvic fin had a more elongated form than at present, and accordingly extended further forwards.

In any case our knowledge of the nature and origin of nervous plexuses is far too imperfect to found upon their character such conclusions as those of Davidoff.

392


612


PAIRED FINS OF ELASMOBRANCHII.


extends into the fin, and which becomes very early segmented into a series of parallel rays at right angles to the longitudinal bar.

In other words, the primitive skeleton of both the fins consists of a longitudinal bar running along the base of the fin,



FIG. 344. PECTORAL FIN OF A YOUNG EMBRYO OF SCYLLIUM IN LONGITUDINAL AND HORIZONTAL SECTION.

The skeleton of the fin was still in the condition of embryonic cartilage. b.p. basipterygium (eventual metapterygium) ; fr. fin rays; p.g. pectoral girdle in transverse section; /. foramen in pectoral girdle; pc. wall of peritoneal cavity.

and giving off at right angles series of rays which pass into the fin. The longitudinal bar, which may be called the basipterygium, is moreover continuous in front with the pectoral or pelvic girdle as the case may be.

The primitive skeleton of the pectoral fin is shewn in longitudinal section in fig. 344, and that of the pelvic fin at a slightly later stage in fig. 345.

A transverse section shewing the basipterygium (inpi) of the pectoral fin, and the plate passing from it into the fin, is shewn in fig. 346.

Before proceeding to describe the later history of the two fins it may be well to point out that their embryonic structure completely supports the view which has been arrived at from the consideration of the soft parts of the fin.

My observations shew that the embryonic skeleton of the paired fin consists of a series of parallel rays similar to those of the unpaired fins. These rays support the soft part of the fin which has the form of a longitudinal ridge, and are continuous at their base with a longitudinal bar, which may very probably


LIMBS.


613


be due to secondary development. As pointed out by Mivart, a longitudinal bar is also occasionally formed to support the cartilaginous rays of unpaired fins. The longitudinal bar of the paired fins is believed by both Thacker and Mivart to be due to the coalescence of the bases of primitively independent rays, of which they believe the fin to have been originally composed. This view is probable enough in itself, but there is no trace



FIG. 345. PELVIC FIN OF A VERY YOUNG FEMALE EMBRYO OF SCYLLIUM STELLARE.

bb. basipterygium ; pu. pubic process of pelvic girdle ; il. iliac process of pelvic girdle.


in the embryo of the bar in question being formed by the coalesceace of rays, though the fact of its being perfectly continuous with the bases of the rays is somewhat in favour of this view 1 .

A point may be noticed here which may perhaps appear to be a difficulty, viz. that to a considerable extent in the pectoral, and to some extent in the pelvic fin the embryonic cartilage from which the fin-rays are developed is at first a continuous lamina, which subsequently segments into rays. I am however inclined to regard this merely as a result of the mode of conversion of the indifferent mesoblast into cartilage ; and in any case no conclusion adverse to the above view can be drawn from it, since I find that the rays of the unpaired fin are similarly segmented from a continuous lamina. In all cases the segmentation of the rays is to a large extent completed before the tissue in question is sufficiently differentiated to be called cartilage by an histologist.

Thacker and Mivart both hold that the pectoral and pelvic girdles have been evolved by ventral and dorsal growths of the anterior end of the longitudinal bar supporting the fin-rays.

There is, so far as I see, no theoretical objection to be taken to this view, and the fact of the pectoral and pelvic girdles originating continuously, and long remaining united with the

1 Thacker more especially founds his view on the adult form of the pelvic fins in the cartilaginous Ganoids ; Polyodon, in which the part which constitutes the basal plate in other forms is divided into separate segments, being mainly relied on. It is possible that the segmentation of this plate, as maintained by Gegenbaur and Davidoff, is secondary, but Thacker's view that the segmentation is a primitive character seems to me, in the absence of definite evidence to the reverse, the more natural one.


614


THE PELVIC FIN.


longitudinal bars of their respective fins is in favour of rather than against this view. The same may be said of the fact that the first part of each girdle to be formed is that in the neighbourhood of the longitudinal bar (basipterygium) of the fin, the dorsal and ventral prolongations being subsequent growths.

The later development of the skeleton of the two fins is more conveniently treated separately.

The pelvic fin. The changes in the pelvic fin are comparatively slight. The fin remains through life as a nearly horizontal lateral projection of the body, and the longitudinal bar the



FIG. 346. TRANSVERSE SECTION THROUGH THE PECTORAL FIN OF A YOUNG

EMBRYO OK SCYLLIUM STELLARE. mpt. basipterygial bar (metapterygium) ; fr. fin ray; m. muscles; hf. horny fibres.

basipterygium at its base always remains as such. It is for a considerable period attached to the pelvic girdle, but eventually becomes segmented from it. Of the fin rays the anterior remains directly articulated with the pelvic girdle on the separation of the basipterygium (fig. 347), and the remaining rays finally become segmented from the basipterygium, though they remain articulated with it. They also become to some extent transversely segmented. The posterior end of the basipterygial bar also becomes segmented off as the terminal ray.

The pelvic fin thus retains in all essential points its primitive arrangement.


LIMBS.


6l 5


The pectoral fin. The earliest stage of the pectoral fin



There


FIG. 347. PELVIC FIN OF A YOUNG MALE EMBRYO OF SCYLLIUM STELLARE.

bp. basipterygium ; m.o. process of basipterygium continued into clasper; il. iliac process of pectoral girdle ; pit. pubis.

differs from that of the pelvic fin only in minor points, is the same longitudinal or basipterygial bar to which the fin-rays are attached, whose position at the base of the fin is clearly seen in the transverse section (fig. 346, mpf). In front the bar is continuous with the pectoral girdle (figs. 344 and

348).

The changes which take place in the course of the further development are however very much more considerable in the case of the pectoral than in that of the pelvic fin. "' 3+8. F^OJJL ,,, v.

By the process spoken m p t me tapterygium (basipterygium of earlier

stage); me.p. rudiment of future pro- and mesopterygium ; sc. cut surface of scapular process ; cr. coracoid process;/;', foramen;/, horny fibres.



of above, by which the attachment of the pec


6l6 THE PECTORAL FIN.

toral fin to the body wall becomes shortened from behind forwards, the basipterygial bar is gradually rotated outwards, its anterior end remaining attached to the pectoral girdle. In this way this bar comes to form the posterior border of the skeleton of the fin (figs. 348 and 349, mp], constituting what Gegenbaur called the metapterygium, and eventually becomes segmented off from the pectoral girdle, simply articulating with its hinder edge.

The plate of cartilage, which is continued outwards from the basipterygium, or as we may now call it, the metapterygium, into the fin, is not nearly so completely divided up into fin-rays as in the case of the pelvic fin, and this is especially the case with the basal part of the plate. This basal part becomes in fact at first only divided into two parts (fig. 348) a small anterior part at the front end (me.p), and a larger posterior along the base of the remainder of the fin. The anterior part directly joins the pectoral girdle at its base, resembling in this respect the anterior fin-ray of the pelvic girdle. It constitutes the rudiment of the mesopterygium and propterygium of Gegenbaur. It bears four fin-rays at its extremity, the anterior not being well marked. The remaining fin-rays are borne by the edge of the plate continuous with the metapterygium.

The further changes in the cartilages of the limb are not important, and are easily understood by reference to fig. 349 representing the limb of a nearly full-grown embryo. The front end of the anterior basal cartilage becomes segmented off as a propterygium, bearing a single fin-ray, leaving the remainder of the cartilage as a mesopterygium. The remainder of the now considerably segmented fin-rays are borne by the metapterygium.

The mode of development of the pectoral fin demonstrates that, as supposed by Mivart, the metapterygium is the homologue of the basal cartilage of the pelvic fin.

From the mode of development of the fins of Scyllium conclusions may be drawn adverse to the views recently put forward on the structure of the fin by Gegenbaur and Huxley, both of whom consider the primitive type of fin to be most nearly retained in Ceratodus, and to consist of a central multisegmented axis with numerous rays. Gegenbaur derives the Elasmobranch pectoral fin from a form which he calls the archipterygium, nearly like that of Ceratodus, with a median axis and two


LIMBS.


6I 7


rows of rays ; but holds that in addition to the rays attached to the median axis, which are alone found in Ceratodus, there were other rays directly articulated to the shoulder-girdle. He considers that in the Elasmobranch fin the majority of the lateral rays on the posterior (median or inner according to his view of the position of the limb) side have become aborted, and that the central axis is represented by the metapterygium ; while the pro- and mesopterygium and their rays are, he believes, derived from those rays of the archipterygium which originally articulated directly with the shoulder-girdle.

Gegenbaur's view appears to me to be absolutely negatived by the facts of development of the pectoral fin in Scyllium ; not so much because the pectoral fin in this form is necessarily to be regarded as primitive, but because what Gegenbaur holds to be the primitive axis of the biserial fin is demonstrated to be really the base, and it is only in the adult that it is conceivable that a second set of lateral rays could have existed on the posterior side of the metapterygium. If Gegenbaur's view were correct we should expect to find in the embryo, if anywhere, traces of the second set of lateral rays ; but the fact is that, as may easily be seen by an inspection of figs. 344 and 346, such a second set of lateral rays could not possibly have existed in a type . of fin like that found in the embryo 1 . With this view of Gegenbaur's it appears to me that the theory held by this anatomist to the effect that the limbs are modified gill arches also falls ; in that his method of deriving the limbs from gill arches ceases to be admissible, while it is not easy to see how a limb, formed on the type of the embryonic limb of Elasmobranchs, could be derived from a visceral arch with its branchial rays 2 .

Gegenbaur's older view



FIG. 349. SKELETON OF THE PECTORAL FIN AND PART OF PECTORAL GIRDLE OF A NEARLY RIPE EMBRYO OF SCYLLIUM STELLARE.

m.p. metapterygium ; me.p. mesopterygium ; //. propterygium ; cr. coracoid process.


1 If, which I very much doubt, Gegenbaur is right in regarding certain rays found in some Elasmobranch pectoral fins as rudiments of a second set of rays on the posterior side of the metapterygium, these rays will have to be regarded as structures in the act of being evolved, and not as persisting traces of a biserial fin.

2 Some arguments in favour of Gegenbaur's theory adduced by Wiedersheim as a result of his researches on Protopterus are interesting. The attachment which he describes between the external gills and the pectoral girdle is no doubt remarkable, but I would suggest that the observations we have on the vascular supply of these gills demonstrate that this attachment is secondary.


6l8 THE CHEIKOPTERYGIUM.

that the Elasmobranch fin retains a primitive uniserial type appears to me to be nearer the truth than his more recent view on this subject ; though I hold that the fundamental point established by the development of these parts in Scyllium is that the posterior border of the adult Elasmobranch fin is the primitive base line, i.e. the line of attachment of the fin to the side of the body.

Huxley holds that the mesopterygium is the proximal piece of the axial skeleton of the limb of Ceratodus, and derives the Elasmobranch fin from that of Ceratodus by the shortening of its axis and the coalescence of some of its elements. The secondary character of the mesopterygium, and its total absence in the embryo Scyllium, appears to me as conclusive against Huxley's view, as the character of the embryonic fin is against that of Gegenbaur ; and I should be much more inclined to hold that the fin of Ceratodus has been derived from a fin like that of the Elasmobranchii by a series of steps similar to those which Huxley supposes to have led to the establishment of the Elasmobranch fin, but in exactly the reverse order.

With reference to the development of the pectoral fin in the Teleostei there are some observations of 'Swirski (No. 488) which unfortunately do not throw very much light upon the nature of the limb.

'Swirski finds that in the Pike the skeleton of the limb is formed of a plate of cartilage, continuous with the pectoral girdle ; which soon becomes divided into a proximal and a distal portion. The former is subsequently segmented into five basal rays, and the latter into twelve parts, the number of which subsequently becomes reduced.

These investigations might be regarded as tending to shew that the basipterygium of Elasmobranchii is not represented in Teleostei, owing to the fin rays not having united into a continuous basal bar, but the observations are not sufficiently complete to admit of this conclusion being founded upon them with any certainty.

Tlie ckeiropterygium.

Observations on the early development of the pentadactyloid limbs of the higher Vertebrata are comparatively scanty.

The limbs arise as simple outgrowths of the sides of the body, formed both of epiblast and mesoblast. In the Amniota, at all events, they are processes of a special longitudinal ridge known as the Wolffian ridge. In the Amniota they also bear at their extremity a thickened cap of epiblast, which may be compared with the epiblastic fold at the apex of the Elasmobranch fin.

Both limbs have at first a precisely similar position, both being directed backwards and being parallel to the surface of the body.


I 111: CHEIROPTERYGIUM.


619


In the Urodela (Gotte) the ulnar and fibular sides are primitively dorsal, and the radial and tibial ventral : in Mammalia however Kolliker states that the radial and tibial edges are from the first anterior.

The exact changes of position undergone by the limbs in the course of development are not fully understood. To suit a terrestrial mode of life the flexures of the two limbs become gradually more and more opposite, till in Mammalia the corresponding joints of the two limbs are turned in completely opposite directions.

Within the mesoblast of the limbs a continuous blastema becomes formed, which constitutes the first trace of the skeleton of the limb. The corresponding elements of the two limbs, viz. the humerus and femur, radius and tibia, ulna and fibula, carpal and tarsal bones, metacarpals and metatarsals, and digits, become differentiated within this, by the conversion of definite regions into cartilage, which may either be completely distinct or be at first united. These cartilaginous elements subsequently ossify.

The later development of the parts, more especially of the carpus and tarsus, has been made the subject of considerable study ; and important results have been thereby obtained as to the homology of the various carpal and tarsal bones throughout the Vertebrata ; but this subject is too special to be treated of here. The early development, including the succession of the growth of the different parts, and the extent of continuity primitively obtaining between them, has on the other hand been but little investigated ; recently however the development of the limbs in the Urodela has been worked out in this way by two anatomists, Gotte (No. 482) and Strasser (No. 487), and their results, though not on all points in complete harmony, are of considerable interest, more especially in their bearing on the derivation of the pentadactyloid limb from the piscine fin. Till however further investigations of the same nature have been made upon other types, the conclusions to be drawn from Gotte and Strasser's observations must be regarded as somewhat provisional, the actual interpretation of various ontological processes being very uncertain.

The forms investigated are Triton and Salamandra. We may remind the reader that the hand of the Urodela has four digits, and the foot five, the fifth digit being absent in the hand 1 . In Triton the proximal row of carpal bones consists (using Gegenbaur's nomenclature) of (i) a radiale, and (2 and 3) an intermedium and ulnare, partially united. The distal row is formed of four carpals, of which the first often does not support the first 1 This seems to me clearly to follow from Gotte and Strasser's observations.


620 THE GHE1ROPTERYGIUM.

metacarpal ; while the second articulates with both the first and second metacarpals. In the foot the proximal row of tarsals consists of a tibiale, an intermedium and a fibulare. The distal row is formed of four tarsals, the first, like that in the hand, often not articulating with the first metatarsal, the second supporting the first and second metatarsals ; and the fourth the fourth and fifth metatarsals.

The mode of development of the hand and foot is almost the same. The most remarkable feature of development is the order of succession of the digits. The two anterior (radial or tibial) are formed in the first instance, and then the third, fourth and fifth in succession.

As to the actual development of the skeleton Strasser, whose observations were made by means of sections, has arrived at the following results.

The humerus with the radius and ulna, and the corresponding parts in the hind limb, are the first parts to be differentiated in the continuous plate of tissue from which the skeleton of the limb is formed. Somewhat later a cartilaginous centre appears at the base of the first and second fingers (which have already appeared as prominences at the end of the limb) in the situation of the permanent second carpal of the distal row of carpals ; and the process of chondrification spreads from this centre into the fingers and into the remainder of the carpus. In this way a continuous carpal plate of cartilage is established, which is on the one hand continuous with the cartilage of the two metacarpals, and on the other with the radius and ulna.

In the cartilage of the carpus two special columns may be noticed, the one on the radial side, most advanced in development, being continuous with the radius ; the other less developed column on the side of the ulna being continuous both with the ulna and with the radius. The ulna and radius are not united with the humerus.

In the further growth the third and fourth digits, and in the foot the fifth digit also, gradually sprout out in succession from the ulnar side of the continuous carpal plate. The carpal plate itself becomes segmented from the radius and ulna, and divided up into the carpal bones.

The original radial column is divided into three elements, a proximal the radiale, a middle element the first carpal, and a distal the second carpal already spoken of. The first carpal is thus situated between the basal cartilage of the second digit and the radiale, and would therefore appear to be the representative of a primitive middle row of carpal bones, of which the centrale is also another representative.

The centrale and intermedium are the middle and proximal products of the segmentation of the ulnar column of the primitive carpus, the distal second carpal being common both to this column and to the radial column.

The ulnar or fibular side of the carpus or tarsus becomes divided into a proximal element the ulnare or fibulare the ulnare remaining partially united with the intermedium. There are also formed from this plate two carpals to articulate with digits 3 and 4 ; while in the foot the corresponding elements articulate respectively with the third digit, and with the fourth and fifth digits.


THE CIIF.IROPTERYGIUM. 621

Gotte, whose observations were made in a somewhat different method to those of Strasser, is at variance with him on several points. He finds that the primitive skeleton of the limb consists of a basal portion, the humerus, continued into a radial and an ulnar ray, which are respectively prolonged into the two first digits. The two rays next coalesce at the base of the fingers to form the carpus, and thus the division of the limb into the brachium, antebrachium and manus is effected.

The ulna, which is primitively prolonged into the second digit, is subsequently separated from it and is prolonged into the third ; from the side of the part of the carpus connecting the ulna with the third digit the fourth digit is eventually budded out, and in the foot the fourth and fifth digits arise from the corresponding region. Each of the three columns connected respectively with the first, second, and third digits becomes divided into three successive carpal bones, so that Gotte holds the skeleton of the hand or foot to be formed of a proximal, a middle, and a distal row of carpal bones each containing potentially three elements. The proximal row is formed of the radiale, intermedium and ulnare ; the middle row of carpal i, the centrale and carpal 4, and the distal of carpal 2 (consisting according to Gotte of two coalesced elements) and carpal 3.

The derivation of the cheiropterygium from the ichthyoptcrygium. All anatomists are agreed that the limbs of the higher Vertebrata are derived from those of Fishes, but the gulf between the two types of limbs is so great that there is room for a very great diversity of opinion as to the mode of evolution of the cheiropterygium. The most important speculations on the subject are those of Gegenbaur and Huxley.

Gegenbaur holds that the cheiropterygium is derived from a uniserial piscine limb, and that it consists of a primitive stem, to which a series of lateral rays are attached on one (the radial) side ; while Huxley holds that the cheiropterygium is derived from a biserial piscine limb by the "lengthening of the axial skeleton, accompanied by the removal of its distal elements further away from the shoulder-girdle and by a diminution in the number of the rays."

Neither of these theories is founded upon ontology, and the only ontological evidence we have which bears on this question is that above recorded with reference to the development of the Urodele limb.

Without holding that this evidence can be considered as in any way conclusive, its tendency would appear to me to be in favour of regarding the cheiropterygium as derived from a uniserial type of fin. The humerus or femur would appear to be the basipterygial bars (metapterygium), which have become directed outwards instead of retaining their original position parallel to the length of the body at the base of the fin. The anterior (proximal) fin-rays and the pro- and mesopterygium must be supposed to have become aborted, while the radius or ulna, and tibia or fibula are two posterior fin-rays (probably each representing several coalesced rays like the pro- and mesopterygium) which support at their distal extremities more numerous fin-rays consisting of the rows of carpal and tarsal bones.


622 THE CHEIROPTERYGIUM.

This view of the cheiropterygium corresponds in some respects with that put forward by Gotte as a result of his investigations on the development of the Urodele limbs, though in other respects it is very different. A difficulty of this view is the fact that it involves our supposing that the radial edge of the limb corresponds with the metapterygial edge of the piscine fin. The difficulties of this position have been clearly pointed out by Huxley, but the fact that in the primitive position of the Urodele limbs the radius is ventral and the ulna dorsal shews that this difficulty is not insuperable, in that it is easy to conceive the radial border of the fin to have become rotated from its primitive Elasmobranch position into the vertical position it occupies in the embryos of the Urodela, and then to have been further rotated from this position into that which it occupies in the adult Urodela and in all higher forms.

BIBLIOGRAPHY of the Limbs.

(477) M. v. Davidoff. "Beitrage z. vergleich. Anat. d. hinteren Gliedmaassen d. Fische I." Morphol. Jahrbuch, Vol. v. 1879.

(478) C. Gegenbaur. Untersuckungen z. vergleich. Anat. d. Wirbelthiere. Leipzig, 1864 5. Erstes Heft. Carpus u. Tarsus. Zweites Heft. Brustflosse d. Fische.

(479) C. Gegenbaur. "Ueb. d. Skelet d. Gliedmaassen d. Wirbelthiere im Allgemeinen u. d. Hintergliedmaassen d. Selachier insbesondere." Jenaische Zeitsckrift, Vol. V. 1870.

(480) C. Gegenbaur. " Ueb. d. Archipterygium." Jenaische Zeitschrift, Vol. vii. 1873.

(481) C. Gegenbaur. "Zur Morphologic d. Gliedmaassen d. Wirbelthiere." Morphologisches Jahrbuch, Vol. II. 1876.

(482) A. Gotte. Ueb. Entivick. u. Regeneration d. Gliedmaassenskelets d. Molche. Leipzig, 1879.

(483) T. H. Huxley. "On Ceratodus Forsteri, with some observations on the classification of Fishes." Proc. Zool. Soc. 1876.

(484) St George Mivart. "On the Fins of Elasmobranchii." Zoological Trans., Vol. x.

(485) A. Rosenberg. "Ueb. d. Entwick. d. Extremitaten-Skelets bei einigen d. Reduction ihrer Gliedmaassen charakterisirten Wirbelthieren." Zeil.f. iviss. Zool., Vol. xxin. 1873.

(486) E. Rosenberg. "Ueb. d. Entwick. d. Wirbelsaule u. d. centrale carpi d. Menschen. " Morphologisches Jahrbuch, Vol. I. 1875.

(487) H. Strasser. "Z. Entwick. d. Extremitatenknorpel bei Salamandern u. Tritonen." Morphologisches Jahrbuch, Vol. V. 1879.

(488) G. 'S wirski. Untersitch. iib. d. Entwick. d. Schultergitrtels u. d. Skelcls d. Brustflosse d. Hechts. Inaug. Diss. Dorpat, 1880.

(489) J. K. Thacker. "Median and paired fins. A contribution to the history of the Vertebrate limbs." Trans, of the Connecticut Acad., Vol. ill. 1877.

(490) J. K. Thacker. "Ventral fins of Ganoids." Trans, of the Connecticut Acad., Vol. iv. 1877.


CHAPTER XXI.


THE BODY CAVITY, THE VASCULAR SYSTEM, AND THE VASCULAR GLANDS.


The Body cavity.

IN the Ccelenterata no body cavity as distinct from the alimentary cavity is present ; but in the remaining Invertebrata the body cavity may (i) take the form of a wide space separating the wall of the gut from the body wall, or (2) may be present in a more or less reduced form as a number of serous spaces, or (3) only be represented by irregular channels between the muscular and connective-tissue cells filling up the interior of the body. The body cavity, in whatever form it presents itself, is probably filled with fluid, and the fluid in it may contain special cellular elements. A well developed body cavity may coexist with an independent system of serous spaces, as in the Vertebrata and the Echinodermata ; the perihaemal section of the body cavity of the latter probably representing the system of serous spaces.

In several of the types with a well developed body cavity it has been established that this cavity originates in the embryo from a pair of alimentary diverticula, and the cavities resulting from the formation of these diverticula may remain distinct, the adjacent walls of the two cavities fusing to form a dorsal and a ventral mesentery.

It is fairly certain that some groups, e.g. the Tracheata, with imperfectly developed body cavities are descended from ancestors which were provided with well developed body cavities, but how far this is universally the case cannot as yet be definitely decided, and for additional information on this subject the


624 CIIORDATA.


reader is referred to pp. 355 360 and to the literature there referred to.

In the Chaetopoda and the Tracheata the body cavity arises as a series of paired compartments in the somites of mesoblast (fig. 350) which have at first a very restricted extension on the ventral side of the body, but eventually extend dorsalwards and vcntralwards till each cavity is a half circle investing the alimentary tract ; on the dorsal side the walls separating the two



FIG. 350. LONGITUDINAL SECTION THROUGH AN EMBRYO OF AGELINA LABYRINTHICA.

The section is taken slightly to one side of the middle line so as to shew the relation of the mesoblastic somites to the limbs. In the interior are seen the yolk segments and their nuclei.

i 16. the segments ; pr.l. procephalic lobe ; do. dorsal integument.

half cavities usually remain as the dorsal mesentery, while ventrally they are in most instances absorbed. The transverse walls, separating the successive compartments of the body cavity, generally become more or less perforated.

Chordata. In the Chordata the primitive body cavity is cither directly formed from a pair of alimentary diverticula (Cephalochorda) (fig. 3) or as a pair of spaces in the mesoblastic plates of the two sides of the body (fig. 20).

As already explained (pp. 294 300) the walls of the dorsal sections of the primitive body cavity soon become separated from those of the ventral, and becoming segmented constitute the muscle plates, while the cavity within them becomes


I


THE BODY CAVITY.


625


the


obliterated : they are dealt with in a separate chapter. The ventral part of the primitive cavity alone constitutes the permanent body cavity.

The primitive body cavity in the lower Vertebrata is at first continued forwards into the region of the head, but on the formation of the visceral clefts the cephalic section of the body cavity becomes divided into a series of separate compartments. Subsequently these sections of the body cavity become obliterated ; and, since their walls give rise to muscles, they may probably be looked upon as equivalent to the dorsal sections of the body cavity in the trunk, and will be treated of in connection with the muscular system.

As a result of its mode of origin the body cavity in trunk is at first divided into two lateral halves ; and part of the mesoblast lining it soon becomes distinguished as a special layer of epithelium, known as the peritoneal epithelium, of which the part bounding the outer wall forms the somatic layer, and that bounding the inner wall the splanchnic layer. Between the two splanchnic layers is placed the gut. On the ventral side, in the region of the permanent gut, the two halves of the body cavity soon coalesce, the septum between them becoming absorbed, and the splanchnic layers of epithelium of the two sides uniting at the ventral side of the gut, and the somatic layers at the median ventral line of the body wall (fig.



In the lower Vertebrata the body cavity is originally present even in the post-anal region of the trunk, but usually atrophies early, frequently before the two halves coalesce.

On the dorsal side of the gut the B. III.


FIG. 351. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNGER THAN

28 F.

sp.c. spinal canal ; W. white matter of spinal cord ; pr. posterior nerve-roots ; cA. notochord ; x. sub-notochordal rod ; ao. aorta ; nip. muscle-plate ; nip 1 , inner layer of muscle-plate already converted into muscles; Vr. rudiment of vertebral body ; si. segmental tube ; sd. segmental duct ; sp.v. spiral valve ; v. subintestinal vein ; p.o. primitive generative cells.

40


626 ABDOMINAL PORES.


two halves of the body cavity never coalesce, but eventually the splanchnic layers of epithelium of the two sides, together with a thin layer of interposed mesoblast, form a delicate membrane, known as the mesentery, which suspends the gut from the dorsal wall of the body (figs. 119 and 351). On the dorsal side the epithelium lining of the body cavity is usually more columnar than elsewhere (fig. 351), and its cells partly form a covering for the generative organs, and partly give rise to the primitive germinal cells. This part of the epithelium is often known as the germinal epithelium.

Over the greater part of the body cavity the lining epithelium becomes in the adult intimately united with a layer of the subjacent connective tissue, and constitutes with it a special lining membrane for the body cavity, known as the peritoneal membrane.

Abdominal pores. In the Cyclostomata, the majority of the Elasmobranchii, the Ganoidei, a few Teleostei, the Dipnoi, and some Sauropsida (Chelonia and Crocodilia) the body cavity is in communication with the exterior by a pair of pores, known as abdominal pores, the external openings of which are usually situated in the cloaca 1 .

The ontogeny of these pores has as yet been but very slightly investigated. In the Lamprey they are formed as apertures leading from the body cavity into the excretory section of the primitive cloaca. This section would appear from Scott's (No. 87) observations to be derived from part of the hypoblastic cloacal section of the alimentary tract.

In all other cases they are formed in a region which appears to belong to the epiblastic region of the cloaca ; and from my observations on Elasmobranchs it may be certainly concluded that they are formed there in this group. They may appear as perforations (i) at the apices of papilliform prolongations of the body cavity, or (2) at the ends of cloacal pits directed from the exterior towards the body cavity, or (3) as simple slit-like openings.

Considering the difference in development between the abdominal pores of most types, and those of the Cyclostomata, it is open to doubt whether these two types of pores are strictly homologous.

In the Cyclostomata they serve for the passage outwards of the generative products, and they also have this function in some of the few Teleostei in which they are found ; and Gegenbaur and Bridge hold that the primitive mode of exit of the generative products, prior to the development of the Miillerian ducts, was probably by means of these pores. I have elsewhere

1 For a full account of these structures the reader is referred to T. W. Bridge, "Pori Abdominales of Vertebrata. " Journal of Anat. and Physiol. , Vol. XIV., 1879.


THE BODY CAVITY.


627



suggested that the abdominal pores are perhaps remnants of the openings of segmental tubes ; there does not however appear to be any definite evidence in favour of this view, and it is more probable that they may have arisen as simple perforations of the body wall.

Pericardial cavity, pleural cavities, and diaphragm.

In all Vertebrata the heart is at first placed in the body cavity (fig. 353 A), but the part of the body cavity containing it afterwards becomes separated as a distinct cavity known as the pericardial cavity. In Elasmobranchii, Acipenser, etc. a passage is however left between the pericardial cavity and the body cavity ; and in the Lamprey a separation between the two cavities does not occur during the Ammoccete stage. In Elasmobranchii the pericardial cavity becomes established as a distinct space in front of the body cavity in the following way. When the two ductus Cuvieri, leading transversely from the sinus venosus to the cardinal veins, become developed, a horizontal septum, shewn on the right side in fig. 352, is formed to support them, stretching across from the splanchnic to the somatic side of the body cavity, and dividing the body cavity (fig. 352) in this part into (i) a dorsal section formed of a right and left division constituting the true body cavity (pp), and (2) a ventral part the pericardial cavity (pc). The septum is at first of a very small longitudinal extent, so that both in front and behind it (fig. 352 on the left side) the dorsal and ventral sections of the body cavity are in free communication. The septum soon however becomes prolonged, and ceasing to be quite horizontal, is directed obliquely upwards and forwards till it meets the dorsal wall of the body

40 2


-ht


FIG. 352. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNGER THAN 28 F.

The figure shews the separation of the body cavity from the pericardial cavity by a horizontal septum in which runs the ductus Cuvieri ; on the left side is seen the narrow passage which remains connecting the two cavities.

sp.c. spinal canal ; w. white matter of spinal cord ; pr. commissure connecting the posterior nerve-roots ; ch. notochord ; x. sub-notochordal rod ; ao. aorta ; sv. sinus venosus ; cav. cardinal vein ; ht. heart ; pp. body cavity ; pc. pericardial cavity ; as. solid oesophagus ; /. liver ; nip. muscle-plate.


628 THE PERICARDIAL CAVITY.

Anteriorly all communication is thus early shut off between the body cavity and the pericardial cavity, but the two cavities still open freely into each other behind.

The front part of the body cavity, lying dorsal to the pericardial cavity, becomes gradually narrowed, and is wholly obliterated long before the close of embryonic life, so that in adult Elasmobranch Fishes there is no section of the body cavity dorsal to the pericardial cavity. The septum dividing the body cavity from the pericardial cavity is prolonged backwards, till it meets the ventral wall of the body at the point where the liver is attached by its ventral mesentery (falciform ligament). In this way the pericardial cavity becomes completely shut off from the body cavity, except, it would seem, for the narrow communications found in the adult. The origin of these communications has not however been satisfactorily worked out.

The septum between the pericardial cavity and the body cavity is attached on its dorsal aspect to the liver. It is at first nearly horizontal, but gradually assumes a more vertical position, and then, owing to the obliteration of the primitive anterior part of the body cavity, appears to mark the front boundary of the body cavity. The above description of the mode of formation of the pericardial cavity, and the explanation of its relations to the body cavity, probably holds true for Fishes generally.

In the higher types the earlier changes are precisely the same as those in Elasmobranch Fishes. The heart is at first placed within the body cavity attached to the ventral wall of the gut by a mesocardium (fig. 353 A). A horizontal septum is then formed, in which the ductus Cuvieri are placed, dividing the body cavity for a short distance into a dorsal (/./) and ventral (p.c) section (fig. 353 B). In Birds and Mammals, and probably also in Reptilia, the ventral and dorsal parts of the body cavity are at first in free communication both in front of and behind this septum. This is shewn for the Chick in fig- 353 A an d B, which are sections of the same chick, A being a little in front of B. The septum is soon continued forwards so as completely to separate the ventral pericardial and the dorsal body cavity in front, the pericardial cavity extending at this period considerably further forwards than the body cavity.

Since the horizontal septum, by its mode of origin, is


THE BODY CAVITY.


629


necessarily attached to the ventral side of the gut, the dorsal part of the primitive body space is divided into two halves by a median vertical septum formed of the gut and its mesentery (fig- 353 B). Posteriorly the horizontal septum grows in a slightly ventral direction along the under surface of the liver (fig- 354)j till it meets the abdominal wall of the body at the insertion of the falciform ligament, and thus completely shuts off the pericardial cavity from the body cavity. The horizontal septum forms, as is obvious from the above description, the dorsal wall of the pericardial cavity 1 .

A. B.



FIG. 353. TRANSVERSE SECTIONS THROUGH A CHICK EMBRYO WITH TWENTYONE MESOBLASTIC SOMITES TO SHEW THE FORMATION OF THE PERICARDIAI, CAVITY, A. BEING THE ANTERIOR SECTION.

p.p. body cavity; p.c. pericardial cavity; al. alimentary cavity ; au. auricle; v. ventricle; s.v. sinus venosus; d.c. ductus Cuvieri ; ao. aorta; nip. muscle-plate; me. medullary cord.

With the complete separation of the pericardial cavity from the body cavity, the first period in the development of these parts is completed, and the relations of the body cavity to the

1 Kolliker's account of this septum, which he calls the mesocardium laterale (No. 298, p. 295), would seem to imply that in Mammals it is completed posteriorly even before the formation of the liver. I doubt whether this takes place quite so early as he implies, but have not yet determined its exact period by my own observations.


630


THE PERICARDIAL CAVITY.


pericardial cavity become precisely those found in the embryos of Elasmobranchii. The later changes are however very different. Whereas in Fishes the right and left sections of the body cavity dorsal to the pericardial cavity soon atrophy, in the higher types, in correlation with the relatively backward situation of the heart, they rapidly become larger, and receive the lungs which soon sprout out from the throat.

The diverticula which form the lungs grow out into the splanchnic mesoblast, in front of the body cavity ; but as they grow, they extend into the two anterior compartments of the body cavity, each attached by its mesentery to the mesentery of the gut (fig. 354, lg). They soon moreover extend beyond the region of the pericardium into the undivided body cavity behind. This holds not only for the embryos of the Amphibia and Sauropsida, but also for those of Mammalia.

To understand the further

rrianfrps in rhp nerirardial ravitv FlG> 354- SECTION THROUGH

pencaraiai cavity THECARDIACREGION OF AN EMBRYO

it is necessary to bear in mind its OF LACERTA MURALIS OF 9 MM. TO

, ,. ,, ,. . . SHEW THE MODE OF FORMATION OF

relations to the adjoining parts. THE PERICARDIAL CAVITY.



'-/it


It lies at this period completely ventral to the two anterior pro


ht. heart ; pc. pericardial cavity ; al. alimentary tract; lg. lung; /. liver ; pp. body cavity ; md. open longations of the body Cavity COn- end of Mullerian duct ; wd. Wolffian . . duct; vc. vena cava inferior; ao.

taming the lungs (fig. 354). Its aorta; ch. notochord; me. medullary

dorsal wall is attached to the gut, cord>

and is continuous with the mesentery of the gut passing to the dorsal abdominal wall, forming the posterior mediastinum of human anatomy.

The changes which next ensue consist essentially in the enlargement of the sections of the body cavity dorsal to the pericardial cavity. This enlargement takes place partly by the elongation of the posterior mediastinum, but still more by the two divisions of the body cavity which contain the lungs extending themselves ventrally round the outside of the peri


THE BODY CAVITY.


631


cardial cavity. This process is illustrated by fig. 355, taken from an embryo Rabbit. The two dorsal sections of the body cavity (pl.p] finally extend so as completely to envelope the pericardial cavity (pc\ remaining however separated from each other below by a lamina extending from the ventral wall of the pericardial cavity to the body wall, which forms the anterior mediastinum of human anatomy.

By these changes the pericardial cavity is converted into a closed bag, completely surrounded at its sides by the two lateral halves of the body cavity, which were primitively placed


SJ3. C.



FIG. 355. SECTION THROUGH AN ADVANCED EMBRYO OF A RABBIT TO SHEW HOW THE PERICARDIAL CAVITY BECOMES SURROUNDED BY THE PLEURAL CAVITIES.

ht. heart; pc. pericardial cavity; //./ pleural cavity; Ig. lung; al. alimentary tract; ao. dorsal aorta; ch. notochord; rp. rib; st. sternum; sp.c. spinal cord.

dorsally to it. These two sections of the body cavity, which in Amphibia and Sauropsida remain in free communication with the undivided peritoneal cavity behind, may, from the fact of their containing the lungs, be called the pleural cavities.

In Mammalia a further change takes place, in that, by the formation of a vertical partition across the body cavity, known as the diaphragm, the pleural cavities, containing the lungs,


632 THE VASCULAR SYSTEM.

become isolated from the remainder of the body or peritoneal cavity. As shewn by their development the so-called pleurae or pleural sacks are simply the peritoneal linings of the anterior divisions of the body cavity, shut off from the remainder of the body cavity by the diaphragm.

The exact mode of formation of the diaphragm is not fully made out ; the account of it recently given by Cadiat (No. 491) not being in my opinion completely satisfactory.

BIBLIOGRAPHY.

(491) M. Cadiat. "Du developpement de la partie cephalothoracique de 1'embryon, de la formation du diaphragme, des pleures, du pericarde, du pharynx et de 1'cesophage." Journal de F Anatomic et de la Physiologic, Vol. xiv. 1878.


Vascular System.

The actual observations bearing on the origin of the vascular system, using the term to include the lymphatic system, are very scanty. It seems probable, mainly it must be admitted on d priori grounds, that vascular and lymphatic systems have originated from the conversion of indefinite spaces, primitively situated in the general connective tissue, into definite channels. It is quite certain that vascular systems have arisen independently in many types ; a very striking case of the kind being the development in certain parasitic Copepoda of a closed system of vessels with a red non-corpusculated blood (E. van Beneden, Heider), not found in any other Crustacea. Parts of vascular systems appear to have arisen in some cases by a canalization of cells.

The blood systems may either be closed or communicate with the body cavity. In cases where the primitive body cavity is atrophied or partially broken up into separate compartments (Insecta, Mollusca, Discophora, etc.) a free communication between the vascular system and the body cavity is usually present ; but in these cases the communication is no doubt secondary. On the whole it would seem probable that the vascular system has in most instances arisen independently of the body cavity, at least in types where the body cavity is


THE VASCULAR SYSTEM. 633

present in a well-developed condition. As pointed out by the Hertwigs, a vascular system is always absent where there is not a considerable development of connective tissue.

As to the ontogeny of the vascular channels there is still much to be made out both in Vertebrates and Invertebrates.

The smaller channels often rise by a canalization of cells. This process has been satisfactorily studied by Lankester in the Leech 1 , and may easily be observed in the blastoderm of the Chick or in the epiploon of a newlyborn Rabbit (Schafer, Ranvier). In either case the vessels arise from a network of cells, the superficial protoplasm and part of the nuclei giving rise to the walls, and the blood-corpuscles being derived either from nucleated masses set free within the vessels (the Chick) or from blood-corpuscles directly differentiated in the axes of the cells (Mammals).

Larger vessels would seem to be formed from solid cords of cells, the central cells becoming converted into the corpuscles, and the peripheral cells constituting the walls. This mode of formation has been observed by myself in the case of the Spider's heart, and by other observers in other Invertebrata. In the Vertebrata a more or less similar mode of formation appears to hold good for the larger vessels, but further investigations are still required on this subject. Gotte finds that in the Frog the larger vessels are formed as longitudinal spaces, and that the walls are derived from the indifferent cells bounding these spaces, which become flattened and united into a continuous layer.

The early formation of vessels in the Vertebrata takes place in the splanchnic mesoblast ; but this appears due to the fact that the circulation is at first mainly confined to the vitelline region, which is covered by splanchnic mesoblast.

The Heart.

The heart is essentially formed as a tubular cavity in the splanchnic mesoblast, on the ventral side of the throat, immediately behind the region of the visceral clefts. The walls of this cavity are formed of two layers, an outer thicker layer, which has at first only the form of a half tube, being incomplete on its dorsal side; and an inner lamina formed of delicate flattened cells. The latter is the epithelioid lining of the heart, and the cavity it contains the true cavity of the heart. The outer layer gives rise to the muscular wall and peritoneal covering of the heart. Though at first it has only the form of a half tube (fig.

1 "Connective and vasifactive tissues of the Leech." Quart. J. of Micr. Science, Vol. XX. 1880.


634


THE HEART.


356), it soon becomes folded in on the dorsal side so as to form for the heart a complete muscular wall. Its two sides, after thus meeting to complete the tube of the heart, remain at first continuous with the splanchnic mesoblast surrounding the throat, and form a provisional mesentery the mesocardium which attaches the heart to the ventral wall of the throat. The superficial stratum of the wall of the heart differentiates itself as the peritoneal covering. The inner epithelioid tube takes its origin at the time when the general cavity of the heart is being formed by the separation of the splanchnicmesoblastfrom the hypoblast. During this process (fig. 357) a layer of mesoblast remains close to the hypoblast, but connected with the main mass



FIG. 356. SECTION THROUGH THE DEVELOPING HEART OF AN EMBRYO OF AN ELASMOBRANCH (Pristiurus).

al. alimentary tract ; sp. splanchnic mesoblast ; so. somatic mesoblast ; ht. heart.



FIG. 357. TRANSVERSE SECTION THROUGH THE POSTERIOR PART OF THE HEAD OF AN EMBRYO CHICK OF THIRTY HOURS.

hb. hind-brain; vg. vagus nerve; ep. epiblast; ch. notochorcl ; x. thickening of hypoblast (possibly a rudiment of the sub-notochordal rod) ; al. throat; ht. heart; //. body cavity; so. somatic mesoblast; sf. splanchnic mesoblast; Ay. hypoblast.


THE VASCULAR SYSTEM.


635


of the mesoblast by protoplasmic processes. A second layer next becomes split from the splanchnic mesoblast, connected with the first layer by the above-mentioned protoplasmic processes. These two layers form together the epithelioid lining of the heart ; between them is the cavity of the heart, which soon loses the protoplasmic trabeculae which at first traverse it. The cavity of the heart may thus be described as being formed by a hollowing out of the splanchnic mesoblast, and resembles in its mode of origin that of other large vascular trunks.

The above description applies only to the development of the heart in those types in which it is formed at a period after the throat has become a closed tube (Elasmobranchii, Amphibia, Cyclostomata, Ganoids (?)). In a number of other cases, in which the heart is formed before the conversion of the throat into a closed tube, of which the most notable is that of Mammals (Hensen, Gotte, Kolliker), the heart arises as two independent

A.



B.


mes fir



FIG. 358. TRANSVERSE SECTION THROUGH THE HEAD OF A RABBIT OF THE

SAME AGE AS FIG. 144 B. (From Kolliker.) B is a more highly magnified representation of part of A.

rf. medullary groove; mp. medullary plate; riv. medullary fold; h. epiblast ; dd. hypoblast; dd' . notochordal thickening of hypoblast; sp. undivided mesoblast; ^.somatic mesoblast; dfp. splanchnic mesoblast; ph. pericardial section of body cavity; ahh. muscular wall of heart; ihh. epithelioid layer of heart; vies, lateral undivided mesoblast ; sw. part of the hypoblast which will form the ventral wall of the pharynx.


636


THE HEART.


tubes (fig. 358), which eventually coalesce into an unpaired structure.

In Mammals the two tubes out of which the heart is formed appear at the sides of the cephalic plates, opposite the region of the mid- and hindbrain (fig. 358). They arise at a time when the lateral folds which form the ventral wall of the throat are only just becoming visible. Each half of the heart originates in the same way as the whole heart in Elasmobranchii, etc. ; and the layer of the splanchnic mesoblast, which forms the muscular wall for each part (ahh), has at first the form of a half tube open below to the hypoblast.

On the formation of the lateral folds of the splanchnic walls, the two halves of the heart become carried inwards and downwards, and eventually



FlG. 359. TWO DIAGRAMMATIC SECTIONS THROUGH THE REGION OF THE HIND-BRAIN OF AN EMBRYO CHICK OF ABOUT 36 HOURS ILLUSTRATING THE FORMATION OF THE HEART.

fib. hind-brain ; nc. notochord ; E. epiblast ; so. somatopleure ; sp. splanchnopleure ; d. alimentary tract ; hy. hypoblast ; hs. heart ; of. vitelline veins.


THE VASCULAR SYSTEM.


637


meet on the ventral side of the throat. For a short time they here remain distinct, but soon coalesce into a single tube.

In Birds, as in Mammals, the heart makes its appearance as two tubes, but arises at a period when the formation of the throat is very much more advanced than in the case of Mammals. The heart arises immediately behind the point up to which the ventral wall of the throat is established and thus has at first a A -shaped form. At the apex of the A , which forms the anterior end of the heart, the two halves are in contact (fig. 357), though they have not coalesced; while behind they diverge to be continued as the vitelline veins. As the folding in of the throat is continued backwards the two limbs of the heart are brought together and soon coalesce from before backwards into a single structure. Fig. 359 A and B shews the heart during this process. The two halves have coalesced anteriorly (A) but are still widely separated behind (B). In Teleostei the heart is formed as in Birds and Mammals by the coalescence of two tubes, and it arises before the formation of the throat.

The fact that the heart arises in so many instances as a double tube might lead to the supposition that the ancestral Vertebrate had two tubes in the place of the present unpaired heart.

The following considerations appear to me to prove that this conclusion cannot be accepted. If the folding in of the splanchnopleure to form the throat were deferred relatively to the formation of the heart, it is clear that a modification in the development of the heart would occur, in that the two halves of the heart would necessarily be formed widely apart, and only eventually united on the folding in of the wall of the throat. It is therefore possible to explain the double formation of the heart without having recourse to the above hypothesis of an ancestral Vertebrate with two hearts. If the explanation just suggested is the true one the heart should only be formed as two tubes when it arises prior to the formation of the throat, and as a single tube when formed after the formation of the throat. Since this is invariably found to be so, it may be safely concluded that the formation of the heart as two cavities is a secondary mode of development, which has been brought about by variations in the period of the closing in of the wall of the throat.

The heart arises continuously with the sinus venosus, which in the Amniotic Vertebrata is directly continued into the vitelline veins. Though at first it ends blindly in front, it is very soon connected with the foremost aortic arches.


638 THE HEART.


The simple tubular heart, connected as above described, grows more rapidly than the chamber in which it is contained, and is soon doubled upon itself, acquiring in this way an S-shaped curvature, the posterior portion being placed dorsally, and the anterior ventrally. A constriction soon appears between the dorsal and ventral portions.

The dorsal section becomes partially divided off behind from the sinus venosus, and constitutes the relatively thin-walled auricular section of the heart; while the ventral portion, after becoming distinct anteriorly from a portion continued forwards from it to the origin of the branchial arteries, which may be called the truncus arteriosus, acquires very thick spongy muscular walls, and becomes the ventricular division of the heart.

The further changes in the heart are but slight in the case of the Pisces. A pair of simple membranous valves becomes established at the auriculoventricular orifice, and further changes take place in the truncus arteriosus. This part becomes divided in Elasmobranchii, Ganoidei, and Dipnoi into a posterior section, called the conus arteriosus, provided with a series of transverse rows of valves, and an anterior section, called the bulb us arteriosus, not provided with valves, and leading into the branchial arteries. In most Teleostei (except Butirinus and a few other forms) the conus arteriosus is all but obliterated, and the anterior row of its valves alone preserved ; and the bulbus is very much enlarged 1 .

In the Dipnoi important changes in the heart are effected, as compared with other Fishes, by the development of true lungs. Both the auricular and ventricular chamber may be imperfectly divided into two, and in the conus a partial longitudinal septum is developed in connection with a longitudinal row of valves 2 .

In Amphibia the heart is in many respects similar to that of the Dipnoi. Its curvature is rather that of a screw than of a simple S. The truncus arteriosus lies to the left, and is continued into the ventricle which lies ventrally and more to the right, and this again into the dorsally placed auricular section.

After the heart has reached the piscine stage, the auricular section (Bombinator) becomes prolonged into a right and left auricular appendage^ A septum next grows from the roof of the auricular portion of the heart

1 Vide Gegenbaur, "Zur vergleich. Anat. d. Herzens." Jenaische Zeit., Vol. n. 1866, and for recent important observations, J. E. V. Boas, "Ueb. Herz u. Arterienbogenbei Ceratodenu. Protopterus," and " Ueber d. Conus arter. b. Butirinus, etc.," Morphol. Jahrb., Vol. VI. 1880.

2 Boas holds that the longitudinal septum is formed by the coalescence of a row of longitudinal valves, but this is opposed to Lankester's statements, "On the hearts of Ceratodus, Protopterus and Chimaera, etc. Zool. Trans. Vol. x. 1879.


THE VASCULAR SYSTEM. 639


obliquely backwards and towards the left, and divides it in two chambers ; the right one of which remains continuous with the sinus venosus, while the left one is completely shut off from the sinus, though it soon enters into communication with the newly established pulmonary veins. The truncus arteriosus 1 is divided into a posterior conus arteriosus (pylangium) and an anterior bulbus (synangium). The former is provided with a proximal row of valves at its ventricular end, and a distal row at its anterior end near the bulbus. It is also provided with a longitudinal septum, which is no doubt homologous with the septum in the conus arteriosus of the Dipnoi. The bulbus is well developed in many Urodela, but hardly exists in the Anura.

In the Amniota further changes take place in the heart, resulting in the abortion of the distal rows of valves of the conus arteriosus 2 , and in the splitting up of the whole truncus arteriosus into three vessels in Reptilia, and two in Birds and Mammals, each opening into the ventricular section of the heart, and provided with a special set of valves at its commencement. In Birds and Mammals the ventricle becomes moreover completely divided into two chambers, each communicating with one of the divisions of the primitive truncus, known in the higher types as the systemic and pulmonary aortae. The character of the development of the heart in the Amniota will be best understood from a description of what takes place in the Chick.

In Birds the originally straight heart (fig. 109) soon becomes doubled up upon itself. The ventricular portion becomes placed on the ventral and right side, while the auricular section is dorsal and to the left. The two parts are separated from each other by a slight constriction known as the canalis auricularis. Anteriorly the ventricular cavity is continued into the truncus, and the venous or auricular portion of the heart is similarly connected behind with the sinus venosus. The auricular appendages grow out from the auricle at a very early period. The general appearance of the heart, as seen from the ventral side on the fourth day, is shewn in fig. 360. Although the external divisions of the heart are well marked even before this stage, it is not till the end of the third day that the internal partitions become apparent ; and, contrary to what might have been anticipated from the evolution of these parts in the lower types, the ventricular septum is the first to be established.

1 For a good description of the adult heart vide Huxley, Article "Amphibia," in the Encyclopedia Britannic a.

2 It is just possible that the reverse may be true, vide note on p. 640. If however, as is most probable, the statement in the text is correct, the valves at the mouth of the ventricle in Teleostei are not homologous with those of the Amniota ; the former being the distal rov/ of the valves of the conus, the latter the proximal.



640 THE HEART OF AVES.

It commences on the third day as a crescentic ridge or fold springing from the convex or ventral side of the rounded ventricular portion of the heart, and on the fourth day grows rapidly across the ventricular cavity towards the concave or dorsal side. It thus forms an incomplete longitudinal partition, extending from the canalis auricularis to the commencement of the truncus arteriosus, and dividing the twisted ventricular tube into two somewhat curved canals, one more to the left and above, the other to

the right and below. These commu- A ^) ) CA

nicate with each other, above the free edge of the partition, along its whole length.

Externally the ventricular portion as yet shews no division into two parts.

By the fifth day the venous end of the heart, though still lying somewhat to the left and above, is placed as far FIG. 360. HEART OF A CHICK ON

forwards as the arterial end, the whole THE FOURTH DAY OF INCUBATION

VIEWED FROM THE VENTRAL SURFACE.

organ appearing to be drawn together.

The ventricular septum is complete. L ?.- lef t a , uricular appendage; C.A.

, e .. , . , , canahs auricularis ; v. ventricle ; b. trun The apex of the ventricles becomes cus arteriosus.

more and more pointed. In the auricular portion a small longitudinal fold appears as the rudiment of the auricular septum, while in the canalis auricularis, which is now at its greatest length, there is also to be seen a commencement of the valvular structures tending to separate the cavity of the auricles from those of the ventricles.

About the io6th hour, a septum begins to make its appearance in the truncus arteriosus in the form of a longitudinal fold, which according to Tonge (No. 495) starts at the end of the truncus furthest removed from the heart. It takes origin from the wall of the truncus between the fourth and fifth pairs of arches, and grows downwards in such a manner as to divide the truncus into two channels, one of which leads from the heart to the third and fourth pairs of arches, and the other to the fifth pair. Its course downwards is not straight but spiral, and thus the two channels into which it divides the truncus arteriosus wind spirally the one round the other.

At the time when the septum is first formed, the opening of the truncus arteriosus into the ventricles is narrow or slit-like, apparently in order to prevent the flow of the blood back into the heart. Soon after the appearance of the septum, however, semilunar valves (Tonge, No. 495) are developed from the wall of that portion of the truncus which lies between the free edge of the septum and the cavity of the ventricles 1 .

1 If Tonge is correct in his statement that the semilunar valves develop at some distance from the mouth of the ventricle, it would seem possible that the portion of the truncus between them and the ventricle ought to be regarded as the embryonic conus arteriosus, and that the distal row of valves of the conus (and not the proximal as suggested above, p. 639) has been preserved in the higher types.


THE VASCULAR SYSTEM.


641


The ventral and the dorsal pairs of valves are the first to appear : the former as two small solid prominences separated from each other by a narrow groove ; the latter as a single ridge, in the centre of which is a prominence indicating the point where the ridge will subsequently become divided into two. The outer valves appear opposite each other, at a considerably later period.

As the septum grows downwards towards the heart, it finally reaches the position of these valves. One of its edges then passes between the two ventral valves, and the other unites with the prominence on the dorsal valve-ridge. At the same time the growth of all the parts causes the valves to appear to approach the heart, and thus to be placed quite at the top of the ventricular cavities. The free edge of the septum of the truncus now

A. B.



FlG. 361. TWO VIEWS OF THE HEART OF A CHICK UPON THE FIFTH DAY

OF INCUBATION.

A. from the ventral, B. from the dorsal side.

La. left auricular appendage; r.a. right auricular appendage ; r.v. right ventricle; l.v. left ventricle; b. truncus arteriosus.

fuses with the ventricular septum, and thus the division of the truncus into two separate channels, each provided with three valves, and each communicating with a separate side of the heart, is complete ; the position of the valves not being very different from that in the adult heart.

That division of the truncus which opens into the fifth pair of arches is the one which communicates with the right ventricle, while that which opens into the third and fourth pairs communicates with the left ventricle. The former becomes the pulmonary artery, the latter the commencement of the systemic aorta.

The external constriction actually dividing the truncus into two vessels does not begin to appear till the septum has extended some way back towards the heart.

The semilunar valves become pocketed at a period considerably later than their first formation (from the H7th to the,i65th hour) in the order of their appearance.

At the end of the sixth day, and even on the fifth day (figs. 361 and 362), the appearance of the heart itself, without reference to the vessels which come from it, is not very dissimilar from that of the adult. The original


B. III.


4 1


642


THE HEART OF MAMMALIA.


r.a



l.v


FIG. 362. HEART OF A CHICK UPON THE SIXTH DAY OF INCUBATION, FROM THE VENTRAL SURFACE.

La. left auricular appendage ; r,a. right auricular appendage ; r.v. right ventricle ; l.v. left ventricle ; b. truncus arteriosus.


protuberance to the right now forms the apex of the ventricles, and the two auricular appendages are placed at the anterior extremity of the heart. The most noticeable difference (in the ventral view) is the still externally undivided condition of the truncus arteriosus.

The subsequent changes which the heart undergoes are concerned more with its internal structure than with its external shape. Indeed, during the next three days, viz. the eighth, ninth, and tenth, the external form of the heart remains nearly unaltered.

In the auricular portion, however, the septum which commenced on the fifth day becomes now more conspicuous. It is placed vertically, and arises from the ventral wall ; commencing at the canalis auricularis and proceeding towards the opening into the sinus venosus.

This latter structure gradually becomes reduced so as to become a special appendage of the right auricle. The inferior vena cava

enters the sinus obliquely from the right, so that its blood has a tendency to flow towards the left auricle of the heart, which is at this time the larger of the two.

The valves between the ventricles and auricles are now well developed, and it is about this time that the division of the truncus arteriosus into the aorta and pulmonary artery becomes visible from the exterior.

By the eleventh to the thirteenth day the right auricle has become as large as the left, and the auricular septum much more complete, though there is still a small opening, the foramen ovale, by which the two cavities communicate with each other.

The most important feature in which the development of the Reptilian heart differs from that of Birds is the division of the truncus into three vessels, instead of two. The three vessels remain bound up in a common sheath, and appear externally as a single trunk. The vessel not represented in Birds is that which is continued into the left aortic arch.

In Mammals the early stages in the development of the heart present no important points of difference from those of Aves. The septa in the truncus, in the ventricular, and in the auricular cavities are formed, so far as is known, in the same way and at the same relative periods in both groups. In the embryo Man, the Rabbit, and other Mammals the division of the ventricles is made apparent externally by a deep cleft, which, though evanescent in these forms, is permanent in the Dugong.

The attachment of the auriculo-ventricular valves to the wall of the ventricle, and the similar attachment of the left auriculo-ventricular valves in Birds, have been especially studied by Gegenbaur and Bernays (No. 492),


ARTERIAL SYSTEM. 643


and deserve to be noticed. In the primitive state the ventricular walls have throughout a spongy character ; and the auriculo-ventricular valves are simple membranous projections like the auriculo-ventricular valves of Fishes. Soon however the spongy muscular tissue of both the ventricular and auricular walls, which at first pass uninterruptedly the one into the other, grows into the bases of the valves, which thus become in the main muscular projections of the walls of the heart. As the wall of the ventricle thickens, the muscular trabeculas, connected at one end with the valves, remain at the other end united with the ventricular wall, and form special bands passing between the two. The valves on the other hand lose their muscular attachment to the auricular walls. This is the condition permanent in Ornithorhynchus. In higher Mammalia the ends of the muscular bands inserted into the valves become fibrous, from the development of intermuscular connective tissue, and the atrophy of the muscular elements. The fibrous parts now form the chordae tendinea?, and the muscular the musculi papillares.

The sinus venosus in Mammals becomes completely merged into the right auricle, and the systemic division of the truncus arteriosus is apparently not homologous with that in Birds.

In the embryos of all the Craniata the heart is situated very far forwards in the region of the head. This position is retained in Pisces. In Amphibia the heart is moved further back, while in all the Amniota it gradually shifts its position first of all into the region of the neck and finally passes completely within the thoracic cavity. The steps in the change of position may be gathered from figs. 109, in, and 118.

BIBLIOGRAPHY of the Heart.

(492) A. C. Bernays. " Entwicklungsgeschichte d. Atrioventricularklappen." Morphol. Jahrbuch,^o\. II. 1876.

(493) E. Gasser. " Ueber d. Entstehung d. Herzens beim Hiihn." Archiv f. mikr. Anat., Vol. xiv.

(494) A. Thomson. "On the development of the vascular system of the foetus of Vertebrated Animals." Edinb. New Phil. Journal, Vol. ix. 1830 and 1831.

(495) M. Tonge. "Observations on the development of the semilunar valves of the aorta and pulmonary artery of the heart of the Chick." Phil. Trans. CLIX. 1869.

Vide also Von Baer (291), Rathke (300), Hensen (182), Kolliker (298), Gotte (296), and Balfour (292).

Arterial System.

In the embryos of Vertebrata the arterial system consists of a forward continuation of the truncus arteriosus, on the ventral

41 2


644


ARTERIES OF PISCES.


side of the throat (figs. 363, abr, and 364, a), which, with a few exceptions to be noticed below, divides into as many branches on each side as there are visceral arches. These branches, after traversing the visceral arches, unite on the dorsal side of the throat into a common trunk on each side. This trunk (figs. 363 and 364) after giving off one (or more) vessels to the head (c and c] turns backv/ards, and bends in towards the middle line, close to its fellow, immediately below the notochord (figs. 21 and 116) and runs backwards in this situation towards the end of the tail. The two parallel trunks below the notochord fuse very early into a single trunk, the dorsal aorta (figs. 363, ad, and 364, a"}.



ttbr v "a,

FIG. 363. DIAGRAMMATIC VIEW OF THE HEAD OF AN EMBRYO TELEOSTEAN, WITH THE PRIMITIVE VASCULAR TRUNKS. (From Gegenbaur.)

a. auricle ; v. ventricle ; abr. branchial artery ; c'. carotid ; ad. dorsal aorta ; s. branchial clefts; sv. sinus venosus; dc. ductus Cuvieri; n. nasal pit

There is given off from each collecting trunk from the visceral arches, or from the commencement of the dorsal aorta, a subclavian artery to each of the anterior limbs ; from near the anterior end of the dorsal aorta a vitelline artery (or before the dorsal aortae have united a pair of arteries fig. 125, R of A and L of A) to the yolk-sack, which subsequently becomes the main visceral artery 1 ; and from the dorsal aorta opposite the hind limbs one (or two) arteries on each side the iliac arteries to the hind limbs ; from these arteries the allantoic arteries are given off in the higher types, which remain as the hypogastric arteries after the disappearance of the allantois.

The primitive arrangement of the arterial trunks is with a few modifications retained in Fishes. With the development of the gills the vessels to the arches become divided into two parts connected by a capillary system in the gill folds, viz. into the

1 In Mammalia the superior inesenteric artery arises from the vitelline artery, which may probably be regarded as a primitive crclinco-mescnteric artery.


ARTERIAL SYSTEM.


branchial arteries bringing the blood to the gills from the truncus arteriosus, and the branchial veins transporting it to the dorsal aorta. The branchial vessels to those arches which do not bear gills, either wholly or partially atrophy; thus in Elasmobranchii the mandibular trunk, which is fully developed in the embryo (fig. 193, \av}, atrophies, except for a small remnant bringing blood to the rudimentary gill of the spiracle from the branchial vein of the hyoid arch. In Ganoids the mandibular artery atrophies, but the hyoid is usually preserved. In Teleostei both mandibular 1 and hyoid arteries are absent in the adult, except that there is usually left a rudiment of the hyoid, supplying the pseudobranch, which is similar to the rudiment of the mandibular artery in Elasmobranchii. In Dipnoi the mandibular artery atrophies, but the hyoid is sometimes preserved (Protopterus), and sometimes lost.

In Fishes provided with a well developed air-bladder this organ receives arteries, which arise sometimes from the dorsal aorta, sometimes from the caeliac arteries, and sometimes from the dorsal section of the last (fourth) branchial trunk. The latter origin is found in Polypterus and Amia, and seems to have been inherited by the Dipnoi where the air-bladder forms a true lung.

The pulmonary artery of all the air-breathing Vertebrata is derived from the pulmonary artery of the Dipnoi.

In all the types above Fishes considerable changes are effected in the primitive arrangement of the arteries in the visceral arches.

In Amphibia the piscine condition is most nearly retained 2 . The mandibular artery is never developed, and the hyoid artery is imperfect, being only connected with the cephalic vessels and never directly joining the dorsal aorta. It is moreover developed later than the arteries of the true branchial arches behind. The subclavian arteries spring from the common trunks which unite to form the dorsal aorta.

In the Urodela there are developed, in addition to the hyoid,

1 The mandibular artery is stated by Gotte never to be developed in Teleostei, but is distinctly figured in Lereboullet (No. 71).

2 In my account of the Amphibia, Gotte (No. 296) has been followed.


646 ARTERIES OF THE AMNIOTA.

four branchial arteries. The three foremost of these at first supply gills, and in the Perennibranchiate forms continue to do so through life. The fourth does not supply a gill, and very early gives off, as in the Dipnoi, a pulmonary branch.

The hyoid artery soon sends forward a lingual artery from its ventral end, and is at first continued to the carotid which grows forward from the dorsal part of the first branchial vessel.

In the Caducibranchiata, where the gills atrophy, the following changes take place. The remnant of the hyoid is continued entirely into the lingual artery. The first branchial is mainly continued into the carotid and other cephalic branches, but a narrow remnant of the trunk, which originally connected it with the dorsal aorta, remains, forming what is known as a ductus Botalli. A rete mirabile on its course is the remnant of the original gill.

The second and third branchial arches are continued as simple trunks into the dorsal aorta, and the blood from the fourth arch mainly passes to the lungs, but a narrow ductus Botalli still connects this arch with the dorsal aorta.

In the Anura the same number of arches is present in the embryo as in the Urodela, all four branchial arteries supplying branchiae, but the arrangement of the two posterior trunks is different from that in the Urodela. The third arch becomes at a very early period continued into a pulmonary vessel, a relativelynarrow branch connecting it with the second arch. The fourth arch joins the pulmonary branch of the third. At the metamorphosis the hyoid artery loses its connection with the carotid, and the only part of it which persists is the root of the lingual artery. The first branchial artery ceases to join the dorsal aorta, and forms the root of the carotid : the so-called carotid gland placed on its course is the remnant of the gill supplied by it before the metamorphosis.

The second artery forms a root of the dorsal aorta. The third, as in all the Amniota, now supplies the lungs, and also sends off a cutaneous branch. The fourth disappears. The connection of the pulmonary artery with both the third and fourth branchial arches in the embryo appears to me clearly to indicate that this artery was primitively derived from the fonrtli arc/i as in the Urodela, and that its permanent connection


ARTERIAL SYSTEM.


647


with the third arch in the Anura and in all the Amniota is secondary.

In the Amniota the metamorphosis of the arteries is in all cases very similar. Five arches, viz. the mandibular, hyoid, and three branchial arches are always developed (fig. 364), but, owing to the absence of branchiae, never function as branchial arteries. Of these the main parts of the first two, connecting the truncus arteriosus with the collecting trunk into which the arterial arches fall, always disappear, usually before the complete development of the arteries in the posterior arches.

The anterior part of the collecting trunk into which these vessels fall is not obliterated when they disappear, but is on the contrary continued forwards as a vessel supplying the brain, homologous with that found in Fishes. It constitutes the internal carotid. Similarly the anterior part of the trunk from which the mandibular and hyoid arteries sprang is continued forwards as a small vessel 1 , which at first passes to the oral region and constitutes in Reptiles the lingual artery, homologous with the lingual artery of the Amphibia ; but in Birds and Mammals becomes more important, and is then known as the external carotid (fig. 125). By these changes the roots of the external and internal carotids spring respectively from the ventral and dorsal ends of the primitive third artery, i.e. the artery of the first branchial arch (fig. 365, c and c'} ; and thus this arterial arch persists in all types as the common carotid,



FIG. 364. DIAGRAM OF THE ARRANGEMENT OF THE ARTERIAL ARCHES IN AN EMBRYO OF ONE OF THE

AMNIOTA. (From Gegenbaur ; after RATHKE.)

a. ventral aorta; a", dorsal aorta; ' 2 > 3> 4> 5- arterial arches ; c. carotid artery.


1 His (No. 232) describes in Man two ventral continuations of the truncus arteriosus, one derived from the mandibular artery, forming the external maxillary artery, and one from the hyoid artery, forming the lingual artery. The vessel from which they spring is the external carotid. These observations of His will very probably be found to hold true for other types.


6 4 8


ARTERIAL ARCHES OF THE AMNIOTA.


and the basal part of the internal carotid. The trunk connecting the third arterial arch with the system of the dorsal aorta persists in some Reptiles (Lacertilia, fig. 366 A) as a ductus Botalli, but is lost in the remaining Reptiles and in Birds and Mammals (fig. 366 B, C, D). It disappears earliest in Mammals (fig. 365 C), later in Birds (fig. 365 B), and still later in the majority of Reptiles.

The fourth arch always continues to give rise, as in the Anura, to the system of the dorsal aorta.

In all Reptiles it persists on both sides (fig. 366 A and B), but with the division of the truncus arteriosus into three vessels



ad


FIG. 365. DEVELOPMENT OF THE GREAT ARTERIAL TRUNKS IN THE EMBRYOS OF A. A LIZARD ; B. THE COMMON FOWL; C. THE PIG. (From Gegenbaur; after Rathke.)

The first two arches have disappeared in all three. In A and B the last three are still complete, but in C the last two are alone complete.

/. pulmonary artery springing from the fifth arch, but still connected with the system of the dorsal aorta by a ductus Botalli; c. external carotid; <'. internal carotid; ad. dorsal aorta; a. auricle; v. ventricle; n. nasal pit; m, rudiment of fore-limb.

one of these, i.e. that opening furthest to the left side of the ventricle (e and d), is continuous with the right fourth arch, and also with the common carotid arteries (c) ; while a second springing from the right side of the ventricle is continuous with the left fourth arch (Ji and f). The right and left divisions of the fourth arch meet however on the dorsal side of the oesophagus to give origin to the dorsal aorta (g).

In Birds (fig. 366 C) the left fourth arch (h) loses its connection with the dorsal aorta, though the ventral part remains as


ARTERIAL SYSTEM.


649


the root of the left subclavian. The truncus arteriosus is moreover only divided into two parts, one of which is continuous with all the systemic arteries. Thus it comes about that in Birds the right fourth arch (e) alone gives rise to the dorsal aorta.

In Mammals (fig. 366 D) the truncus arteriosus is only divided into two, but the left fourth arch (>), instead of the right, is that continuous with the dorsal aorta, and the right fourth arch (/) is only continued into the right vertebral and right subclavian arteries.

The fifth arch always gives origin to the pulmonary artery (fig. 365, /) and is continuous with one of the divisions of the truncus arteriosus. In Lizards (fig. 366 A, i), Chelonians and Birds (fig. 366 C, i] and probably in Crocodilia, the right and left pulmonary arteries spring respectively from the right and left fifth arches, and during the greater part of embryonic life the parts of the fifth arches between the origins of the pulmonary arteries and the system of the dorsal aorta are preserved as ductus Botalli. These ductus Botalli persist for life in the Chelonia. In Ophidia (fig. 366 B, Ji) and Mammalia (fig. 366 D, m) only one of the fifth arches gives origin to the two pulmonary arteries, viz. that on the right side in Ophidia, and the left in Mammalia.

The ductus Botalli of the fifth arch (known in Man as the ductus arteriosus) of the side on which the pulmonary arteries are formed, may remain (e.g. in Man) as a solid cord connecting the common stem of the pulmonary aorta with the systemic aorta.

The main history of the arterial arches in the Amniota has been sufficiently dealt with, and the diagram, fig. 366, copied from Rathke, shews at a glance the character of the metamorphosis these arches undergo in the different types. It merely remains for me to say a few words about the subclavian and vertebral arteries.

The subclavian arteries in Fishes usually spring from the trunks connecting the branchial veins with the dorsal aorta. This origin, which is also found in Amphibia, is typically found in the embryos of the Amniota. In the Lizards this origin persists through life, but both subclavians spring from the right


650


ARTERIAL ARCHES OF THE AMNIOTA.


side. In most other types the origin of the subclavians is carried upwards, so that they usually spring from a trunk common to them and the carotids (arteria anonyma) (Birds and some Mammals); or the left one, as in Man and some other Mammals, arises from the systemic aorta just beyond the carotids. Various further modifications in the origin of the subclavians of the same general nature are found in Mammalia, A 13



FIG. 366. DIAGRAMS ILLUSTRATING THE METAMORPHOSIS OF THE ARTERIAL

ARCHES IN A LlZARD A, A SNAKE B, A BlRD C AND A MAMMAL D. (From Mivart ; after Rathke.)

A. a. internal carotid; b. external carotid ; c. common carotid; d. ductus Botalli between the third and fourth arches ; e. right aortic trunk ; /. subclavian ; g. dorsal aorta; h. left aortic trunk; i. pulmonary artery; k. rudiment of ductus Botalli between the pulmonary artery and the system of the dorsal aorta.

B. a. internal carotid; b. external carotid; c. common carotid; d. right aortic trunk; e. vertebral artery;/, left aortic trunk of dorsal aorta; h. pulmonary artery ; i. ductus Botalli of pulmonary artery.

C. a. internal carotid ; b. external carotid ; c. common carotid ; d. systemic aorta; e. fourth arch of right side (root of dorsal aorta);/, right subclavian; g. dorsal aorta; h, left subclavian (fourth arch of left side); i. pulmonary artery; k. and /. right and left ductus Botalli of pulmonary arteries.

D. a. internal carotid; b. external carotid; c. common carotid; d. systemic aorta; c. fourth arch of left side (root of dorsal aorta);/ dorsal aorta; g. left vertebral artery; h. left subclavian artery; i. right subclavian (fourth arch of right side); k. right vertebral; /. continuation of right subclavian; in. pulmonary artery; n. ductus Botalli of pulmonary artery.


THE VENOUS SYSTEM.


6 5 I


but they need not be specified in detail. The vertebral arteries usually arise in close connection with the subclavians, but in Birds they arise from the common carotids.

BIBLIOGRAPHY of the Arterial System.

(496) H. Rathke. " Ueb. d. Entwick. d. Arterien vv. bei d. Saugethiere von d. Bogen d. Aorta ausgehen." Miiller's Archiv, 1843.

(-197) H. Rathke. " Untersuchungen lib. d. Aortenwurzeln d. Saurier." Denkschriften d. k. Akad. Wien, Vol. XIII. 1857.

Vide also His (No. 232) and general works on Vertebrate Embryology.

TJie Venous System,.

The venous system, as it is found in the embryos of Fishes, consists in its earliest condition of a single large trunk, which traverses the splanchnic mesoblast investing the part of the alimentary tract behind the heart. This trunk is directly continuous in front with the heart, and underlies the alimentary canal through both its praeanal and postanal sections. It is shewn in section in fig. 367, v, and may be called the subintestinal vein. This vein has been found in the embryos of Teleostei, Ganoidei, Elasmobranchii and Cyclostomata, and runs parallel to the dorsal aorta above, into which it is sometimes continued behind (Teleostei, Ganoidei, etc.).

In Elasmobranch embryos the subintestinal vein terminates, as may be gathered from sections (fig. 368, v.cau), shortly before the end of the tail. The same series of sections also shews that at the cloaca, where the gut enlarges and comes in contact with the skin, this vein bifurcates, the two branches uniting into a single vein both in front of and behind the cloaca.

In most Fishes the anterior part of this vein atrophies, the caudal section alone remaining, but the anterior section of it persists in the fold of the intestine in Petromyzon, and also remains in the spiral valve of some Elasmobranchii. In Amphioxus, moreover, it forms, as in the embryos of higher types, the main venous trunk, though even here it is usually broken up into two or three parallel vessels.

It no doubt represents one of the primitive longitudinal trunks of the vermiform ancestors of the Chordata. The heart and the branchial artery constitute a specially modified anterior continuation of this vein. The


652


THE SUBINTESTINAL VEIN.


-p.o


rp.r.


dilated portal sinus of Myxine is probably also part of it ; and if this is really rhythmically contractile 1 the fact would be interesting as shewing that this quality, which is now localised in the heart, was once probably common to the subintestinal vessel for its whole length.

On the development of the cardinal veins (to be described below) considerable changes are effected in the subintestinal vein. Its postanal section, which is known in the adult as the caudal vein, unites with the cardinal veins. On this junction being effected retrogressive changes take place in the praeanal section of the original subintestinal vessel. It breaks up in front into a number of smaller vessels, the most important of which is a special vein, which lies in the fold of the spiral valve, and which is more conspicuous in some Elasmobranchii than in Scyllium, in which the development of the vessel has been mainly studied. The lesser of the two branches connecting it round the cloaca with the caudal vein first vanishes, and then the larger ; and the two posterior cardinals are left as the sole forward continuations of the caudal vein. The latter then becomes prolonged forwards, so that the two cardinals open into it some little distance in front of the hind end of the kidneys. By these changes, and by the disappearance of the postanal section of the gut, the caudal vein is made to appear as a supraintestinal and not, as it really is, a subintestinal vessel.

From the subintestinal vein there is given off a branch which supplies the yolk-sack. This leaves the subintestinal vein close

1 J. Miiller holds that this sack is not rhythmically contractile.



FIG. 367. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNGER

THAN 28 F.

sp.c. spinal canal; W. white matter of spinal cord ; pr. posterior nerve-roots; ch. notochord ; x. sub-notochordal rod ; ao. aorta ; mp. muscle plate; ;;//'. inner layer of muscle-plate already converted into muscles; Vr. rudiment of vertebral body; st. segmental tube ; sd. segmental duct ; sp.v. spiral valve; v. subintestinal vein ; p.o. primitive generative cells.


THE VENOUS SYSTEM.


653


to the liver. The liver, on its development, embraces the subintestinal vein, which then breaks up into a capillary system in the liver, the main part of its blood coming at this period from the yolk-sack.

The portal system is thus established from the subintestinal vein ; but is eventually joined by the various visceral, and sometimes by the genital, veins as they become successively developed.

The blood from the liver is brought back to the sinus venosus by veins known as the hepatic veins, which, like the hepatic capillary system, are derivatives of the subintestinal vessel.

There join the portal system in Myxinoids and many Teleostei a number of veins from the anterior abdominal walls, representing a commencement of the anterior abdominal or epigastric vein of higher types 1 .

In the higher Vertebrates the original subintestinal vessel never attains a full development, even in the embryo. It is represented by (i) the ductus



FIG. 368. FOUR SECTIONS THROUGH THE POSTANAL PART OF THE TAIL OF AN EMBRYO OF THE SAME AGE AS FIG. 28 F.

A. is the posterior section.

nc. neural canal; al. post-anal gut; alv. caudal vesicle of post-anal gut; x. subnotochordal rod; mp. muscle-plate; c/i. notochord; cl.al. cloaca; ao. aorta; v.cait. caudal vein.

1 Stannius, Vergleich. Anat., p. 251.


654


THE CARDINAL VEINS.


venosus, which, like the true subintestinal vein, gives origin (in the Amniota) to the vitelline veins to the yolk-sack, and (2) by the caudal vein. Whether the partial atrophy of the subintestinal vessel was primitively caused by the development of the cardinal veins, or for some other reason, it is at any rate a fact that in all existing Fishes the cardinal veins form the main venous channels of the trunk.

Their later development than the subintestinal vessel as well as their absence in Amphioxus, probably indicate that they became evolved, at any rate in their present form, within the Vertebrate phylum.

The embryonic condition of the venous system, with a single large subintestinal vein is, as has been stated, always modified by the development of a paired system of vessels, known as the cardinal veins, which bring to the heart the greater part of the blood from the trunk.

The cardinal veins appear in Fishes as four paired longitudinal trunks (figs. 363 and 369), two anterior (/) and two posterior (c). They unite into two transverse trunks on either side, known as the ductus Cuvieri (dc), which fall into the sinus venosus, passing from the body wall to the sinus by a lateral mesentery of the heart already spoken of (p. 627, fig. 352). The anterior pair, known as the anterior cardinal or jugular veins, bring to the heart the blood from the head and neck. They are placed one on each side above the level of the branchial arches (fig. 299, a.cv). The posterior cardinal veins lie immediately dorsal to the mesonephros (Wolfifian body), and are mainly supplied by the blood from this organ and from the walls of the body (fig. 275, c.a.v). In many forms (Cyclostomata, Elasmobranchii and many Teleostei) they unite posteriorly with the caudal veins in the manner already described, and in a large number of instances the connecting branch between the two systems, in its passage through the mesonephros, breaks up into a capillary network, and so gives rise to a renal portal system.

The vein from the anterior pair of fins (subclavian) usually unites with the anterior jugular vein.



j


FIG. 369. DIAGRAM OF THE PAIRED VENOUS SYSTEM

OF A FISH. (From Gegenbaur. )

j. jugular vein (anterior cardinal vein) ; c. posterior cardinal vein; //. hepatic veins ; sv. sinus venosus ; dc. ductus Cuvieri.


THE VENOUS SYSTEM. 655

The venous system of the Amphibia and Amniota always differs from that of Fishes in the presence of a new vessel, the vena cava inferior, which replaces the posterior cardinal veins; the latter only being present, in their piscine form, during embryonic life. It further differs from that of all Fishes, except the Dipnoi, in the presence of pulmonary veins bringing back the blood directly from the lungs.

In the embryos of all the higher forms the general characters of the venous system are at first the same as in Fishes, but with the development of the vena cava inferior the front sections of the posterior cardinal veins atrophy, and the ductus Cuvieri, remaining solely connected with the anterior cardinals and their derivatives, constitute the superior venae cavae. The inferior cava receives the hepatic veins.

Apart from the non-development of the subintestinal vein the visceral section of the venous system is very similar to that in Fishes.

The further changes in the venous system must be dealt with separately for each group.

Amphibia. In Amphibia (Gotte, No. 296) the anterior and posterior cardinal veins arise as in Pisces. From the former the internal jugular vein arises as a branch ; the external jugular constituting the main stem. The subclavian with its large cutaneous branch also springs from the system of the anterior cardinal. The common trunk formed by the junction of these three veins falls into the ductus Cuvieri.

The posterior cardinal veins occupy the same position as in Pisces, and unite behind with the caudal veins, which Gotte has shewn to be originally situated below the post-anal gut. The iliac veins unite with the posterior cardinal veins, where the latter fall into the caudal vein. The original piscine condition of the veins is not long retained. It is first of all disturbed by the development of the anterior part of the important unpaired venous trunk which forms in the adult the vena cava inferior. This is developed independently, but unites behind with the right posterior cardinal. From this point backwards the two cardinal veins coalesce for some distance, to give rise to the posterior section of the vena cava inferior, situated between the kidneys 1 . The anterior sections of the cardinal veins subsequently atrophy. The posterior part of the cardinal veins, from their junction with the vena cava inferior to the caudal veins, forms a rhomboidal figure. The iliac vein joins the outer angle of this figure, and is thus in direct communication with the inferior vena cava, but it is also connected with a longitu 1 This statement of Gotte's is opposed to that of Rathke for the Amniota, and cannot be considered as completely established.


656 VEINS OF THE SNAKE.

dinal vessel on the outer border of the kidneys, which receives transverse vertebral veins and transmits their blood to the kidneys, thus forming a renal portal system. The anterior limbs of the rhomboid formed by the cardinal veins soon atrophy, so that the blood from the hind limbs can only pass to the inferior vena cava through the renal portal system. The posterior parts of the two cardinal veins (uniting in the Urodela directly with the unpaired caudal vein) still persist. The iliac veins also become directly connected with a new vein, the anterior abdominal vein, which has meanwhile become developed. Thus the iliac veins become united with the system of the vena cava inferior through the vena renalis advehens on the outer border of the kidney, and with the anterior abdominal veins by the epigastric veins.

The visceral venous system begins with the development of two vitelline veins, which at first join the sinus venosus directly. They soon become enveloped in the liver, where they break up into a capillary system, which is also joined by the other veins from the viscera. The hepatic system has in fact the same relations as in Fishes. Into this system the anterior abdominal vein also pours itself in the adult. This vein is originally formed of two vessels, which at first fall directly into the sinus venosus, uniting close to their opening into the sinus with a vein from the truncus arteriosus. They become prolonged backwards, and after receiving the epigastric veins above mentioned from the iliac veins, and also veins from the allantoic bladder, unite behind into a single vessel. Anteriorly the right vein atrophies and the left continues forward the unpaired posterior section.

A secondary connection becomes established between the anterior abdominal vein and the portal system ; so that the blood originally transported by the former vein to the heart becomes diverted so as to fall into the liver. A remnant of the primitive connection is still retained in the adult in the form of a small vein, the so-called vena bulbi posterior, which brings the blood from the walls of the truncus arteriosus directly into the anterior abdominal vein.

The pulmonary veins grow directly from the heart to the lungs.

For our knowledge of the development of the venous system of the Amniota we are mainly indebted to Rathke.

Reptilia. As an example of the Reptilia the Snake may be selected, its venous system having been fully worked out by Rathke in his important memoir on its development (No. 300).

The anterior (external jugular) and posterior cardinal veins are formed in the embryo as in all other types (fig. 370, vj and vc] ; and the anterior cardinal, after giving rise to the anterior vertebral and to the cephalic veins, persists with but slight modifications in the adult ; while the two ductus Cuvieri constitute the superior venos cavas.

The two posterior cardinals unite behind with the caudal veins. They are placed in the usual situation on the dorsal and outer border of the kidneys.


THE VENOUS SYSTEM.


657



U FIG. 370. ANTERIOR PORTION OF THE VENOUS SYSTEM OF AN EMBRYONIC SNAKE. (From Gegenbaur; after Rathke.)

vc. posterior cardinal vein; vj. jugular vein; DC. ductus Cuvieri ; vu. allantoic vein ; v. ventricle ; ba. truncus arteriosus ; a. visceral clefts ; /. auditory vesicle.


With the development of the vena cava inferior, to be described below, the blood from the kidneys becomes mainly transported by this vessel to the heart ; and the section of the posterior cardinals opening into the ductus Cuvieri gradually atrophies, their posterior parts remaining however on the outer border of the kidneys as the vena? renales advehentes 1 .

While the front part of the posterior cardinal veins is undergoing atrophy, the intercostal veins, which originally poured their blood into the posterior cardinal veins, become also connected with two longitudinal veins the posterior vertebral veins which are homologous with the azygos and hemiazygos veins of Man ; and bear the same relation to the anterior vertebral veins that the anterior and posterior cardinals do to each other.

These veins are at first connected by trans verse anastomoses with the posterior cardinals, but, on the disappearance of the front part of the latter, the whole of the blood from the intercostal veins falls into the posterior vertebral veins. They are united in front with the anterior vertebral veins, and the common trunk of the two veins on each side falls into the jugular vein.

The posterior vertebral veins are at first symmetrical, but after becoming connected by transverse anastomoses, the right becomes the more important of the two.

The vena cava inferior, though considerably later in its development than the cardinals, arises fairly early. It constitutes in front an unpaired trunk, at first very small, opening into the right allantoic vein, close to the heart. Posteriorly it is continuous with two veins placed on the inner border of the kidneys 2 .

The vena cava inferior passes through the dorsal part of the liver, and in doing so receives the hepatic veins.

The portal system is at first constituted by the vitelline vein, which is directly continuous with the venous end of the heart, and at first receives the two ductus Cuvieri, but at a later period unites with the left ductus.

1 Rathke's account of the vena renalis advehens is thus entirely opposed to that which Gotte gives for the Frog, but my own observations on the Lizard incline me to accept Rathke's statements, for the Amniota at any rate.

2 The vena cava inferior does not according to Rathke's account unite behind with the posterior cardinal veins, as it is stated by Gotte to do in the Anura. Gb'tte questions the accuracy of Rathke's statements on this head, but my own observations are entirely in favour of Rathke's observations, and lend no support whatever to Gotte's views.


B. III.


658 VEINS OF THE CHICK.

It soon receives a mesenteric vein bringing the blood from the viscera, which is small at first but rapidly increases in importance.

The common trunk of the vitelline and mesenteric veins, which may be called the portal vein, becomes early enveloped by the liver, and gives off branches to this organ, the blood from which passes by the hepatic veins to the vena cava inferior. As the branches in the liver become more important, less and less blood is directly transported to the heart, and finally the part of the original vitelline vein in front of the liver is absorbed, and the whole of the blood from the portal system passes from the liver into the vena cava inferior.

The last section of the venous system to be dealt with is that of the anterior abdominal vein. There are originally, as in the Anura, two veins belonging to this system, which owing to the precocious development of the bladder to form the allantois, constitute the allantoic veins (fig. 370, vu}.

These veins, running along the anterior abdominal wall, are formed somewhat later than the vitelline vein, and fall into the two ductus Cuvieri. They unite with two epigastric veins (homologous with those in the Anura), which connect them with the system of the posterior cardinal veins. The left of the two eventually atrophies, so that there is formed an unpaired allantoic vein. This vein at first receives the vena cava inferior close to the heart, but eventually the junction of the two takes place in the region of the liver, and finally the anterior abdominal vein (as it comes to be after the atrophy of the allantois) joins the portal system and breaks up into capillaries in the liver 1 .

In Lizards the iliac veins join the posterior cardinals, and so pour part of their blood into the kidneys ; they also become connected by the epigastric veins with the system of the anterior abdominal or allantoic vein. The subclavian veins join the system of the superior venae cavas.

The venous system of Birds and Mammals differs in two important points from that of Reptilia and Amphibia. Firstly the anterior abdominal vein is only a foetal vessel, forming during foetal life the allantoic vein ; and secondly a direct connection is established between the vena cava inferior and the veins of the hind limbs and posterior parts of the cardinal veins, so that there is no renal portal system.

Aves. The Chick may be taken to illustrate the development of the venous system in Birds.

On the third day, nearly the whole of the venous blood from the body of the embryo is carried back to the heart by two main venous trunks, the anterior (fig. 125, S.Ca.V) and posterior (V.Ca) cardinal veins, joining on each side to form the short transverse ductus Cuvieri (DC), both of which unite with the sinus venosus close to the heart. As the head and neck continue to enlarge, and the wings become developed, the single anterior

1 The junction between the portal system and the anterior abdominal vein is apparently denied by Rathke (No. 300, p. 173), hut this must he an error on his part.


THE VENOUS SYSTEM.


659



V.C.L


cardinal or jugular vein (fig. 371, /), of each side, is joined by two new veins : the vertebral vein, bringing back blood from the head and neck, and the subclavian vein from the wing (W\

On the third day the posterior cardinal veins are the only veins which return the blood from the hinder part of the body of the embryo.

About the fourth or fifth day, however, the vena cava inferior (fig. 371, V.C.L) makes its appearance. This, starting from the sinus venosus not far from the heart, is on the fifth day a short trunk running backward in the middle line below the aorta, and speedily losing itself in the tissues of the Wolffian bodies. When the true kidneys are formed it also receives blood from them, and thenceforward enlarging rapidly becomes the channel by which the greater part of the blood from the hinder part of the body finds its way to the heart. In proportion as the vena cava inferior increases in size, the posterior cardinal veins diminish.

The blood originally coming to them from the posterior part of the spinal cord and trunk is transported into two posterior vertebral veins, similar to those in Reptilia, which are however placed dorsally to the heads of the ribs, and join the anterior vertebral veins. With their appearance the anterior parts of the posterior cardinals disappear. The blood from the hind limbs becomes transported directly through the kidney into the vena cava inferior, without forming a renal portal system 1 .

On the third day the course of the vessels from the yolk-sack is very simple. The two vitelline veins, of which the right is already the smaller, form the ductus venosus, from which, as it passes through the liver on its way to the heart, are given off the two sets of vena advehentes and vena revehentes (fig. 371).

With the appearance of the allantois on the fourth day, a new feature is introduced. From the ductus venosus there is given off a vein which quickly divides into two branches. These, running along the ventral walls of the body from which they receive some amount of blood, pass to the allantois. They are the allantoic veins (fig. 371, U] homologous with the anterior abdominal vein of the lower types. They unite in front to form a single vein, which becomes, by reason of the rapid growth of the allantois, very long. The right branch soon diminishes in size and finally disappears. Meanwhile the left on reaching the allantois bifurcates ; and, its two


FIG. 371. DIAGRAM OF THE VENOUS CIRCULATION IN THE CHICK AT THE COMMENCEMENT OF THE FIFTH

DAY.

H. heart ; d. c. ductus Cuvieri. Into the ductus Cuvieri of each side fall/, the jugular vein, W. the vein from the wing, and c. the inferior cardinal vein ; S. V. sinus venosus ; Of. vitelline vein ; U. allantoic vein, which at this stage gives off branches to the bodywalls ; V.C.l. inferior vena cava ; /. liver.


The mode in which this is effected requires further investigation.

42 2


66o


VEINS OF THE CHICK.



branches becoming large and conspicuous, there still appear to be two main allantoic veins. At its first appearance the allantoic vein seems to be but a small branch of the vitelline, but as the allantois grows rapidly, and the yolk-sack dwindles, this state of things is reversed, and the less conspicuous vitelline appears as a branch of the larger allantoic vein.

On the third day the blood returning from the walls of the intestine is insignificant in amount. As however the intestine becomes more and more developed, it acquires a distinct venous system, and its blood is returned by veins which form a trunk, the mesenteric vein (fig. 372, M") falling into the vitelline vein at its junction with the allantoic vein.

These three great veins, in fact, form a large common trunk, which enters at once into the liver, and which we may now call the portal vein (fig. 372, P. V}. This, at its entrance into the liver, partly breaks up into the vena advehentes, and partly continues as the ductus venosus (D.V} straight through the liver, emerging from which it joins the vena cava inferior. Before the establishment of the vena cava inferior, the venas revehentes, carrying back the blood which circulates through the hepatic capillaries, join the ductus venosus close to its exit from the liver. By the time however that the vena cava has become a large and important vessel it is found that the venae revehentes, or as we may now call them the hepatic veins, have shifted their embouchment, and now fall directly into that vein, the ductus venosus making a separate junction rather higher up (fig. 372).

This state of things continues with but slight changes till near the end of incubation, when the chick begins to breathe the air in the air-chamber of the shell, and respiration is no longer carried on by the allantois. Blood then ceases to flow along the allantoic vessels ; they become obliterated. The vitelline vein, which as the yolk becomes gradually absorbed proportionately diminishes in size and importance, comes to appear as a mere branch of the portal vein. The ductus venosus becomes obliterated ; and hence the whole of the blood coming through the portal vein flows into the substance of the liver, and so by the hepatic veins into the vena cava.

Although the allantoic (anterior abdominal) vein is obliterated in the adult, there is nevertheless established an anastomosis between the portal system and the veins bringing the blood from the limbs to the vena cava


FIG. 372. DIAGRAM OF THE VENOUS CIRCULATION IN THE CHICK DURING THE LATER DAYS OF INCUBATION.

H. heart ; V.S.R. right vena cava superior; V.S.L. left vena cava superior. The two venas cavrc superiores are the original 'ductus Cuvieri,' they open into the sinus venosus. J. jugular vein; Su.V. anterior vertebral vein ; In. V. inferior vertebral vein ; W. subclavian; V.C.I, vena cava inferior; D. V. ductus venosus ; P. V. portal vein ; M. mesenteric vein bringing blood from the intestines into the portal vein ; O.f. vitelline vein ; U. allantoic vein. The three last mentioned veins unite together to form the portal vein ; /. liver.


THE VENOUS SYSTEM.


66l


inferior, in that the caudal vein and posterior pelvic veins open into a vessel, known as the coccygeo-mesenteric vein, which joins the portal vein ; while at the same time the posterior pelvic veins are connected with the common iliac veins by a vessel which unites with them close to their junction with the coccygeo-mesenteric vein.

Mammalia. In Mammals the same venous trunks are developed in the embryo as in other types (fig. 373 A). The anterior cardinals or external jugulars form the primitive veins of the anterior part of the body, and the internal jugulars and anterior vertebrals are subsequently formed. The subclavians (fig. 373 A, j), developed on the formation of the anterior limbs, also pour their blood into these primitive trunks. In the lower Mammalia (Monotremata, Marsupialia, Insectivora, some Rodentia, etc., the two ductus Cuvieri remain as the two superior venae cavae, but more usually an anastomosis arises between the right and left innominate veins, and eventually the whole of the blood of the left superior cava is carried to the right side, and there is left only a single superior cava (fig. 373 B and C).



F IG - 373- DIAGRAM OF THE DEVELOPMENT OF THE PAIRED VENOUS SYSTEM OF

MAMMALS (MAN). (From Gegenbaur.)

j. jugular vein ; cs. vena cava superior; s. subclavian veins; c. posterior cardinal vein ; v. vertebral vein ; az. azygos vein ; cor. coronary vein.

A. Stage in which the cardinal veins have already disappeared. Their position is indicated by dotted lines.

B. Later stage when the blood from the left jugular vein is carried into the right to form the single vena cava superior ; a remnant of the left superior cava being however still left.

C. Stage after the left vertebral vein has disappeared; the right vertebral remaining as the azygos vein. The coronary vein remains as the last remnant of the left superior vena cava.

A small rudiment of the left superior cava remains however as the sinus coronartus and receives the coronary vein from the heart (figs. 373 C, cor and 374, cs).

The posterior cardinal veins form at first the only veins receiving the


662


THE VEINS OF MAMMALIA.


blood from the posterior part of the trunk and kidneys ; and on the development of the hind limbs receive the blood from them also.

As in the types already described an unpaired vena cava inferior becomes eventually developed, and gradually carries off a larger and larger portion of the blood originally returned by the posterior cardinals. It unites with the common stem of the allantoic and vitelline veins in front of the liver.

At a later period a pair of trunks is established bringing the blood from the posterior part of the cardinal veins and the crural veins directly into the vena cava inferior (fig. 374, il}. These vessels, whose development has not been adequately investigated, form the common iliac veins, while the posterior ends of the cardinal veins which join them become the hypogastric veins (fig. 374, hy). Owing to the development of the common iliac veins there is no renal portal system like that of the Reptilia and Amphibia.

Posterior vertebral veins, similar to those of Reptilia and Birds, are established in connection with the intercostal and lumbar veins, and unite anteriorly with the front part of the posterior



FIG. 374. DIAGRAM OF THE CHIEF

VENOUS TRUNKS OF MAN. (From Gegenbaur.)

cs. vena cava superior ; s. subclavian vein ; ji. internal jugular ; je. external jugular ; az. azygos vein ; ha. hemiazygos vein ; c. clotted line shewing previous position of cardinal veins ; ci. vena cava inferior ; r. renal veins ; il. iliac ; hy. hypogastric veins ; h. hepatic veins.

The dotted lines shew the position of embryonic vessels aborted in the adult.


cardinal veins (fig. 373 A) 1 .

On the formation of the posterior vertebral veins, and as the inferior vena cava becomes more important, the middle part of the posterior cardinals becomes completely aborted (fig. 374, f), the anterior and posterior parts still persisting, the former as the continuations of the posterior vertebrals into the anterior vena cava (az\ the latter as the hypogastric veins (Ay).

Though in a few Mammalia both the posterior vertebrals persist, a transverse connection is usually established between them, and the one (the right) becoming the more important constitutes the azygos vein (fig. 374, az), the persisting part of the left forming the hemiazygos vein (ha}.

The remainder of the venous system is formed in the embryo of the vitelline and allantoic veins, the former being eventually joined by the mesenteric vein so as to constitute the portal vein.

1 Rathke, as mentioned above, holds that in the Snake the front part of the posterior cardinals completely aborts. Further investigations are required to shew whether there really is a difference between Mammalia and Reptilia in this matter.




THE VENOUS SYSTEM. 663

The vitelline vein is the first part of this system established, and divides near the heart into two veins bringing back the blood from the yolk-sack (umbilical vesicle). The right vein soon however aborts.

The allantoic (anterior abdominal) veins are originally paired. They are developed very early, and at first course along the still widely open somatic walls of the body, and fall into the single vitelline trunk in front. The right allantoic vein disappears before long, and the common trunk formed by the junction of the vitelline and allantoic veins becomes considerably elongated. This trunk is soon enveloped by the liver.

The succeeding changes have been somewhat differently described by Kolliker and Rathke. According to the former the common trunk of the allantoic and vitelline veins in its passage through the liver gives off branches to the liver, and also receives branches from this organ near its anterior exit. The main trunk is however never completely aborted, as in the embryos of other types, but remains as the ductus venosus Arantii.

With the development of the placenta the allantoic vein becomes the main source of the ductus venosus, and the vitelline or portal vein, as it may perhaps be now conveniently called, ceases to join it directly, but falls into one of its branches in the liver.

The vena cava inferior joins the continuation of the ductus venosus in front of the liver, and, as it becomes more important, it receives directly the hepatic veins which originally brought back blood into the ductus venosus. The ductus venosus becomes moreover merely a small branch of the vena cava.

At the close of foetal life the allantoic vein becomes obliterated up to its place of entrance into the liver ; the ductus venosus becomes a solid cord the so-called round ligament and the whole of the venous blood is brought to the liver by the portal vein 1 .

Owing to the allantoic (anterior abdominal) vein having merely a fcetal existence an anastomosis between the iliac veins and the portal system by means of the anterior abdominal vein is not established.


BIBLIOGRAPHY of the Venous System.

(498) J. Marshall. "On the development of the great anterior veins." Phil. Trans., 1859.

(499) H. Rathke. " Ueb. d. Bildung d. Pfortader u. d. Lebervenen b. Saugethieren." MeckeVs Archiv, 1830.

(500) H. Rathke. "Ueb. d. Bau u. d. Entwick. d. Venensystems d. Wirbelthiere." Bericht. Jib. d. natttrh. Seminar, d. Univ. Konigsberg, 1838.

Vide also Von Baer (No. 291), Gotte (No. 296), Kolliker (No. 298), and Rathke (Nos. 299, 300, and 301).

1 According to Rathke the original trunk connecting the allantoic vein directly with the heart through the liver is aborted, and the ductus venosus Arantii is a secondary connection established in the latter part of foetal life.


664 LYMPHATIC SYSTEM.


Lymphatic System.

The lymphatic system arises from spaces in the general parenchyma of the body, independent in their origin of the true body cavity, though communicating both with this cavity and with the vascular system.

In all the true Vertebrata certain parts of the system form definite trunks communicating with the venous system ; and in the higher types the walls of the main lymphatic trunks become quite distinct.

But little is known with reference to the ontogeny of the lymphatic vessels, but they originate late in larval life, and have at first the form of simple intercellular spaces.

The lymphatic glands appear to originate from lymphatic plexuses, the cells of which produce lymph corpuscles. It is only in Birds and Mammals, and especially in the latter, that the lymphatic glands form definite structures.

The Spleen. The spleen, from its structure, must be classed with the lymphatic glands, though it has definite relations to the vascular system. It is developed in the mesoblast of the mesogastrium, usually about the same time and in close connection with the pancreas.

According to Miiller and Peremeschko the mass of mesoblast which forms the spleen becomes early separated by a groove on the one side from the pancreas and on the other from the mesentery. Some of its cells become elongated, and send out processes which uniting with like processes from other cells form the trabecular system. From the remainder of the tissue are derived the cells of the spleen pulp, which frequently contain more than one nucleus. Especial accumulations of these cells take place at a later period to form the so-called Malpighian corpuscles of the spleen.

BIBLIOGRAPHY of Spleen.

(501) W. Miiller. "The Spleen." Strieker's Histology.

(502) Peremeschko. " Ueb. d. Entwick. d. Milz." Sitz. d. Wuti. Akad. Wiss., Vol. LVI. 1867.

Suprarenal ^bodies.

In Elasmobranch Fishes two distinct sets of structures are found, both of which have been called suprarenal bodies. As shewn in the sequel both of these structures probably unite in the higher types to form the suprarenal bodies.

One of them consists of a series of paired bodies, situated on the branches of the dorsal aorta, segmentally arranged, and forming a chain extending from close behind the heart to the hinder end of the body cavity. Each body is formed of a series of lobes, and exhibits a well-marked distinction into a cortical layer of columnar cells, and a medullary substance formed of irregular polygonal cells. As first shewn by Leydig, they are


SUPRARENAL BODIES. 665

closely connected with the sympathetic ganglia, and usually contain numerous ganglion cells distributed amongst the proper cells of the body.

The second body consists of an unpaired column of cells placed between the dorsal aorta and unpaired caudal vein, and bounded on each side by the posterior parts of the kidney. I propose to call it the interrenal body. In front it overlaps the paired suprarenal bodies, but does not unite with them. It is formed of a series of well-marked lobules, etc. In the fresh state Leydig (No. 506) finds that "fat molecules form the chief mass of the body, and one finds freely imbedded in them clear vesicular nuclei." As may easily be made out from hardened specimens it is invested by a tunica propria, which gives off septa dividing it into well-marked areas filled with polygonal cells. These cells constitute the true parenchyma of the body. By the ordinary methods of hardening, the oil globules, with which they are filled in the fresh state, completely disappear.

The paired suprarenal bodies (Balfour, No. 292, pp. 242 244) are developed from the sympathetic ganglia. These ganglia, shewn in an early stage in fig. 380, sy.g, become gradually divided into a ganglionic part and a glandular part. The former constitutes the sympathetic ganglia of the adult ; the latter the true paired suprarenal bodies. The interrenal body is however developed (Balfour, No. 292, pp. 245 247) from indifferent mesoblast cells between the two kidneys, in the same situation as in the adult.

The development of the suprarenal bodies in the Amniota has been most fully studied by Braun (No. 503) in the Reptilia.

In Lacertilia they consist of a pair of elongated yellowish bodies, placed between the vena renalis revehens and the generative glands.

They are formed of two constituents, viz. (i) masses of brown cells placed on the dorsal side of the organ, which stain deeply with chromic acid, like certain of the cells of the suprarenals of Mammalia, and (2) irregular cords, in part provided with a lumen, filled with fat-like globules l , amongst which are nuclei. On treatment with chromic acid the fat globules disappear, and the cords break up into bodies resembling columnar cells.

The dorsal masses of brown cells are developed from the sympathetic ganglia in the same way as the paired suprarenal bodies of the Elasmobranchii, while the cords filled with fat-like globules are formed of indifferent mesoblast cells as a thickening in the lateral walls of the inferior vena cava, and the cardinal veins continuous with it. The observations of Brunn (No. 504) on the Chick, and Kolliker (No. 298, pp. 953955) n the Mammal, add but little to those of Braun. They shew that the greater part of the gland (the cortical substance) in these two types is derived from the mesoblast, and that the glands are closely connected with sympathetic ganglia ; while Kolliker also states that the posterior part of the organ is unpaired in the embryo rabbit of 1 6 or 17 days.

The structure and development of what I have called the interrenal body

1 These globules are not formed of a true fatty substance, and this is also probably true for the similar globules of the interrenal bodies of Elasmobranchii.


666 SUPRARENAL BODIES.

in Elasmobranchii so closely correspond with that of the mesoblastic part of the suprarenal bodies of the Reptilia, that I have very little hesitation in regarding them as homologous 1 ; while the paired bodies in Elasmobranchii, derived from the sympathetic ganglia, clearly correspond with the part of the suprarenals of Reptilia having a similar origin ; although the anterior parts of the paired suprarenal bodies of Fishes have clearly become aborted in the higher types.

In Elasmobranch Fishes we thus have (i) a series of paired bodies, derived from the sympathetic ganglia, and (2) an unpaired body of mesoblastic origin. In the Amniota these bodies unite to form the compound suprarenal bodies, the two constituents of which remain, however, distinct in their development. The mesoblastic constituent appears to form the cortical part of the adult suprarenal body, and the nervous constituent the medullary part.

BIBLIOGRAPHY of the Suprarenal bodies,

(503) M. Braun. "Bau u. Entwick. d. Nebennieren bei Reptilien. " Arbeit, a. d. zool.-zoot. Institut Wurzlttrg, Vol. V. 1879.

(504) A. v. Brunn. "Ein Beitrag z. Kenntniss d. feinern Baues u. d. Entwick. d. Nebennieren." Archiv f. mikr. Anat., Vol. VIII. 1872.

(505) Fr. Leydig. Untersiich. iib. Fische u. fieptilten. Berlin, 1853.

(506) Fr. Leydig. Rochen u. Haie. Leipzig, 1852.

Vide also F. M. Balfour (No. 292), Kolliker (No. 298), Remak (No. 302), etc.

1 The fact of the organ being unpaired in Elasmobranchii and paired in the Amniota is of no importance, as is shewn by the fact that part of the organ is unpaired in the Rabbit.


CHAPTER XXII.


THE MUSCULAR SYSTEM.



IN all the Ccelenterata, except the Ctenophora, the contractile elements of the body wall consist of filiform processes of ectodermal or entodermal epithelial cells (figs. 375 and 376 B). The elements provided with these processes, which were first discovered by Kleinenberg, are known as myo-epithelial cells. Their contractile parts may either be striated (fig. 376) or non-striated (fig. 375). In some instances the epithelial part of the cell may nearly abort, its nucleus alone remaining (fig. 376 A) ; and in this way a layer of muscles lying completely below the surface may be established.

There is embryological evidence of the derivation of the voluntary muscular system of a large number of types from myo-epithelial cells of this kind. The more important of these groups are the Chaetopoda, the Gephyrea, the Chaetognatha, the Nematoda, and the Vertebrata 1 .

While there is clear evidence that the muscular system of a large number of types is composed of cells which had their origin in myo-epithelial cells, the mode of evolution of the

1 If recent statements of Metschnikoff are to be trusted, the Echinodermata must be added to these groups. The amoeboid cells stated in the first volume of this treatise to form the muscles in this group, on the authority of Selenka, give rise, according to Metschnikoff, only to the cutis, while the same naturalist states the epithelial cells of the vasoperitoneal vesicles are provided with muscular tails.


FIG. 375. MYO-EPITHELIAL CELLS OF HYDRA. (From Gegenbaur ; after Kleinenberg.)

m. contractile fibres.


668 THE MUSCULAR FIBRES.

muscular system of other types is still very obscure. The muscles may arise in the embryo from amoeboid or indifferent cells, and the Hertwigs 1 hold that in many of these instances the muscles have also phylogenetically taken their origin from indifferent connective-tissue cells. The subject is however beset with very serious difficulties, and to discuss it here would carry me too far into the region of pure histology.

The voluntary muscular system of the CJiordata.

The muscular fibres. The muscular elements of the Chordata undoubtedly belong to the myo-epithelial type. The embryonic muscle-cells are at first simple epithelial cells, but



FIG. 376. MUSCLE-CELLS OF LIZZIA KOLLIKERI. (From Lankester ; after O. and R. Hertwig.)

A. Muscle-cell from the circular fibres of the subumbrella.

B. Myo-epithelial cells from the base of a tentacle.

soon become spindle-shaped : part of their protoplasm becomes differentiated into longitudinally placed striated muscular fibrils, while part, enclosing the nucleus, remains indifferent, and constitutes the epithelial element of the cells. The muscular fibrils are either placed at one side of the epithelial part of the cell, or in other instances (the Lamprey, the Newt, the Sturgeon, the Rabbit) surround it. The latter arrangement is shewn for the Sturgeon in fig. 57.

The number of the fibrils of each cell gradually increases, and the protoplasm diminishes, so that eventually only the nucleus, or nuclei resulting from its division, are left. The products of each cell probably give rise, in conjunction with a further division of the nucleus, to a primitive bundle, which,

1 O. and R. Hertwig, Die Calomthcorie. Jena, 1881.


THE MUSCULAR SYSTEM.


669


t>r



except in Amphioxus, Petromyzon, etc., is surrounded by a special investment of sarcolemma.

The voluntary muscular system. For the purposes of description the muscular system of the Vertebrata may conveniently be divided into two sections, viz. that of the head and that of the trunk. The main part, if not the whole, of the muscular system of the trunk is derived from certain structures, known as the muscle-plates, which take their origin from part of the primitive mesoblastic somites.

It has already been stated (pp. 292 ^296) that the mesoblastic somites are derived from the dorsal segmented part of the primitive mesoblastic plates. Since the history of these bodies is presented in its simplest form in Elasmobranchii it will be convenient to commence with this group. Each somite is composed of two layers a somatic and a splanchnic both formed of a single row of columnar cells. Between these two layers is a cavity, which is at first directly continuous with the general body cavity, of which indeed it merely forms a specialised part (fig. 377). Before long the cavity becomes however completely constricted off from the permanent body cavity.

Very early (fig. 377) the inner or splanchnic wall of the somites loses its simple constitution, owing to the middle part of it undergoing peculiar changes. The meaning of the changes is at once shewn by longitudinal horizontal sections, which prove (% 378) that the cells in this situation (mp') have become extended in a longitudinal direction, and, in fact, form typical spindle-shaped embryonic muscle-cells, each with a large nucleus. Every muscle-cell extends for the whole length of a somite. The inner layer of each somite, immediately within the muscle-band just described, begins to proliferate, and produce


FIG. 377. TRANSVERSE SECTION THROUGH THETRUNK OF AN EMBRYO SLIGHTLY OLDER THAN FIG. 28 E.

nc. neural canal ; pr. posterior root of spinal nerve ; x. subnotochordal rod ; ao. aorta ; sc. somatic mesoblast ; sf>. splanchnic mesoblast ; mp. muscle-plate ; mp', portion of muscle-plate converted into muscle ; Vr. portion of the vertebral plate which will give rise to the vertebral bodies ; al. alimentary tract.


THE MUSCLE-PLATES.


a mass of cells, placed between the muscles and the notochord ( Vr\ These cells form the commencing vertebral bodies, and have at first (fig. 378) the same segmentation as the somites from which they sprang.

After the separation of the vertebral bodies from the somites the remaining parts of the somites may be called muscle-plates ; since they become directly converted into the whole voluntary muscular system of the trunk (fig. 379, mp}.

According to the statements of Bambeke and Go'tte, the Amphibians present some noticeable peculiarities in the development of their muscular system, in that such distinct muscle-plates as those of other vertebrate types are not developed. Each side-plate of mesoblast is divided into a somatic and a splanchnic layer, continuous throughout the vertebral and parietal portions of the plate. The vertebral portions (somites) of the plates soon become separated from the parietal, and form independent masses of cells constituted of two layers, which were originally continuous with the somatic and splanchnic layers of the parietal plates (fig. 79). The outer or somatic layer of the vertebral plates is formed of a single row of cells, but the inner or splanchnic layer is made up of a kernel of cells on the side of the somatic layer and an inner layer. The kernel of the splanchnic layer and the outer or somatic layer together correspond to a muscle- plate of other Vertebrata, and exhibit a similar segmentation.

Osseous Fishes are stated to agree with Amphibians in the development of their somites and muscular system 1 , but further observations on this point are required.

In Birds the horizontal splitting of the mesoblast extends at first to the dorsal summit of the mesoblastic plates, but after the isolation of the somites the split between the somatic and splanchnic layers becomes to a large extent obliterated, though in the anterior somites it appears in part to persist. The somites on the second day, as seen in a transverse section (fig. 115, P.?'.), are somewhat quadrilateral in form but broader than they are deep.

Each at that time consists of a somewhat thick cortex of radi


FlG. 378. HORIZONTALSECTION THROUGH THE TRUNK OF AN EMBRYO OF SCYLL1UM CONSIDERABLY YOUNGER THAN 28 F.


The section is taken at the level of the notochord, and shews the separation of the cells to form the vertebral bodies from the muscle-plates.

ch. notochord ; ep. epiblast ; Vr, rudiment of vertebral body ; mp. muscle- plate ; mp' . portion of muscle-plate already differentiated into longitudinal muscles.


1 Ehrlich, " Ueber den peripher. Theil d. Urwirbel." Archiv f. mikr. Anal., Vol. XI.


THE MUSCULAR SYSTEM. 671

ating rather granular columnar cells, enclosing a small kernel of spherical cells. They are not, as may be seen in the above figure, completely separated from the ventral (or lateral as they are at this period) parts of the mesoblastic plate, and the dorsal and outer layer of the cortex of the somites is continuous with the somatic layer of mesoblast, the remainder of the cortex, with the central kernel, being continuous with the splanchnic layer. Towards the end of the second and beginning of the third day the upper and outer layer of the cortex, together probably with some of the central cells of the kernel, becomes separated off as a muscle-plate (fig. 1 16). The muscle-plate when formed (fig. 117) is found to consist of two layers, an inner and an outer, which enclose between them an almost obliterated central cavity ; and no sooner is the muscle-plate formed than the middle portion of the inner layer becomes converted into longitudinal muscles. The avian muscle-plates have, in fact, precisely the same constitution as those of Elasmobranchii. The central space is clearly a remnant of the vertebral portion of the body cavity, which, though it wholly or partially disappears in a previous stage, reappears again on the formation of the muscle-plate.

The remainder of the somite, after the formation of the muscle-plate, is of very considerable bulk ; the cells of the cortex belonging to it lose their distinctive characters, and the major part of it becomes the vertebral rudiment.

In Mammalia the history appears to be generally the same as in Elasmobranchii. The split which gives rise to the body cavity is continued to the dorsal summit of the mesoblastic plates, and the dorsal portions of the plates with their contained cavities become divided into somites, and are then separated off from the ventral. The later development of the somites has not been worked out with the requisite care, but it would seem that they form somewhat cubical bodies in which all trace of the primitive slit is lost. The further development resembles that in Birds.

The first changes of the mesoblastic somites and the formation of the muscle-plates do not, according to existing statements, take place on quite the same type throughout the Vertebrata, yet the comparison which has been instituted between Elasmobranchs and other Vertebrates appears to prove that there are important common features in their development, which may be regarded as primitive, and as having been inherited from the ancestors of Vertebrates. These features are (i) the extension of the body cavity into the vertebral plates, and subsequent enclosure of this cavity between the two layers of the muscleplates ; (2) the primitive division of the vertebral plate into an outer (somatic) and an inner (splanchnic) layer, and the formation of a large part of the voluntary muscular system out of the inner


THE MUSCLE-PLATES.


sp.c


layer, which in all cases is converted into muscles earlier than the outer layer.

The conversion of the muscle-plates into muscles. It

will be convenient to commence this subject with a description of the changes which take place in such a simple type as that of the Elasmobranchii.

At the time when the muscleplates have become independent structures they form flat two-layered oblong bodies enclosing a slit-like central cavity (fig. 379, mp). The outer or somatic wall is formed of simple epithelial -like cells. The inner or splanchnic wall has however a somewhat complicated structure. It is composed dorsally and ventrally of a columnar epithelium, but in its middle portion of the muscle-cells previously spoken of. Between these and the central cavity of the plates the epithelium forming the remainder of the layer commences to insert itself; so that between the first-formed muscle and the cavity of the muscle-plate there appears a thin layer of cells, not however continuous throughout.

When first formed the muscleplates, as viewed from the exterior, have nearly straight edges ; soon however they become bent in the middle, so that the edges have an obtusely angular form, the apex of the angle being directed forwards. They are so arranged that the anterior edge of the one plate fits into the posterior edge of the one in front. In the lines of junction between the plates layers of connective-tissue cells appear, which form the commencements of the intermuscular septa.

The growth of the plates is very rapid, and their upper ends



FIG. 379. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNGER THAN

28 F.

sp.c. spinal canal ; W. white matter of spinal cord ; pr. posterior nerve-roots ; ch. notochord ; x. sub-notochordal rod ; ao. aorta ; mp. muscle-plate; mp' . inner layer of muscle-plate already converted into muscles ; Vr. rudiment of vertebral body ; si. segmental tube ; sd. segmental duct ; sp.v. spiral valve ; z/. subintestinal vein ; P.O. primitive generative cells.


THE MUSCULAR SYSTEM. 673

soon extend to the summit of the neural canal, and their lower ones nearly meet in the median ventral line. The original band of muscles, whose growth at first is very slow, now increases with great rapidity, and forms the nucleus of the whole voluntary muscular system (fig. 380, mp'). It extends upwards and downwards by the continuous conversion of fresh cells of the splanchnic layer into muscle-cells. At the same time it grows rapidly in thickness by the addition of fresh spindle-shaped muscle-cells from the somatic layer as well as by the division of the already existing cells.

Thus both layers of the muscle-plate are concerned in forming the great longitudinal lateral muscles, though the splanchnic layer is converted into muscles very much sooner than the somatic 1 .

Each muscle-plate is at first a continuous structure, extending from the dorsal to the ventral surface, but after a time it becomes divided by a layer of connective tissue, which becomes developed nearly on a level with the lateral line, into a dorso-lateral and a ventro-lateral section. The ends of the muscle-plates continue for a long time to be formed of undifferentiated columnar cells. The complicated outlines of the inter-muscular septa become gradually established during the later stages of development, causing the well-known appearances of the muscles in transverse sections, which require no special notice here.

The muscles of the limbs. The limb muscles are formed in Elasmobranchii, coincidently with the cartilaginous skeleton, as two bands of longitudinal fibres on the dorsal and ventral surfaces of the limbs (fig. 346). The cells, from which these muscles originate, are derived from the muscle-plates. When the ends of the muscle-plates reach the level of the limbs they bend outwards and enter the tissue of the limbs (fig. 380). Small portions of several muscle-plates (m.pl) come in this way to be situated within the limbs, and are very soon segmented off from the remainder of the muscle-plates. The portions of the muscle-plates thus introduced soon lose their original dis 1 The brothers Hertwig have recently maintained that only the inner layer of the muscle-plates is converted into muscles. In the Elasmobranchs it is easy to demonstrate the incorrectness of this view, and in Acipenser (vide fig. 57, mp) the two layers of the muscle-plate retain their original relations after the cells of both of them have become converted into muscles.

B. in. 43


674


THE MUSCLE-PLATES.


3,-n,



FIG. 380. TRANSVERSE SECTION THROUGH THE ANTERIOR PART OF THE TRUNK OF AN EMBRYO OF SCYLLIUM SLIGHTLY OLDER THAN FIG. 29 B.

The section is diagrammatic in so far that the anterior nerve-roots have been inserted for the whole length ; whereas they join the spinal cord half-way between two posterior roots.

sp.c. spinal cord; sp.g. ganglion of posterior root; ar. anterior root; dn. dorsally directed nerve springing from posterior root; nip. muscle-plate; mp'. part of muscleplate already converted into muscles; vi.pl. part of muscle-plate which gives rise to the muscles of the limbs; /. nervus lateralis; ao. aorta; ch. notochord; sy.g. sympathetic ganglion; ca.v. cardinal vein; sp.n. spinal nerve; sd. segmental (archinephric) duct; st. segmental tube; du. duodenum; pan. pancreas; hp.d. point of junction of hepatic duct with duodenum ; umc. umbilical canal.


THE MUSCULAR SYSTEM. 675

tinctness. There can however be but little doubt that they supply the tissue for the muscles of the limbs. The muscleplates themselves, after giving off buds to the limbs, grow downwards, and soon cease to shew any trace of having given off these buds.

In addition to the longitudinal muscles of the trunk just described, which are generally characteristic of Fishes, there is found in Amphioxus a peculiar transverse abdominal muscle, extending from the mouth to the abdominal pore, the origin of which has not been made out.

It has already been shewn that in all the higher Vertebrata muscle-plates appear, which closely resemble those in Elasmobranchii; so that all the higher Vertebrata pass through, with reference to their muscular system, a fish- like stage. The middle portion of the inner layers of their muscle-plates becomes, as in Elasmobranchii, converted into muscles at a very early period, and the outer layer for a long time remains formed of indifferent cells. That these muscle-plates give rise to the main muscular system of the trunk, at any rate to the episkeletal muscles of Huxley, is practically certain, but the details of the process have not been made out.

In the Perennibranchiata the fish-like arrangement of muscles is retained through life in the tail and in the dorso-lateral parts of the trunk. In the tail of the Amniotic Vertebrata the primitive arrangement is also more or less retained, and the same holds good for the dorso-lateral trunk muscles of the Lacertilia. In the other Amniota and the Anura the dorso-lateral muscles have become divided up into a series of separate muscles, which are arranged in two main layers. It is probable that the intercostal muscles belong to the same group as the dorso-lateral muscles.

The abdominal muscles of the trunk, even in the lowest Amphibia, exhibit a division into several layers. The recti abdominis are the least altered part of this system, and usually retain indications of the primitive inter-muscular septa, which in many Amphibia and Lacertilia are also to some extent preserved in the other abdominal muscles.

In the Amniotic Vertebrates there is formed underneath the vertebral column and the transverse processes a system of muscles, forming part of the hyposkeletal system of Huxley, and called by Gegenbaur the subvertebral muscles. The development of this system has not been worked out, but on the whole I am inclined to believe that it is derived from the muscle-plates. Kolliker, Huxley and other embryologists believe however that these muscles are independent of the muscle-plates in their origin.

432


676 THE HEAD-CAVITIES.


Whether the muscle of the diaphragm is to be placed in the same category as the hyposkeletal muscles has not been made out.

It is probable that the cutaneous muscles of the trunk are derived from the cells given off from the muscle-plates. Kolliker however believes that they have an independent origin.

The limb-muscles, both extrinsic and intrinsic, as may be concluded from their development in Elasmobranchii, are derived from the muscleplates. Kleinenberg found in Lacertilia a growth of the muscle-plates into the limbs, and in Amphibia Gotte finds that the outer layer of the muscle-plates gives rise to the muscles of the limbs.

In the higher Vertebrata on the other hand the entrance of the muscleplates into the limbs has not been made out (Kolliker). It seems therefore probable that by an embryological modification, of which instances are so frequent, the cells which give rise to the muscles of the limbs in the higher Vertebrata can no longer be traced into a direct connection with the muscleplates.

TJte Somites and muscular system of the head.

The extension of the somites to the anterior end of the body in Amphioxus clearly proves that somites, similar to those of the trunk, were originally present in a region, which in the higher Vertebrata has become differentiated into the head. In the adult condition no true Vertebrate exhibits indications of such somites, but in the embryos of several of the lower Vertebrata structures have been found, which are probably equivalent to the somites of the trunk : they have been frequently alluded to in the previous chapters of this volume. These structures have been most fully worked out in Elasmobranchii.

The mesoblast in Elasmobranch embryos becomes first split into somatic and splanchnic layers in the region of the head ; and between these layers there are formed two cavities, one on each side, which end in front opposite the blind anterior extremity of the alimentary canal ; and are continuous behind with the general body-cavity (fig. 20 A, vp}. I propose calling them the head-cavities. The cavities of the two sides have no communication with each other.

Coincidently with the formation of an outgrowth from the throat to form the first visceral cleft, the head-cavity on each side becomes divided into a section in front of the cleft and a section behind the cleft ; and at a later period it becomes, owing to the formation of a second cleft, divided into three sections :


THE MUSCULAR SYSTEM.


677


vn~.



(i) a section in front of the first or hyomandibular cleft; (2) a section in the hyoid arch between the hyomandibular cleft and the hyobranchial or first branchial cleft ; (3) a section behind the first branchial cleft.

The front section of the head-cavity grows forward, and soon becomes divided, without the intervention of a visceral cleft, into an anterior and posterior division. The anterior lies close to the eye, and in front of the commencing mouth involution. The posterior part lies completely within the mandibular arch.

As the rudiments of the successive visceral clefts are formed, the posterior part of the head-cavity becomes divided into successive sections, there being one section for each arch. Thus the whole headcavity becomes on each side divided into (i) a premandibular section ; (2) a mandibular section (vide fig. 29 A, PP] > (3) a hyoid section ; (4) sections in each of the branchial arches.

The first of these divisions forms a space of a considerable size, with epithelial walls of somewhat short columnar cells (fig. 381, ipp}. It is situated close to the eye, and presents a rounded or sometimes a triangular figure in section. The two halves of the cavity are prolonged ventralwards, and meet below the base of the fore-brain. The connection between them appears to last for a considerable time. These two cavities are the only parts of the body-cavity within the head which unite ventrally. The section of the head-cavity just described is so similar to the remaining sections that it must be considered as serially homologous with them.

The next division of the head-cavity, which from its position


FIG. 381. TRANSVERSE SECTION THROUGH THE FRONT PART OF THE HEAD OF A YOUNG PRISTIURUS EMBRYO.

The section, owing to the cranial flexure, cuts both the foreand the hind-brain. It shews the premandibular and mandibular head-cavities ipp and ipp, etc. The section is moreover somewhat oblique from side to side.

fb. fore-brain ; /. lens of eye ; m. mouth ; pt. upper end of mouth, forming pituitary involution; lao. mandibular aortic arch; ipp. and ipp. first and second head-cavities; \vc. first visceral cleft; V. fifth nerve ; aim. auditory nerve ; VII. seventh nerve ; aa. dorsal aorta ; acv. anterior cardinal vein ; ch, notochord.


678 THE HEAD-CAVITIES.

may be called the mandibular cavity, presents a spatulate shape, being dilated dorsally, and produced ventrally into a long thin process parallel to the hyomandibular gill-cleft (fig. 20, pp}. Like the previous space it is lined by a short columnar epithelium.

The mandibular aortic arch is situated close to its inner side (fig. 381, 2pp). After becoming separated from the lower part (Marshall), the upper part of the cavity atrophies about the time of the appearance of the external gills. Its lower part also becomes much narrowed, but its walls of columnar cells persist. The outer or somatic wall becomes very thin indeed, the splanchnic wall, on the other hand, thickens and forms a layer of several rows of elongated cells. In each of the remaining arches there is a segment of the original body-cavity fundamentally similar to that in the mandibular arch (fig. 382). A dorsal dilated portion appears, however, to be present in the third or hyoid section alone (fig. 20), and even there disappears very soon, after being segmented off from the lower part (Marshall). The cavities in the posterior parts of the head become much reduced like those in its anterior part, though at rather a later period. FlG . 382 . HORIZONTAL

It has been shewn that the divi- SECTION THROUGH THE PENULTIMATE VISCERAL ARCH OF

sions of the body-cavity in the head, AN EMBRYO OF PRISTIURUS. with the exception of the anterior, e p. epiblast; vc. pouch of early become atrophied, not so how- hypoblast which will form the

walls of a visceral cleit ; //. CVer their walls. The cells forming segment of body-cavity in vis the walls both of the dorsal and ven- ceral arch ; aa ' aortic arch ' tral sections of these cavities become elongated, and finally become converted into muscles. Their exact history has not been followed in its details, but they almost unquestionably become the musculus contrictor superficialis and musculus interbranchialis 1 ; and probably also musculus levator mandibuli and other muscles of the front part of the head.

The anterior cavity close to the eye remains unaltered much longer than the remaining cavities.

1 Vide Vetter, " Die Kiemen und Kiefermusculatur d. Fische." Jenaische Zcltschrift, Vol. vn.



THE MUSCULAR SYSTEM.


679


Its further history is very interesting. In my original account of this cavity (No. 292, p. 208) I stated my belief that its walls gave rise to the eye-muscles, and the history of this process has been to some extent worked out by Marshall in his important memoir (No. 509).

Marshall finds that the ventral portion of this cavity, where its two halves meet, becomes separated from the remainder. The eventual fate of this part has not however been followed. Each dorsal section acquires a cup-like form, investing the posterior and inner surface of the eye. The cells of its outer wall subsequently give rise to three sets of muscles. The middle of these, partly also derived from the inner walls of the cup, becomes the rectus internus of the eye, the dorsal set forms the rectus superior, and the ventral the rectus inferior. The obliquus inferior appears also to be in part developed from the walls of this cavity.

Marshall brings evidence to shew that the rectus externus (as might be anticipated from its nerve supply) has no connection with the walls of the premandibular head-cavity, and finds that it arises close to the position originally occupied by the second and third cavities. Marshall has not satisfactorily made out the mode of development of the obliquus superior.

The walls of the cavities, whose history has just been recorded, have definite relations with the cranial nerves, an account of which has already been given at p. 461.

Head-cavities, in the main similar to those of Elasmobranchii, have been found in the embryo of Petromyzon (fig. 45, /ic\ the Newt (Osborn and Scott), and various Reptilia (Parker).

BIBLIOGRAPHY.

(507) G.M.Humphry. " Muscles in Vertebrate Animals." Journ. of Anat. and Phys., Vol. vi. 1872.

(508) J. Miiller. " Vergleichende Anatomic d. Myxinoiden. Part I. Osteologie u. Myologie." Akad. Wiss., Berlin, 1834.

(509) A. M. Marshall. "On the head cavities and associated nerves of Elasmobranchs." Quart. J. of Micr. Science, Vol. xxi. 1881.

(510) A. Schneider. " Anat. u. Entwick. d. Muskelsystems d. Wirbelthierc." Silz. d. Oberhessischen Gesellschaft, 1873.

(511) A. Schneider. Beitrdge z. vergleich. Anat. . Entwick. d. Wirbelthiere. Berlin, 1879.

Vide 2^0 Gotte (No. 296), Kolliker (N o. 298), Balfour (No. 292), Huxley, etc.


CHAPTER XXIII.


EXCRETORY ORGANS.


EXCRETORY organs consist of coiled or branched and often ciliated tubes, with an excretory pore opening on the outer surface of the body, and as a rule an internal ciliated orifice placed in the body-cavity. In forms provided with a true vascular system, there is a special development of capillaries around the glandular part of the excretory organs. In many instances the glandular cells of the organs are filled with concretions of uric acid or some similar product of nitrogenous waste.

There is a very great morphological and physiological similarity between almost all the forms of excretory organ found in the animal kingdom, but although there is not a little to be said for holding all these organs to be derived from some common prototype, the attempt to establish definite homologies between them is beset with very great difficulties.

Platyelminthes. Throughout the whole of the Platyelminthes these organs are constructed on a well-defined type, and in the Rotifera excretory organs of a similar form to those of the Platyelminthes are also present.

These organs (Fraipont, No. 513) are more or less distinctly paired, and consist of a system of wide canals, often united into a network, which open on the one hand into a pair of large tubes leading to the exterior, and on the other into fine canals which terminate by ciliated openings, either in spaces between the connective-tissue cells (Platyelminthes), or in the body-cavity (Rotifera). The fine canals open directly into the larger ones, without first uniting into canals of an intermediate size.


EXCRETORY ORGANS.


68 1


The two large tubes open to the exterior, either by means of a median posteriorly placed contractile vesicle, or by a pair of vesicles, which have a ventral and anterior position. The former type is characteristic of the majority of the Trematoda, Cestoda. and Rotifera, and the latter of the Nemertea and some Trematoda. In the Turbellaria the position of the external openings of the system is variable, and in a few Cestoda (Wagner) there are lateral openings on each of the successive proglottides, in addition to the terminal openings. The mode of development of these organs is unfortunately not known.

Mollusca. In the Mollusca there are usually present two independent pairs of excretory organs one found in a certain number of forms during early larval life only 1 , and the other always present in the adult.

The larval excretory organ has been found in the pulmonate Gasteropoda (Gegenbaur, Fol 2 , Rabl), in Teredo (Hatschek), and possibly also in Paludina. It is placed in the anterior region of the body, and opens ventrally on each side, a short way behind the velum. It is purely a larval organ, disappearing before the close of the veliger stage. In the aquatic Pulmonata, where it is best developed, it consists on each side of a V-shaped tube, with a dorsally-placed apex, containing an enlargement of the lumen. There is a ciliated cephalic limb, lined by cells with concretions, and terminating by an internal opening near the eye, and a nonciliated pedal limb opening to the exterior 3 .

Two irreconcilable views are held as to the development of this system. Rabl (Vol. II. No. 268) and Hatschek hold that it is developed in the mesoblast ; and Rabl states that in Planorbis it is formed from the anterior mesoblast cells of the mesoblastic bands. A special mesoblast cell on each side elongates into two processes, the commencing limbs of the future organ. A lumen is developed in this cell, which is continued into each limb, while

1 I leave out of consideration an external renal organ found in many marine Gasteropod larvte, vide Vol. II. p. 280.

2 H. Fol, "Etudes sur le devel. d. Mollusques. " Mem. Hi. Archiv d. Zool. exfJr. et gener., Vol. VIII.

3 The careful observations of Fol seem to me nearly conclusive in favour of this limb having an external opening, and the statement to the reverse effect on p. 280 of Vol. ii. of this treatise, made on the authority of Rabl and Biitschli, must probably be corrected.


682 POLYZOA.

the continuations of the two limbs are formed by perforated mesoblast cells.

According to Fol these organs originate in aquatic Pulmonata as a pair of invaginations of the epiblast, slightly behind the mouth. Each invagination grows in a dorsal direction, and after a time suddenly bends on itself, and grows ventralwards and forwards. It thus acquires its V-shaped form.

In the terrestrial Pulmonata the provisional excretory organs are, according to Fol, formed as epiblastic invaginations, in the same way as those in the aquatic Pulmonata, but have the form of simple non-ciliated sacks, without internal openings.

The permanent renal organ of the Mollusca consists typically of a pair of tubes, although in the majority of the Gasteropoda one of the two tubes is not developed. It is placed considerably behind the provisional renal organ.

Each tube, in its most typical form, opens by a ciliated funnel into the pericardial cavity, and has its external opening at the side of the foot. The pericardial funnel leads into a glandular section of the organ, the lining cells of which are filled with concretions. This section is followed by a ciliated section, from which a narrow duct leads to the exterior.

As to the development of this organ the same divergence of opinion exists as in the case of the provisional renal organ.

Rabl's careful observations on Planorbis (Vol. II. No. 268) tend to shew that it is developed from a mass of mesoblast cells, near the end of the intestine. The mass becomes hollow, and, attaching itself to the epiblast on the left side of the anus, acquires an opening to the exterior. Its internal opening is not established till after the formation of the heart. Fol gives an equally precise account, but states that the first rudiment of the organ arises as a solid mass of epiblast cells. Lankester finds that this organ is developed as a paired invagination of the. epiblast in Pisidium, and Bobretzky also derives it from the epiblast in marine Prosobranchiata. In Cephalopoda on the other hand Bobretzky's observations (I conclude this from his figures) indicate that the excretory sacks of the renal organs are derived from the mesoblast.

Polyzoa. Simple excretory organs, consisting of a pair of ciliated canals, opening between the mouth and the anus, have


EXCRETORY ORGAN>.


68 3


been found by Hatschek and Joliet in the Entoproctous Polyzoa, and are developed, according to Hatschek, by whom they were first found in the larva, from the mesoblast

Brachiopoda. One or rarely two (Rhynchonella) pairs of canals, with both peritoneal and external openings, are found in the Brachiopoda. They undoubtedly serve as genital ducts, but from their structure are clearly of the same nature as the excretory organs of the Chaetopoda described below. Their development has not been worked out.

Chaetopoda. Two forms of excretory organ have been met with in the Chaetopoda. The one form is universally or nearly universally present in the adult, and typically consists of a pair of coiled tubes repeated in every segment. Each tube has an internal opening, placed as a rule in the segment in front of that in which the greater part of the organ and the external opening are situated.

There are great variations in the structure of these organs, which cannot be dealt with here. It may be noted however that the internal opening may be absent, and that there may be several internal openings for each organ (Polynoe). In the Capitellidae moreover several pairs of excretory tubes have been shewn by Eisig (No. 512) to be present in each of the posterior segments.

The second form of excretory organ has as yet only been found in the larva of Polygordius, and will be more conveniently dealt with in connection with the development of the excretory system of this form.

There is still considerable doubt as to the mode of formation of the excretory tubes of the Chaetopoda. Kowalevsky (No. 277), from his observations on the Oligochasta, holds that they develop as outgrowths of the epithelial layer covering the posterior side of the dissepiments, and secondarily become connected with the epidermis.

Hatschek finds that in Criodrilus they arise from a continuous linear thickening of the somatic mesoblast, immediately beneath the epidermis, and dorsal to the ventral band of longitudinal muscles. They break up into S-shaped cords, the anterior end of each of which is situated in front of a dissepiment, and is formed at first of a single large cell, while the posterior part is


684 CHvETOPODA.


continued into the segment behind. The cords are covered by a peritoneal lining, which still envelopes them, when in the succeeding stage they are carried into the body-cavity. They subsequently become hollow, and their hinder ends acquire openings to the exterior. The formation of their internal openings has not been followed.

Kleinenberg is inclined to believe that the excretory tubes take their origin from the epiblast, but states that he has not satisfactorily worked out their development.

The observations of Risig (No. 512) on the Capitellidae support Kowalevsky's view that the excretory tubes originate from the lining of the peritoneal cavity.

Hatschek (No. 514) has given a very interesting account of the development of the excretory system in Polygordius.

The excretory system begins to be formed, while the larva is still in the trochospere stage (fig. 383, npli), and consists of a provisional excretory organ, which is placed in front of the future segmented part of the body, and occupies a position very similar to that of the provisional excretory organ found in some Molluscan larvae (vide p. 68 1).

Hatschek, with some shew of reason, holds that the provisional excretory organs of Polygordius are homologous with those of the Mollusca.

In its earliest stage the provisional excretory organ of Polygordius consists of a pair of simple ciliated tubes, FIG. 383. POLYOORDIUS

, . , r 11-1 LARVA. (After Hatschek.)

each with an anterior funnel-like open- m _ moulh . ^ supraKBSO .

ing situated in the midst of the meSO- phageal ganglion ; nph. nephri11 11 . , dion ; ine.p. mesoblastic band;

blast cells, and a posterior external an _ anus 5 oL stomach . opening. The latter is placed immediately in front of what afterwards becomes the segmented region of the embryo. While the larva is still unsegmented, a second internal opening is formed for each tube (fig. 383, np/i) and the two openings so formed may eventually become divided into five (fig. 384 A), all communicating by a single pore with the exterior.

When the posterior region of the embryo becomes segmented,



EXCRETORY ORGANS.


685


paired excretory organs are formed in each of the posterior segments, but the account of their development, as given by Hatschek, is so remarkable that I do not think it can be definitely accepted without further confirmation.

From the point of junction of the two main branches of the larval kidney there grows backwards (fig. 384 B), to the hind end of the first segment, a very delicate tube, only indicated by its ciliated lumen, its walls not being differentiated. Near the front end of this tube a funnel, leading into the larval body cavity of the head, is formed, and subsequently the posterior end of the tube acquires an external opening, and the tube distinct walls. The communication with the provisional excretory organ is then lost, and thus the excretory tube of the first segment is established.

The excretory tubes in the second and succeeding segments are formed in the same way as in the first, i.e. by the continuation of the lumen of the hind end of the excretory tube from the preceding segment, and the subsequent separation of this part as a separate tube.

The tube may be continued with a sinuous course through



A A

A +

A.


Y

Y Y Y Y


J)


FIG. 384. DIAGRAM ILLUSTRATING THE DEVELOPMENT OF THE EXCRETORY SYSTEM OF POLYGORDIUS. (After Hatschek.)

several segments without a distinct wall. The external and internal openings of the permanent excretory tubes are thus secondarily acquired. The internal openings communicate with the permanent body-cavity. The development of the perma


686 GEPHYREA.


nent excretory tubes is diagrammatically represented in fig. 384 C and D.

The provisional excretory organ atrophies during larval life.

If Hatschek's account of the development of the excretory system of Polygordius is correct, it is clear that important secondary modifications must have taken place in it, because his description implies that there sprouts from the anterior excretory organ, while it has its own external opening, a posterior duct, which does not communicate either with the exterior or with the body-cavity! Such a duct could have no function. It is intelligible either (i) that the anterior excretory organ should lead into a longitudinal duct, opening posteriorly ; that then a series of secondary openings into the body-cavity should attach themselves to this, that for each internal opening an external should subsequently arise, and the whole break up into separate tubes ; or (2) that behind an anterior provisional excretory organ a series of secondary independent segmental tubes should be formed. But from Hatschek's account neither of these modes of evolution can be deduced.

Gephyrea. The Gephyrea may have three forms of excretory organs, two of which are found in the adult, and one, similar in position and sometimes also in structure, to the provisional excretory organ of Polygordius, has so far only been found in the larvae of Echiurus and Bonellia.

In all the Gephyrea the so-called 'brown tubes' are apparently homologous with the segmented excretory tubes of Chaetopods. Their main function appears to be the transportation of the generative products to the exterior. There is but a single highly modified tube in Bonellia, forming the oviduct and uterus ; a pair of tubes in the Gephyrea inermia, and two or three pairs in most Gephyrea armata, except Bonellia. Their development has not been studied.

In the Gephyrea armata there is always present a pair of posteriorly placed excretory organs, opening in the adult into the anal extremity of the alimentary tract, and provided with numerous ciliated peritoneal funnels. These organs were stated by Spengel to arise in Bonellia as outgrowths of the gut ; but in Echinrus Hatschek (No. 515) finds that they are developed from the somatic mesoblast of the terminal part of the trunk. They soon become hollow, and after attaching themselves to the epiblast on each side of the anus, acquire external openings. They are not at first provided with peritoneal funnels, but these parts of the organs become developed from a ring of cells at


EXCRETORY ORGANS.


687


their inner extremities ; and there is at first but a single funnel for each vesicle. The mode of increase of the funnels has not been observed, nor has it been made out how the organs themselves become attached to the hind-gut.

The provisional excretory organ of Echiurus is developed at an early larval stage, and is functional during the whole of larval life. It at first forms a ciliated tube on each side, placed in front of that part of the larva which becomes the trunk of the adult. It opens to the exterior by a fine pore on the ventral side, immediately in front of one of the mesoblastic bands, and appears to be formed of perforated cells. It terminates internally in a slight swelling, which represents the normal internal ciliated funnel. The primitively simple excretory organ becomes eventually highly complex by the formation of numerous branches, each ending in a slightly swollen extremity. These branches, in the later larval stages, actually form a network, and the inner end of each main branch divides into a bunch of fine tubes. The whole organ resembles in many respects the excretory organ of the Platyelminthes.

In the larva of Bonellia Spengel has described a pair of provisional excretory tubes, opening near the anterior end of the body, which are probably homologous with the provisional excretory organs of Echiurus (vide Vol. II., fig. 162 C, se).

Discophora. As in many of the types already spoken of, permanent and provisional excretory organs may be present in the Discophora. The former are usually segmentally arranged, and resemble in many respects the excretory tubes of the Chaetopoda. They may either be provided with a peritoneal funnel (Nephelis, Clepsine) or have no internal opening (Hirudo).

Bourne 1 has shewn that the cells surrounding the main duct in the medicinal Leech are perforated by a very remarkable network of ductules, and the structure of these organs in the Leech is so peculiar that it is permissible to state with due reserve their homology with the excretory organs of the Chaetopoda.

The excretory tubes of Clepsine are held by Whitman to be developed in the mesoblast.

1 "On the Structure of the Nephridia of the Medicinal Leech." Quart. J. of Micr. Science, Vol. XX. 1880.


688 ARTHROPODA.


There are found in the embryos of Nephelis and Hirudo certain remarkable provisional excretory organs the origin and history of which are not yet fully made out. In Nephelis they appear as one (according to Robin), or (according to Biitschli) as two successive pairs of convoluted tubes on the dorsal side of the embryo, which are stated by the latter author to develop from the scattered mesoblast cells underneath the skin. At their fullest development they extend, according to Robin, from close to the head to near the ventral sucker. Each of them is U-shaped, with the open end of the U forwards, each limb of the U being formed by two tubes united in front. No external opening has been clearly made out. Fiirbringer is inclined from his own researches to believe that they open laterally. They contain a clear fluid.

In Hirudo, Leuckart has described three similar pairs of organs, the structure of which he has fully elucidated. They are situated in the posterior part of the body, and each of them commences with an enlargement, from which a convoluted tube is continued for some distance backwards; the tube then turns forwards again, and after bending again upon itself opens to the exterior. The anterior part is broken up into a kind of labyrinthic network.

The provisional excretory organs of the Leeches cannot be identified with the anterior provisional organs of Polygordius and Echiurus.

Arthropoda. Amongst the Arthropoda Peripatus is the only form with excretory organs of the type of the segmental excretory organs of the Chsetopoda 1 .

These organs are placed at the bases of the feet, in the lateral divisions of the body-cavity, shut off from the main median division of the body-cavity by longitudinal septa of transverse muscles.

Each fully developed organ consists of three parts :

(i) A dilated vesicle opening externally at the base of a foot. (2) A coiled glandular tube connected with this, and subdivided again into several minor divisions. (3) A short terminal portion opening at one extremity into the coiled tube

1 Vide F. M. Balfour, " On some points in the Anatomy of Peripatus Capensis." Quart. J, of Micr. Science, Vol. XIX. 1879.


EXCRETORY ORGANS. 689


and at the other, as I believe, into the body cavity. This section becomes very conspicuous, in stained preparations, by the intensity with which the nuclei of its walls absorb the colouring matter.

In the majority of the Tracheata the excretory organs have the form of the so-called Malpighian tubes, which always (vide Vol. II.) originate as a pair of outgrowths of the epiblastic proctodaeum. From their mode of development they admit of comparison with the anal vesicles of the Gephyrea, though in the present state of our knowledge this comparison must be regarded as somewhat hypothetical.

The antennary and shell-glands of the Crustacea, and possibly also the so-called dorsal organ of various Crustacean larvae appear to be excretory, and the two former have been regarded by Claus and Grobben as belonging to the same system as the segmental excretory tubes of the Chaetopoda.

Nematoda. Paired excretory tubes, running for the whole length of the body in the so-called lateral line, and opening in front by a common ventral pore, are present in the Nematoda. They do not appear to communicate with the body cavity, and their development has not been studied.

Very little is known with reference either to the structure or development of excretory organs in the Echinodermata and the other Invertebrate types of which no mention has been so far made in this Chapter.

Excretory organs and generative ducts of the Craniata.

Although it would be convenient to separate, if possible, the history of the excretory organs from that of the generative ducts, yet these parts are so closely related in the Vertebrata, in some cases the same duct having at once a generative and a urinary function, that it is not possible to do so.

The excretory organs of the Vertebrata consist of three distinct glandular bodies and of their ducts. These are (i) a small glandular body, usually with one or more ciliated funnels opening into the body cavity, near the opening of which there projects into the body cavity a vascular glomerulus. It is situated very far forwards, and is usually known as the head 44


690 ELASMOBRANCHII.


kidney, though it may perhaps be more suitably called, adopting Lankester's nomenclature, the pronepliros. Its duct, which forms the basis for the generative and urinary ducts, will be called the segmented duct.

(2) The Wolffian body, which may be also called the mesonepJiros. It consists of a series of, at first, segmentally (with a few exceptions) arranged glandular canals (segmental tubes) primitively opening at one extremity by funnel-shaped apertures into the body cavity, and at the other into the segmental duct. This duct becomes in many forms divided longitudinally into two parts, one of which then remains attached to the segmental tubes and forms the Wolffian or mesonepJiric duct, while the other is known as the Milllerian dnct.

(3) The kidney proper or metanephros. This organ is only found in a completely differentiated form in the amniotic Vertebrata. Its duct is an outgrowth from the Wolrfian duct.

The above parts do not coexist in full activity in any living adult member of the Vertebrata, though all of them are found together in certain embryos. They are so intimately connected that they cannot be satisfactorily dealt with separately.

Elasmobranchii. The excretory system of the Elasmobranchii is by no means the most primitive known, but at the same time it forms a convenient starting point for studying the modifications of the system in other groups. The most remarkable peculiarity it presents is the absence of a pronephros. The development of the Elasmobranch excretory system has been mainly studied by Semper and myself.

The first trace of the system makes its appearance as a knob of mesoblast, springing from the intermediate cell-mass near the level of the hind end of the heart (fig. 385 K,pd). 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 (fig. 385 B, pd). 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 (fig. 421, sd) continuous with a lumen, which


EXCRETORY ORGANS.


691


makes its appearance in the column (fig. 386, sd). The knob forms the only structure which can be regarded as a rudiment of the pronephros.


spn


spn



FlG. 385. TWO SECTIONS OF A PRISTIURUS EMBRYO WITH THREE VISCERAL

CLEFTS.

The sections illustrate the development of the segmental duct (pd) or primitive duct of the pronephros. In A (the anterior of the two sections) this appears as a solid knob (pd) projecting towards the epiblast. In B is seen a section of the column which has grown backwards from the knob in A.

spn. rudiment of a spinal nerve; me. medullary canal; ch. notochord; X. subnotochordal rod; mp. muscle-plate; mp' . specially developed portion of muscle-plate; ao. dorsal aorta ; pd. segmental duct ; so. somatopleure ; sp. splanchnopleure ; //. body cavity; ep. epiblast; al. alimentary canal.

While the lumen is gradually being formed, the segmental tubes of the mesonephros become established. They appear to arise as differentiations of the parts of the primitive lateral plates of mesoblast, placed between the dorsal end of the body cavity and the muscle-plate (fig. 386, st) 1 , which are usually known as the intermediate cell-masses.

The lumen of the segmental tubes, though at first very small, soon becomes of a considerable size. It appears to be established in the position of the section of the body cavity in the intermediate cell-mass, which at first unites the part of the body cavity in the muscle-plates with the permanent body cavity. The lumen of each tube opens at its lower end into the dorsal part of the body cavity (fig. 386, st}, and each tube curls obliquely

1 In my original account of the development I held these tubes to be invaginations of the peritoneal epithelium. Sedgwick (No. 549) was led to doubt the accuracy of my original statement from his investigations on the chick ; and from a re-examination of my specimens he arrived at the results stated above, and which I am now myself inclined to adopt.

442


692


ELASMOBRANCHII.


sp.c



backwards round the inner and dorsal side of the segmental duct, near which it at first ends blindly.

One segmental tube makes its appearance for each somite (fig. 265), commencing with that immediately behind the abdominal opening of the segmental duct, the last tube being situated a few segments behind the anus. Soon after their formation the blind ends of the segmental tubes come in contact with, and open into the segmental duct, and each of them becomes divided into four parts. These are (i) a section carrying the peritoneal opening, known as the peritoneal funnel, (2) a dilated vesicle into which this opens, (3) a coiled tubulus proceeding from (2), and terminating in (4) a wider portion opening into the segmental duct. At the same time, or shortly before this, each segmental duct unites with and opens into one of the horns of the cloaca, and also retires from its primitive position between the epiblast and mesoblast, and assumes a position close to the epithelium lining the body cavity (fig. 380, sd}. The general features of the excretory organs at this period are diagrammatically represented in the woodcut (fig. 387). In this fig. pd is the segmental duct and o its abdominal opening; s.t points to the segmental tubes, the finer details of whose structure are not represented in the diagram. The mesonephros thus forms at this period an elongated gland composed of a series of isolated coiled tubes, one extremity of each of which opens into the body cavity, and the other into the segmental duct, which forms the only duct of the system, and communicates at its front end with the body cavity, and behind with the cloaca.


FIG. 386. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNGER THAN

28 F.

sp.c. spinal canal; W. white matter of spinal cord ; pr. posterior nerve-roots ; ch. notochord ; x. sub-notochordal rod ; ao. aorta ; nip, muscle-plate ; nip', inner layer of muscle-plate already converted into muscles ; Vr, rudiment of vertebral body ; st. segmental tube; sd. segmental duct; sp.v. spiral valve ; v. subintestinal vein ; p.o. primitive generative cells.


EXCRETORY ORGANS. 693


The next important change concerns the segmental duct, which becomes longitudinally split into two complete ducts in the female, and one complete duct and parts of a second duct in the male. The manner in which this takes place is diagrammatically represented in fig. 387 by the clear line x, and in transverse section in figs. 388 and 389. The resulting ducts are (i) the Wolffian duct or mesonephric duct (wd\ dorsally, which remains continuous with the excretory tubules of the mesonephros, and ventrally (2) the oviduct or Miillerian duct in the female, and the rudiments of this duct in the male. In the



FIG. 387. DIAGRAM OF THE PRIMITIVE CONDITION OF THE KIDNEY IN AN

ELASMOBRANCH EMBRYO.

pd. segmental duct. It opens at o into the body cavity and at its other extremity into the cloaca; x. line along which the division appears which separates the segmental duct into the Wolffian duct above and the Miillerian duct below; s.t. segmental tubes. They open at one end into the body cavity, and at the other into the segmental duct.

female the formation of these ducts takes place (fig. 389) 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. This nearly solid cord is the Miillerian duct (pd}. A very small portion of the lumen of the original segmental duct is perhaps continued into it, but in any case it very soon acquires a wide lumen (fig. 389 A). The anterior part of the segmental duct is not divided, but remains continuous with the Mullerian duct, of which its anterior pore forms the permanent peritoneal opening 1 (fig. 387). 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 these ducts in the male differs from that in the female chiefly

1 Five or six segmental tubes belong to the region of the undivided anterior part of the segmental duct, which forms the front end of the Mullerian duct ; but they appear to atrophy very early, without acquiring a definite attachment to the segmental duct.


694


ELASMOBRANCHIL


in the fact of the anterior undivided part of the segmental duct, which forms the front end of the Miillerian duct, being shorter,



trd/



FIG. 389. FOUR SECTIONS THROUGH THE ANTERIOR I'ART OF THE SEGMENTAL DUCT OF A FEMALE EMBRYO OF SCYLLIUM CANICULA.

The figure shews how the segmental duct becomes split into the Wolffian or mesonephric duct above, and Miillerian duct or oviduct below.

wd. Wolffian or mesonephric duct; od. Miillerian duct or oviduct ; sd. segmental duct.


FIG. 388. DIAGRAMMATIC REPRESENTATION OF A TRANSVERSE SECTION OF A

SCYLLIUM EMBRYO ILLUSTRATING THE FORMATION OF THE WOLFFIAN AND MlJLLERIAN DUCTS BY THE LONGITUDINAL SPLITTING OF THE SEGMENTAL DUCT.

me. medullary canal; mp. muscle-plate; ch. notochord; ao. aorta; cav. cardinal vein; st. segmental tube. On the left side the section passes through the opening of a segmental tube into the body cavity. On the right this opening is represented by dotted lines, and the opening of the segmental tube into the Wolffian duct has been cut through; iv.d. Wolffian duct; m.d. Miillerian duct. The section is taken through the point where the segmental duct and Wolffian duct have just become separate; gr. the germinal ridge with the thickened germinal epithelium ; /. liver ; i. intestine with spiral valve.

and in the column of cells with which it is continuous being from the first incomplete.

The segmental tubes of the mesonephros undergo further important changes. The vesicle at the termination of each peritoneal funnel sends a bud forwards towards the preceding tubulus, which joins the fourth section of it close to the opening


EXCRETORY ORGANS.


695



into the Wolffian duct (fig. 390, px). The remainder of the vesicle becomes converted into a Malpighian body (mg}.

By the first of these changes 10^-4 M @W>f a tube is established connecting each pair of segments of the mesonephros, and though this tube is in part aborted (or only represented by a fibrous band) in the anterior part of the excretory organs in the adult, and most probably in the hinder part, yet it seems almost certain that the secondary and tertiary Malpighian bodies of the majority of segments are developed from its persisting blind end. Each of these


FIG. 390. LONGITUDINAL VERTICAL SECTION THROUGH PART OF THE MESONEPHROS OF AN EMBRYO OF SCYLLIUM.

The figure contains two examples of the budding of the vesicle of a segmental tube (which forms a Malpighian body in its own segment) to unite with the tubulus in the preceding segment close to its opening into the Wolffian (mesonephric) duct.

ge. epithelium of body-cavity; st. peritoneal funnel of segmental tube with its peritoneal opening; mg. Malpighian body; px. bud from Malphigian body uniting with preceding segment.


secondary and tertiary Malpighian bodies is connected with a convoluted tubulus (fig. 391, a.mg), which is also developed from the tube connecting each pair of segmental tubes, and therefore falls into the primary tubulus close to its junction with the


st.c



w.d


FIG. 391. THREE SEGMENTS OF THE ANTERIOR PART OF THE MESONEPHROS OF A NEARLY RIPE EMBRYO OF SCYLLIUM CANICULA AS A TRANSPARENT OBJECT. The figure shews a fibrous band passing from the primary to the secondary Malpighian bodies in two segments, which is the remains of the outgrowth from the primary Malpighian body.

sf.o. peritoneal funnel; p. ing. primary Malpighian body; a.mg. accessory Malpighian body; w.d. mesonephric (Wolffian) duct.


696 ELASMOBRANCI1II.


segmental duct. Owing to the formation of the accessory tubuli the segments of the mesonephros acquire a compound character.

The third section of each tubulus becomes by continuous growth, especially in the hinder segments, very bulky and convoluted.

The general character of a slightly developed segment of the mesonephros at its full growth may be gathered from fig. 391. It commences with (i) a peritoneal opening, somewhat oval in form (st.d) and leading directly into (2) a narrow tube, the segmental tube, which takes a more or less oblique course backwards, and, passing superficially to the Wolffian duct (w.d}, opens into (3) a Malpighian body (p.mg) at the anterior extremity of an isolated coil of glandular tubuli. This coil forms the third section of each segment, and starts from the Malpighian body. It consists of a considerable number of rather definite convolutions, and after uniting with tubuli from one, two, or more (according to the size of the segment) accessory Malpighian bodies (a.mg) smaller than the one into which the segmental tube falls, eventually opens by (4) a narrowish collecting tube into the Wolffian duct at the posterior end of the segment. Each segment is probably completely isolated from the adjoining segments, and never has more than one peritoneal funnel and one communication with the Wolffian duct.

Up to this time there has been no distinction between the anterior and posterior tubuli of the mesonephros, which alike open into the Wolffian duct. The collecting tubes of a considerable number of the hindermost tubuli (ten or eleven in Scyllium canicula), either in some species elongate, overlap, while at the same time their openings travel backward so that they eventually open by apertures (not usually so numerous as the separate tubes), on nearly the same level, into the hindermost section of the Wolffian duct in the female, or into the urinogenital cloaca, formed by the coalesced terminal parts of the Wolffian ducts, in the male; or in other species become modified, by a peculiar process of splitting from the Wolnian duct, so as to pour their secretion into a single duct on each side, which opens in a position corresponding with the numerous ducts of the other species (fig. 392). In both cases the modified posterior kidney-segments are probably equivalent to the per


EXCRETORY ORGANS. 697


manent kidney or metanephros of the amniotic Vertebrates, and for this reason the numerous collecting tubes or single collecting tube, as the case may be, will be spoken of as ureters. The anterior tubuli of the primitive excretory organ retain their early relation to the Wolffian duct, and form the permanent Wolffian body or mesonephros.

The originally separate terminal extremities of the Wolffian ducts always coalesce, and form a urinal cloaca, opening by a single aperture, situated at the extremity of the median papilla behind the anus. Some of the peritoneal openings of the segmental tubes in Scyllium, or in other cases all the openings, become obliterated.

In the male the anterior segmental tubes undergo remarkable modifications, and become connected with the testes. Branches appear to grow from the first three or four or more of them (though probably not from their peritoneal openings), which pass to the base of the testis, and there uniting into a longitudinal canal, form a network, and receive the secretion of the testicular ampullae (fig. 393, nf). These ducts, the vasa efferent ia, carry the semen to the Wolffian body, but before opening into the tubuli of this body they unite into a canal known as the longitudinal canal of the Wolffian body (l.c\ from which pass off ducts equal in number to the vasa efferentia, each of which normally ends in a Malpighian corpuscle. From the Malpighian corpuscles so connected there spring the convoluted tubuli, forming the generative segments of the Wolffian body, along which the semen is conveyed to the Wolffian duct (v.d). The Wolffian duct itself becomes much contorted and acts as vas deferens.

Figs. 392 and 393 are diagrammatic representations of the chief constituents of the adult urinogenital organs in the two sexes. In the adult female (fig. 392), there are present the following parts :

(1) The oviduct or Mullerian duct (m.d) split off from the segmental duct of the kidneys. Each oviduct opens at its anterior extremity into the body cavity, and behind the two oviducts have independent communications with the general cloaca.

(2) The mesonephric ducts (w.d), the other product of the


698


ELASMOBRANCHII.


segmental ducts of the kidneys. They end in front by becoming continuous with the tubulus of the anterior persisting segment of the mesonephros on each side, and unite behind to



FIG. 392. DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS

IN AN ADULT FEMALE ELASMOBRANCH.

m.d. Miillerian duct; w.d. Wolffian duct; s.t. segmental tubes; five of them are represented with openings into the body cavity, the posterior segmental tubes form the mesonephros ; ov. ovary.

open by a common papilla into the cloaca. The mesonephric duct receives the secretion of the anterior tubuli of the primitive mesonephros.

(3) The ureter which carries off the secretion of the kidney proper or metanephros. It is represented in my diagram in its most rare and differentiated condition as a single duct connected with the posterior segmental tubes.

(4) The segmental tubes (.$-./) some of which retain their


-S.t:



FIG. 393. DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS

IN AN ADULT MALE ELASMOBRANCH.

m.d. rudiment of Miillerian duct; w.d. Wolffian duct, marked vd in front and serving as vas deferens; s.t. segmental tubes; two of them are represented with openings into the body cavity; d. ureter; /. testis; nt. canal at the base of the testis; VE, vasa efferentia; Ic. longitudinal canal of the Wolffian body.


EXCRETORY ORGANS. 699


original openings into the body cavity, and others are without them. They are divided into two groups, an anterior forming the mesonephros or Wolffian body, which pours its secretion into the Wolffian duct ; and a posterior group forming a gland which is probably equivalent to the kidney proper of amniotic Craniata, and is connected with the ureter.

In the male the following parts are present (fig. 393):

(1) The Mlillerian duct (m.d], consisting of a small rudiment attached to the liver, representing the foremost end of the oviduct of the female.

(2) The mesonephric duct (w.d] which precisely corresponds to the mesonephric duct of the female, but, in addition to serving as the duct of the Wolffian body, also acts as a vas deferens (vd}. In the adult male its foremost part has a very tortuous course.

(3) The ureter (d\ which has the same fundamental constitution as in the female.

(4) The segmental tubes (s.t). The posterior tubes have the same arrangement in both sexes, but in the male modifications take place in connection with the anterior tubes to fit them to act as transporters of the semen.

Connected with the anterior tubes there are present (i) the vasa efferentia (VE], united on the one hand with (2) the central canal in the base of the testis (/), and on the other with the longitudinal canal of the Wolffian body (/<?). From the latter are seen passing off the successive tubuli of the anterior segments of the Wolffian body, in connection with which Malpighian bodies are typically present, though not represented in my diagram.

Apart from the absence of the pronephros the points which deserve notice in the Elasmobranch excretory system are (i) The splitting of the segmental duct into Wolffian (mesonephric) and Mullerian ducts. (2) The connection of the former with the mesonephros, and of the latter with the abdominal opening of the segmental duct which represents the pronephros of other types. (3) The fact that the Mullerian duct serves as oviduct, and the Wolffian duct as vas deferens. (4) The differentiation of a posterior section of the mesonephros into a special gland foreshadowing the metanephros of the Amniota.


/OO CYCLOSTOMATA.


Cyclostomata. The development of the excretory system amongst the Cyclostomata has only been studied in Petromyzon (Miiller, Furbringer, and Scott).

The first part of the system developed is the segmental duct. It appears in the embryo of about 14 days (Scott) as a solid cord of cells, differentiated from the somatic mesoblast near the dorsal end of the body cavity. This cord is at first placed immediately below the epiblast, and grows backwards by a continuous process of differentiation of fresh mesoblast cells. It soon acquires a lumen, and joins the cloacal section of the alimentary tract before the close of foetal life. Before this communication is established, the front end of the duct sends a process towards the body cavity, the blind end of which acquires a ciliated opening into the latter. A series of about four or five successively formed outgrowths from the duct, one behind the other, give rise to as many ciliated funnels opening into the body cavity, and each communicating by a more or less elongated tube with the segmental duct. These funnels, which have a metameric arrangement, constitute the pronephros, the whole of which is situated in the pericardial region of the body cavity.

On the inner side of the peritoneal openings of each pronephros there is formed a vascular glomerulus, projecting into the body cavity, and covered by peritoneal epithelium. For a considerable period the pronephros constitutes the sole functional part of the excretory system.

A mesonephros is formed (Furbringer) relatively late in larval life, as a segmentally arranged series of solid cords, derived from the peritoneal epithelium. These cords constitute the rudiments of the segmental tubes. They are present for a considerable portion of the body cavity, extending backwards from a point shortly behind the pronephros. They soon separate from the peritoneal epithelium, become hollowed out into canals, and join the segmental duct. At their blind extremity (that originally connected with the peritoneal epithelium) a Malpighian body is formed.

The pronephros is only a provisional excretory organ, the atrophy of which commences during larval life, and is nearly completed when the Ammoccete has reached 180 mm. in length.


EXCRETORY ORGANS. 70 1

Further changes take place in connection with the excretory system on the conversion of the Ammoccete into the adult.

The segmental ducts in the adult fall into a common urinogenital cloaca, which opens on a papilla behind the anus. This cloaca also communicates by two apertures (abdominal pores) with the body cavity. The generative products are carried into the cloaca by these pores ; so that their transportation outwards is not performed by any part of the primitive urinary system. The urinogenital cloaca is formed by the separation of the portion of the primitive cloaca containing the openings of the segmental ducts from that connected with the alimentary tract.

The mesonephros of the Ammoccete undergoes at the metamorphosis complete atrophy, and is physiologically replaced by a posterior series of segmental tubes, opening into the hindermost portion of the segmental duct (Schneider).

In Myxine the excretory system consists (i) of a highly developed pronephros with a bunch of ciliated peritoneal funnels opening into the pericardial section of the body cavity. The coiled and branched tubes of which the pronephros is composed open on the ventral side of the anterior portion of the segmental duct, which in old individuals is cut off from the posterior section of the duct. On the dorsal side of the portion of the segmental duct belonging to the pronephros there are present a small number of diverticula, terminating in glomeruli : they are probably to be regarded as anterior segmental tubes. (2) Of a mesonephros, which commences a considerable distance behind the pronephros, and is formed of straight extremely simple segmental tubes opening into the segmental duct (fig. 385).

The excretory system of Myxine clearly retains the characters of the system as it exists in the larva of Petromyzon.

Teleostei. In most Teleostei the pronephros and mesonephros coexist through life, and their products are carried off by a duct, the nature of which is somewhat doubtful, but which is probably homologous with the mesonephric duct of other types.

The system commences in the embryo (Rosenberg, Oellacher, Gotte, Furbringer) with the formation of a groove-like fold of the somatic layer of peritoneal epithelium, which becomes gradually constricted into a canal; the process of constriction commencing in the middle and extending in both directions. The canal does not however close anteriorly, but remains open to the body cavity, thus giving rise to a funnel equivalent to the pronephric funnels of Petromyzon and Myxine. On the inner side of this


702


TELEOSTEI.


funnel there is formed a glomerulus, projecting into the body

cavity ; and at the same time that

this is being formed the anterior end

of the canal becomes elongated and

convoluted. The above structures

constitute a pronephros, while the

posterior part of the primitive canal

forms the segmental duct.

The portion of the body cavity with the glomerulus and peritoneal funnel of the pronephros (fig. 395, po) soon becomes completely isolated from the remainder, so as to form a closed cavity (gl). The development of the mesonephros does not take place till long after that of the pronephros. The segmental tubes which form it are stated by Fiirbringer to arise from solid ingrowths of peritoneal epithelium, developed successively from before backwards, but Sedgwick informs me that they arise as differentiations of the mesoblastic cells near the peritoneal epithelium. They soon become hollow, and unite with the segmental duct. Malpighian bodies are developed on their median portions. They grow very greatly in length, and become much convoluted, but the details of this process have not been followed out.

The foremost segmental tubes are situated close behind the pronephros, while the hindermost are in many cases developed in the post-anal continuations of the body cavity. The pronephros appears to form the swollen cephalic portion of the kidney of the adult, and the mesonephros the remainder ; the so-called caudal portion, where present, being derived (?) from the postanal segmental tubes.

In some cases the cephalic portion of the kidneys is absent



FIG. 394. PORTIONS OF THE MESONEPHROS OF MYXINE. (From Gegenbaur; after J. Miiller.)

a. segmental duct ; b. segmental tube; c. glomerulus ; d. afferent, e. efferent artery.

B represents a portion of A highly magnified.


EXCRETORY ORGANS. 703


in the adult, which probably implies the atrophy of the pronephros ; in other instances the cephalic portion of the kidneys is the only part developed. Its relation to the embryonic proncphros requires however further elucidation.

In the adult the ducts in the lower part of the kidneys lie as a rule on their outer borders, and almost invariably open into a



pr


FIG. 395. SECTION THROUGH THE PRONEPHROS OF A TROUT AND ADJACENT PARTS TEN DAYS BEFORE HATCHING.

pr.n. pronephros ; po. opening of pronephros into the isolated portion of the body cavity containing the glomerulus ; gl. glomerulus ; ao. aorta ; ch. notochord ; x. subnotochordal rod ; al. alimentary tract.

urinary bladder, which usually opens in its turn on the urinogenital papilla immediately behind the genital pore, but in a few instances there is a common urinogenital pore.

In most Osseous Fish there are true generative ducts continuous with the investment of the generative organs. It appears to me most probable, from the analogy of Lepidostcus, to be described in the next section, that these ducts are split off from the primitive segmental duct, and correspond with the Miillerian ducts of Elasmobranchii, etc. ; though on this point we have at present no positive embryological evidence (vide general considerations at the end of the Chapter). In the female Salmon and the male and female Eel the generative products are carried to the exterior by abdominal pores. It is possible that this may represent a primitive condition, though it


704


GANOIDEI.


is more probably a case of degeneration, as is indicated by the presence of ducts in the male Salmon and in forms nearly allied to the Salmonidae.

The coexistence of abdominal pores and generative ducts in Mormyrus appears to me to demonstrate that the generative ducts in Teleostei cannot be derived from the coalescence of the investment of the generative organs with the abdominal pores.

Ganoidei. The true excretory gland of the adult Ganoidei resembles on the whole that of Teleostei, consisting of an elongated band on each side the mesonephros an anterior dilatation of which probably represents the pronephros.

There is in both sexes a Mullerian duct, provided, except in Lepidosteus, with an abdominal funnel, which is however situated relatively very far back in the abdominal cavity. The Mullerian ducts appear to serve as generative canals in both sexes. In Lepidosteus they are continuous with the investment of the generative glands, and thus a relation between the generative ducts and glands, very similar to that in Teleostei, is brought about.

Posteriorly the Mullerian ducts and the ducts of the mesonephros remain united. The common duct so formed on each side is clearly the primitive segmental duct. It receives the secretion of a certain number of the posterior mesonephric tubules, and usually unites with its fellow to form a kind of bladder, opening by a single pore into the cloaca, behind the anus. The duct which receives the secretion of the anterior mesonephric tubules is the true mesonephric or Wolffian duct.

The development of the excretory system, which has been partially worked out in Acipenscr and Lepidosteus 1 , is on the whole very similar to that in the Teleostei. The first portion of the system to



FIG. 396. SECTION THROUGH THE TRUNK OF A LEPIDOSTEUS EMBRYO ON THE SIXTH DAY AFTER IMPREGNATION.

me. medullary cord ; ms. mesoblast ; sg. segmental duct ; ch. notochord ; .r. subnotochordal rod; hy. hypoblast.


1 Acipenser has been investigated by Fiirbringer, Salensky, Sedgwick, and also by myself, and Lepidosteus by W. N. Parker and myself.


EXCRETORY ORGANS.


705


be formed is the segmental duct. In Lepidosteus this duct is formed as a groove-like invagination of the somatic peritoneal epithelium, precisely as in Teleostei, and shortly afterwards forms a duct lying between the mesoblast and the epiblast (fig. 396, sg}. In Acipenser (Salensky) however it is formed as



FIG. 397. TRANSVERSE SECTION THROUGH THE ANTERIOR PART OF AN ACIPENSER

EMBRYO. (After Salensky.)

Rf. medullary groove ; Alp. medullary plate ; Wg. segmental duct ; Ch. notochord ; En. hypoblast ; Sgp. mesoblastic somite ; Sp. parietal part of mesoblastic plate.

a solid ridge of the somatic mesoblast, as in Petromyzon and Elasmobranchii (fig. 397, Wg).

In both forms the ducts unite behind with the cloaca, and a pronephros of the Teleostean type appears to be developed. This gland is provided with but one 1 peritoneal opening, which together with the glomerulus belonging to it becomes encapsuled in a special section of the body cavity. The opening of the pronephros of Acipenser into this cavity is shewn in fig. ^<^>,pr.n. At this early stage of Acipenser (larva of 5 mm.) I could find no glomerulus.

The mesonephros is formed some distance behind, and some time after the pronephros, both in Acipenser and Lepidosteus, so that in the larvae of both these genera the pronephros is for a considerable period the only excretory organ. In Lepidosteus especially the development of the mesonephros occurs very late.

The development of the mesonephros has not been worked out in Lepidosteus, but in Acipenser the anterior segmental tubes become first established as (I believe) solid cords of cells, attached at one extremity to the peritoneal epithelium on each

1 I have not fully proved this point, but have never found more than one opening.


B. III.


45


GANOIDEI.


side of the insertion of the mesentery, and extending upwards and outwards round the segmental duct 1 . The posterior segmental tubes arise later than the anterior, and (as far as can be determined from the sections in my possession) they are formed independently of the peritoneal epithelium, on the dorsal side of the segmental duct.

In later stages (larvae of 7 10 mm.) the anterior segmental tubes gradually lose their attachment to the peritoneal epithelium. The extremity near the peritoneal epithelium forms a Malpighian body, and the other end unites with the segmental duct. At a still later stage wide peritoneal funnels are es


sjy.c


mjo


pr.n



FIG. 398. TRANSVERSE SECTION THROUGH THE REGION OF THE STOMACH OF A

LARVA OF ACIPENSER 5 MM. IN LENGTH.

st. epithelium of stomach ; yk. yolk ; ch. notochord, below which is a subnotochordal rod; pr.n. pronephros ; ao. aorta; mf. muscle-plate formed of large cells, the outer parts of which are differentiated into contractile fibres ; sp.c. spinal cord ; b.c. body cavity.

tablished, for at any rate a considerable number of the tubes, leading from the body cavity to the Malpighian bodies. These

1 Whether the segmental tubes are formed as ingrowths of the peritoneal epithelium, or in situ, could not be determined.


EXCRETORY ORGANS. 707

funnels have been noticed by Furbringer, Salensky and myself, but their mode of development has not, so far as I know, been made out. The funnels appear to be no longer present in the adult. The development of the Mullerian ducts has not been worked out.

Dipnoi. The excretory system of the Dipnoi is only known in the adult, but though in some respects intermediate in character between that of the Ganoidei and Amphibia, it resembles that of the Ganoidei in the important feature of the Mullerian ducts serving as genital ducts in both sexes.

Amphibia. In Amphibia (Gotte, Furbringer) the development of the excretory system commences, as in Teleostei, by the formation of the segmental duct from a groove formed by a fold of the somatic layer of the peritoneal epithelium, near the dorsal border of the body cavity (fig. 399, u). The anterior end of the groove is placed immediately behind the branchial region. Its posterior part soon becomes converted into a canal by a constriction which commences a short way from the front end of the groove, and thence extends backwards. This canal at first ends blindly close to the cloaca, into which however it soon opens.

The anterior open part of the groove in front of the constriction (fig. 399, n] becomes differentiated into a longitudinal duct, which remains in open communication with the body cavity by two (many Urodela) three (many Anura) or four (Cceciliidae) canals. This constitutes the dorsal part of the pronephros. The ventral part of the gland is formed from the section of the duct immediately behind the longitudinal canal. This part grows in length, and, assuming an S-shaped curvature, becomes placed on the ventral side of the first formed part of the pronephros. By continuous growth in a limited space the convolutions of the canal of the pronephros become more numerous, and the complexity of the gland is further increased by the outgrowth of blindly ending diverticula.

At the root of the mesentery, opposite the peritoneal openings of the pronephros, a longitudinal fold, lined by peritoneal epithelium, and attached by a narrow band of tissue, makes its appearance. It soon becomes highly vascular, and constitutes a glomerulus homologous with that in Petromyzon and Teleostei.

452


AMPHIBIA.


a*'


The section of the body cavity which contains the openings of the pronephros and the glomerulus, becomes dilated, and then temporarily shut off from the remainder. At a later period it forms a special though not completely isolated compartment. For a long time the pronephros and its duct form the only excretory organs of larval Amphibia. Eventually however the formation of the mesonephros commences, and is followed by the atrophy of the pronephros. The mesonephros is composed, as in other types, of a series of segmental tubes, but these, except in Cceciliidae, no longer correspond in number with the myotomes, but are in all instances more numerous. Moreover, in the posterior part of the mesonephros in the Urodeles, and through the whole length of the gland in other types, secondary and tertiary segmental tubes are formed in addition to the primary tubes.



FIG. 399. TRANSVERSE SECTION THROUGH A VERY YOUNG TADPOLE OF BOMBINATOR AT THE LEVEL OF THE ANTERIOR END OF THE YOLK-SACK. (After

Gotte.)

a. fold of epiblast continuous with the dorsal fin; is", neural cord; m. lateral muscle; as 1 . outer layer of muscle-plate; s. lateral plate of mesoblast ; b. mesentery ; u. open end of the segmental duct, which forms the pronephros ; f. alimentary tract ; f. ventral diverticulum which becomes the liver; e. junction of yolk cells and hypoblast cells ; d. yolk cells.


The development of the mesonephros commences in Salamandra (Fiirbringer) with the formation of a series of solid cords, which in the anterior myotomes spring from the peritoneal epithelium on the inner side of the segmental duct, but posteriorly arise independently of this epithelium in the adjoining mesoblast. Sedgwick informs me that in the

Frog the segmental tubes are throughout developed in the mesoblast, independently of the peritoneal epithelium. These cords next become detached from the peritoneal epithelium (in so far as they are primitively united to it), and after first assuming a vesicular form, grow out into coiled tubes, with a median limb the blind end of which assists in forming a Malpighian body, and a lateral limb which comes in contact with and opens into the segmental duct, and an intermediate portion connecting the two. At the junction of the median with the intermediate portion, and therefore at the neck of the Malpighian body, a canal grows out in a ventral direction, which meets the


EXCRETORY ORGANS. 709

peritoneal epithelium, and then develops a funnel-shaped opening into the body cavity, which subsequently becomes ciliated. In this way the peritoneal funnels which are present in the adult are established.

The median and lateral sections of the segmental tubes become highly convoluted, and the separate tubes soon come into such close proximity that their primitive distinctness is lost.

The first fully developed segmental tube is formed in Salamandra maculata in about the sixth myotome behind the pronephros. But in the region between the two structures rudimentary segmental tubes are developed.

The number of primary segmental tubes in the separate myotomes of Salamandra is as follows :

In the 6th myotome (i.e. the first with a true

segmental tube) 12 segmental tubes

yth roth myotome 23

IIth ... 34

I2th 3 4 or 4 5

I3th y> 45

1 3th i6th 56

It thus appears that the segmental tubes are not only more numerous than the myotomes, but that the number in each myotome increases from before backwards. In the case of Salamandra there are formed in the region of the posterior (10 16) myotomes secondary, tertiary, etc. segmental tubes out of independent solid cords, which arise in the mesoblast dorsally to the tubes already established.

The secondary segmental tubes appear to develop out of these cords exactly in the same way as the primary ones, except that they do not join the segmental duct directly, but unite with the primary segmental tubes shortly before the junction of the latter with the segmental duct. In this way compound segmental tubes are established with a common collecting tube, but with numerous Malpighian bodies and ciliated peritoneal openings. The difference in the mode of origin of these compound tubes and of those in Elasmobranchii is very striking.

The later stages in the development of the segmental tubes have not been studied in the other Amphibian types.

In Cceciliidas the earliest stages are not known, but the tubes present in the adult (Spengel) a truly segmental arrangement, and in the young each of them is single, and provided with only a single peritoneal funnel. In the adult however many of the segmental organs become compound, and may have as many as twenty funnels, etc. Both simple and compound segmental tubes occur in all parts of the mesonephros, and are arranged in no definite order.

In the Anura (Spengel) all the segmental tubes are compound, and an enormous number of peritoneal funnels are present on the ventral surface, but it has not yet been definitely determined into what part of the segmental tubes they open.


710 AMPHIBIA.


Before dealing with the further changes of the Wolffian body it is necessary to return to the segmental duct, which, at the time when the pronephros is undergoing atrophy, becomes split into a dorsal Wolffian and ventral Mullerian duct. The process in Salamandra (Fiirbringer) has much the same character as in Elasmobranchii, the Mullerian duct being formed by the gradual separation, from before backwards, of a solid row of cells from the ventral side of the segmental duct, the remainder of the duct constituting the Wolffian duct. During the formation of the Mullerian duct its anterior part becomes hollow, and attaching itself in front to the peritoneal epithelium acquires an opening into the body cavity. The process of hollowing is continued backwards pari passu with the splitting of the segmental duct. In the female the process is continued till the Mullerian duct opens, close to the Wolffian duct, into the cloaca. In the male the duct usually ends blindly. It is important to notice that the abdominal opening of the Mullerian duct in the Amphibia (Salamandra) is a formation independent of the pronephros, and placed slightly behind it ; and that the undivided anterior part of the segmental duct (with the pronephros) is not, as in Elasmobranchii, united with the Mullerian duct, but remains connected with the Wolffian duct.

The development of the Mullerian duct has not been satisfactorily studied in other forms besides Salamandra. In Cceciliidae its abdominal opening is on a level with the anterior end of the Wolffian body. In other forms it is usually placed very far forwards, close to the root of the lungs (except in Proteus and Batrachoseps, where it is placed somewhat further back), and some distance in front of the Wolffian body.

The Mullerian duct is always well developed in the female, and serves as oviduct. In the male it does not (except possibly in Alytes) assist in the transportation of the genital products, and is always more or less rudimentary, and in Anura may be completely absent.

After the formation of the Mullerian duct, the Wolffian duct remains as the excretory channel for the Wolffian body, and, till the atrophy of the pronephros, for this gland also. Its anterior section, in front of the Wolffian body, undergoes a more or less complete atrophy.

The further changes of the excretory system concern (i) the junction in the male of the anterior part of the Wolffian body with the testis ; (2) certain changes in the collecting tubes of the


EXCRETORY ORGANS.


711


posterior part of the mesonephros. The first of these processes results in the division of the Wolffian body into a sexual and a non-sexual part, and in Salamandra and other Urodeles the division corresponds with the distribution of the simple and compound segmental tubes.

Since the development of the canals connecting the testes with the sexual part of the Wolffian body has not been in all points satisfactorily elucidated, it will be convenient to commence with a description of the adult arrangement of the parts (fig. 400 B). In most instances a non-segmental system of canals the vasa effcrentia (ve) coming from the testis, fall into a canal known as the longitudinal canal of the Wolffian body, from which there pass off transverse canals, which fall into, and are equal in number to, the primary Malpighian bodies of the sexual part of the gland. The spermatozoa, brought to the Malpighian bodies, are thence transported along the segmental tubes to the Wolffian duct, and so to the exterior. The system of canals connecting the testis with the Malpighian bodies is known as the testicular network. The number of segmental tubes connected with the testis varies very greatly. In Siredon there are as many as from 30 32 (Spengel).

The longitudinal canal of the Wolffian body is in rare instances (Spelerpes, etc.) absent, where the sexual part of the Wolffian body is slightly developed. In the Urodela the testes are united with the anterior part of the Wolffian body. In the Cceciliidas the junction takes place in an homologous part of the Wolffian body, but, owing to the development of the anterior segmental tubes, which are rudimentary in the Urodela, it is situated some way behind the front end. Amongst the Anura the connection of the testis with the tubules of the Wolffian body is subject to considerable variations. In Bufo cinereus the normal Urodele type is preserved, and in Bombinator the same arrangement is found in a rudimentary condition, in that there are transverse trunks from the longitudinal canal of the Wolffian body, which end blindly, while the semen is carried into the Wolffian duct by canals in front of the Wolffian body. In Alytes and Discoglossus the semen is carried away by a similar direct continuation of the longitudinal canal in front of the Wolffian body, but there are no rudimentary transverse canals passing into the Wolffian body, as in Bombinator. In Rana the transverse ducts which pass off from the longitudinal canal of the Wolffian body, after dilating to form (?) rudimentary Malpighian bodies, enter directly into the collecting tubes near their opening into the Wolffian duct.


712 AMPHIBIA.


In most Urodeles the peritoneal openings connected with the primary generative Malpighian bodies atrophy, but in Spelerpes they persist. In the Cceciliidie they also remain in the adult state.

With reference to the development of these parts little is known except that the testicular network grows out from the primary Malpighian bodies, and becomes united with the testis. Embryological evidence, as well as the fact of the persistence of the peritoneal funnels of the generative region in the adults of some forms, proves that the testicular network is not developed from the peritoneal funnels.

Rudiments of the testicular network are found in the female Cceciliidae and in the females of many Urodela (Salamandra, Triton). These rudiments may in their fullest development consist of a longitudinal canal and of transverse canals passing from this to the Malpighian bodies, together with some branches passing into the mesovarium.

Amongst the Urodela the collecting tubes of the hinder non-sexual part of the Wolffian body, which probably represents a rudimentary metanephros, undergo in the male sex a change similar to that which they usually undergo in Elasmobranchii. Their points of junction with the Wolffian duct are carried back to the hindermost end of the duct (fig. 400 B), and the collecting tubes themselves unite together into one or more short ducts (ureters) before joining the Wolffian duct.

In Batrachoseps only the first collecting tube becomes split off in this way ; and it forms a single elongated ureter which receives all the collecting tubes of the posterior segmental tubes. In the female and in the male of Proteus, Menobranchus, and Siren the collecting tubes retain their primitive transverse course and open laterally into the Wolffian duct. In rare cases (Ellipsoglossus, Spengel} the ureters open directly into the cloaca.

The urinary bladder of the Amphibia is an outgrowth of the ventral wall of the cloacal section of the alimentary tract, and is homologous with the allantois of the amniotic Vertebrata.

The subjoined diagram (fig. 400) of the urogenital system of Triton illustrates the more important points of the preceding description.

In the female (A) the following parts are present :

(1) The Mullerian duct or oviduct (od) derived from the splitting of the segmental duct.

(2) The Wolffian duct (sug) constituting the portion of the segmental duct left after the formation of the Mullerian duct.

(3) The mesonephros (r), divided into an anterior sexual part


EXCRETORY ORGANS.


7'3


connected with a rudimentary testicular network, and a posterior part. The collecting tubes from both parts fall transversely into the Wolffian duct.

(4) The ovary (ov).

(5) The rudimentary testicular network.

In the male (B) the following parts are present :

(1) The functionless though fairly developed Miillerian duct (;).

(2) The Wolffian duct (sug).

(3) The mesonephros (r) divided into a true sexual part, through the segmental tubes of which the semen passes, and a non-sexual part. The collecting tubes of the latter do not enter the Wolffian duct directly, but bend obliquely backwards and only fall into it close to its cloacal aperture, after uniting to form one or two primary tubes (ureters).

(4) The testicular network (ve) consisting of (i) transverse ducts from the testes, falling into (2) the longitudinal canal of the Wolffian body, from which (3) transverse canals are again given off to the Malpighian bodies.

Amniota. The amniotic Vertebrata agree, so far as is known, very closely amongst themselves in the formation of the urinogenital system.

The most characteristic feature of the system is the full development of a metanephros, which constitutes the functional kidney on the atrophy of the mesonephros or Wolffian body, which is a purely embryonic organ. The first part of the system to develop is a duct, which is usually spoken of as the Wolffian duct, but which is really the homologue of the seg


FIG. 400. DIAGRAM OF THE URINOGENITAL SYSTEM OF TRITON. (From Gegenbaur ; after Spengel.)

A. Female. B. Male. r. mesonephros, on the surface of which numerous peritoneal funnels are visible ; sug. mesonephric or Wolffian duct; od. oviduct (Miillerian duct); in. Miillerian duct of male ; ve. vasa efferentia of testis ; t. testis ; ov. ovary ; up. urinogenital pore.


714 AMNIOTA.


mental duct. It apparently develops in all the Amniota nearly on the Elasmobranch type, as a solid rod, primarily derived from the somatic mesoblast of the intermediate cell mass (fig. 401 W.d}\

The first trace of it is visible in an embryo Chick with eight somites, as a ridge projecting from the intermediate cell mass towards the epiblast in the region of the seventh somite. In the course of further development it continues to constitute such a ridge as far as the eleventh somite (Sedgwick), but from this point it grows backwards in the space between the epiblast and mesoblast In an embryo with fourteen somites a small lumen has appeared in its middle part and in front it is connected with rudimentary Wolffian tubules, which develop in continuity with it (Sedgwick). In the succeeding stages the lumen of the duct gradually extends backwards and forwards, and the duct itself also passes inwards relatively to the epiblast (fig. 402). Its hindend elongates till it comes into connection with, and opens into, the cloacal section of the hind-gut' 2 .

It might have been anticipated that, as in the lower types, the anterior end of the segmental duct would either open into the body cavity, or come into connection with a pronephros. Neither of these occurrences takes place, though in some types (the Fowl) a structure, which is probably the rudiment of a pronephros, is developed ; it does not however appear till a later stage, and is then unconnected with the segmental duct. The next part of the system to appear is the mesonephros or Wolffian body.

This is formed in all Amniota as a series of segmental tubes, which in Lacertilia (Braun) correspond with the myotomes, but in Birds and Mammalia are more numerous.

In Reptilia (Braun, No. 542), the mesonephric tubes develop as segmentally-arranged masses on the inner side of the Wolffian duct, and appear to be at first united with the peritoneal epithelium. Each mass soon becomes an oval vesicle, probably opening for a very short period into the

1 Dansky and Kostenitsch (No. 543) describe the Wolffian duct in the Chick as developing from a groove opening to the peritoneal cavity, which subsequently becomes constricted into a duct. I have never met with specimens such as those figured by these authors.

2 The foremost extremity of the segmental duct presents, according to Gasser, curious irregularities and an anterior completely isolated portion is often present.


EXCRETORY ORGANS.


715


peritoneal cavity by a peritoneal funnel. The vesicles become very early detached from the peritoneal epithelium, and lateral outgrowths from them give rise to the main parts of the segmental tubes, which soon unite with the segmental duct.

In Birds the development of the segmental tubes is more complicated 1 .

The tubules of the Wolffian body are derived from the intermediate cell mass, shewn in fig. 401, between the upper end of the body cavity and the


g.o.



FIG. 401. TRANSVERSE SECTION THROUGH THE DORSAL REGION OF AN

EMBRYO CHICK OF 45 HOURS.

M.c. medullary canal ; P.v. mesoblastic somite ; W.d. Wolffian duct which is in contact with the intermediate cell mass ; So. somatopleure ; S.p. splanchnopleure ; p.p. pleuroperitoneal cavity ; ch. notochord ; op. boundary of area opaca; v. bloodvessel.

muscle-plate. In the Chick the mode of development of this mass into the segmental tubules is different in the regions in front of and behind about the sixteenth segment. In front of about the sixteenth segment the intermediate cell mass becomes detached from the peritoneal epithelium at certain points, remaining attached to it at other points, there being several such to each segment. The parts of the intermediate cell mass attached to the peritoneal epithelium become converted into S-shaped cords (fig. 402, st] which soon unite with the segmental duct (wd}. Into the commencement of each of these cords the lumen of the body cavity is for a short distance prolonged, so that this part constitutes a rudimentary peritoneal funnel.

1 Correct figures of the early stages of these structures were first given by Kolliker, but the correct interpretation of them and the first satisfactory account of the development of the excretory organs of Birds was given by Sedgwick (No. 549).


716


AMNIOTA.


In the Duck the attachment of the intermediate cell mass to the peritoneal epithelium is prolonged further back than in the Chick.

In the foremost segmental tubes, which never reach a very complete development, the peritoneal funnels widen considerably, while at the same time they acquire a distinct lumen. The section of the tube adjoining the wide peritoneal funnel becomes partially invaginated by the formation of a glomerulus, and this glomerulus soon grows to such an extent as to project through the peritoneal funnel, the neck of which it completely fills, into the body cavity (fig. 403, gl). There is thus formed a series of free peritoneal glomeruli belonging to the anterior Wolfnan tubuli 1 . These tubuli become however early aborted.

In the case of the remaining tubules developed from the S-shaped cords the attachment to the peritoneal epithelium is very soon lost. The cords acquire a lumen, and open into the segmental duct. Their blind extremities constitute the rudiments of Malpighian bodies.


am



FIG. 402. TRANSVERSE SECTION THROUGH THE TRUNK OF A DUCK EMBRYO WITH

ABOUT TWENTY-FOUR MESOBLASTIC SOMITES.

am. amnion ; so. somatopleure ; sp. splanchnopleure ; ivd. Wolffian duct ; st. segmental tube; ca.v. cardinal vein; m.s. muscle-plate; sp.g. spinal ganglion; sp.c. spinal cord ; ch. notochord ; ao. aorta ; hy. hypoblast.

1 These external glomeruli were originally mistaken by me (No. 539) for the glomeralus of the pronephros, from their resemblance to the glomerulus of the Amphibian pronephros. Their true meaning was made out by Sedgwick (No. 550).


EXCRETORY ORGANS.


717


In the posterior part of the Wolffian body of the Chick the intermediate cell mass becomes very early detached from the peritoneal epithelium, and at a considerably later period breaks up into oval vesicles similar to those of the Reptilia, which form the rudiments of the segmental tubes.

Secondary and tertiary segmental tubules are formed in the Chick, on the dorsal side of the primary tubules, as direct differentiations of the mesoblast. They open independently into the Wolffian duct.

In Mammalia the segmental tubules (Egli) are formed as solid masses in the same situation as in Birds and Reptiles. It is not known whether they are united with the peritoneal epithelium. They soon become oval vesicles, which develop into complete tubules in the manner already indicated.



After the establishment of the Wolffian body there is formed in both sexes in all the Amniota a duct, which in the female becomes the oviduct, but which is functionless and disappears more or less completely in the male. This duct, in spite of certain peculiarities in its development, is without doubt homologous with the Mullerian duct of


FIG. 403. SECTION THROUGH THE EXTERNAL GLOMERULUS OF ONE OF THE ANTERIOR SEGMENTAL TUBES OF AN EMBRYO CHICK OF ABOUT IOO H.

gl. glomerulus ; ge. peritoneal epithelium ; Wd. Wolffian duct ; ao. aorta ; me. mesentery. The segmental tube, and the connection between the external and internal parts of the glomerulus are not shewn in this figure.



FIG. 404. SECTIONS SHEWING TWO OF THE PERITONEAL INVAGINATIONS WHICH GIVE RISE TO THE ANTERIOR PART OF THE MULLERIAN DUCT (PRONEPHROS). (After Balfour and Sedgwick. )

A is the nth section of the series. B i 5th

C i8th ,, ,,

gri. second groove ; gr$. third groove ; ri. second ridge ; wit. Wolffian duct.


7 i8


AMNIOTA.


the Ichthyopsida. In connection with its anterior extremity certain structures have been found in the Fowl, which are probably, on grounds to be hereafter stated, homologous with the pronephros (Balfour and Sedgwick).

The pronephros, as I shall call it, consists of a slightly convoluted longitudinal canal with three or more peritoneal openings. In the earliest condition, 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. It takes its origin from the layer of thickened peritoneal epithelium situated near the dorsal angle of the body cavity, and is situated some considerable distance behind the front end of the Wolfifian duct.

In a slightly later stage the ridges connecting the grooves become partially constricted off from the peritoneal epithelium,



FIG. 405. SECTION OF THE WOLFFIAN BODY DEVELOPING PRONEPHROS AND GENITAL GLAND OF THE FOURTH DAY. (After Waldeyer.) Magnified 160 times. m. mesentery; Z. somatopleure ; a', portion of the germinal epithelium from which the involution (2) to form the pronephros (anterior part of Miillerian duct) takes place; a. thickened portion of the germinal epithelium in which the primitive germinal cells C and o are lying ; E. modified mesoblast which will form the stroma of the ovary ; WK. Wolffian body ; y. Wolffian duct.


EXCRETORY ORGANS. 719

and develop a lumen. The condition of the structure at this stage is illustrated by fig. 404, representing three transverse sections through two grooves, and through the ridge connecting them.

The pronephros may in fact now be described as a slightly convoluted duct, opening into the body cavity by three groovelike apertures, and continuous behind with the rudiment of the true Miillerian duct.

The stage just described is that of the fullest development of the pronephros. In it, as in all the previous stages, there appear to be only three main openings into the body cavity ; but in some sections there are indications of the possible presence of one or two additional rudimentary grooves.

In an embryo not very much older than the one last described the pronephros atrophies as such, its two posterior openings vanishing, and its anterior opening remaining as the permanent opening of the Miillerian duct.

The pronephros is an extremely transitory structure, and its development and atrophy are completed between the QOth and i2Oth hours of incubation.

The position of the pronephros in relation to the Wolffian body is shewn in fig. 405, which probably passes through a region between two of the peritoneal openings. As long as the pronephros persists, the Mullerian duct consists merely of a very



FlG. 406. TWO SECTIONS SHEWING THE JUNCTION OF THE TERMINAL SOLID PORTION OF THE MtJLLERIAN DUCT WITH THE WOLFFIAN DUCT. (After Balfour

and Sedgwick.)

In A the terminal portion of the duct is quite distinct ; in B it has united with the walls of the Wolffian duct.

md. Mullerian duct ; Wd. Wolffian duct.


72O AMNIOTA.


small rudiment, continuous with the hindermost of the three peritoneal openings, and its solid extremity appears to unite with the walls of the Wolffian duct.

After the atrophy of the pronephros, the Miillerian duct commences to grow rapidly, and for the first part of its course it appears to be split off as a solid rod from the outer or ventral wall of the Wolffian duct (fig. 406). Into this rod the lumen, present in its front part, subsequently extends. Its mode of development in front is thus precisely similar to that of the Miillerian duct in Elasmobranchii and Amphibia.

This mode of development only occurs however in the anterior part of the duct. In the posterior part of its course its growing point lies in a bay formed by the outer walls of the Wolffian duct, but does not become definitely attached to that duct. It seems however possible that, although not actually split off from the walls of the Wolrfian duct, it may grow backwards from cells derived from that duct.

The Miillerian duct finally reaches the cloaca though it does not in the female for a long time open into it, and in the male never does so.

The mode of growth of the Miillerian duct in the posterior part of its course will best be understood from the following description quoted from the paper by Sedgwick and myself.

"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. 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. 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 Miillerian


EXCRETORY ORGANS. 721

duct finally terminates quite suddenly, and in the section immediately behind its termination the Wolffian duct assumes its normal appearance, and the part of its outer wall on the level of the Miillerian duct conies into contact with the germinal epithelium."

Before describing the development of the Mullerian duct in other Amniotic types it will be well to say a few words as to the identifications above adopted. The identification of the duct, usually called the Wolffian duct, with the segmental duct (exclusive of the pronephros) appears to be morphologically justified for the following reasons : (i) that it gives rise to part of the Mullerian duct as well as to the duct of the Wolffian body ; behaving in this respect precisely as does the segmental duct of Elasmobranchii and Amphibia. (2) That it serves as the duct for the Wolffian body, before the Mullerian duct originates from it. (3) That it develops in a manner strikingly similar to that of the segmental duct of various lower forms.

With reference to the pronephros it is obvious that the organ identified as such is in many respects similar to the pronephros of the Amphibia. Both consist of a somewhat convoluted longitudinal canal, with a certain number of peritoneal openings ;

The main difficulties in the homology are :

(1) the fact that the pronephros in the Bird is not united with the segmental duct ;

(2) the fact that it is situated behind the front end of the Wolffian body. It is to be remembered in connection with the first of these difficulties

that in the formation of the Mullerian duct in Elasmobranchii the anterior undivided extremity of the primitive segmental duct, with the peritoneal opening, which probably represents the pronephros, is attached to the Mullerian duct, and not to the Wolffian duct ; though in Amphibia the reverse is the case. To explain the discontinuity of the pronephros with the segmental duct it is only necessary to suppose that the segmental duct and pronephros, which in the Ichthyopsida develop as a single formation, develop in the Bird as two independent structures a far from extravagant supposition, considering that the pronephros in the Bird is undoubtedly quite functionless.

With reference to the posterior position of the pronephros it is only necessary to remark that a change in position might easily take place after the acquirement of an independent development, and that the shifting is probably correlated with a shifting of the abdominal opening of the Mullerian duct.

The pronephros has only been observed in Birds, and is very possibly not developed in other Amniota. The Mullerian duct is also usually stated to develop as a groove of the peritoneal epithelium, shewn in the Lizard in fig. 354, md., which is continued backward as a primitively solid rod in the space between B. ill. 46


722


AM N IOTA.


the Wolffian duct and peritoneal epithelium, without becoming attached to the Wolffian duct.

On the formation of the Miillerian duct, the duct of the mesonephros becomes the true mesonephric or Wolffian duct.

After these changes have taken place a new organ of great importance makes its appearance. This organ is the permanent kidney, or metanephros.

Metanephros. The mode of development of the metanephros has as yet only been satisfactorily elucidated in the Chick (Sedgwick, No. 549). The ureter and the collecting tubes of the kidney are developed from a dorsal outgrowth of the hinder part of the Wolffian duct. The outgrowth from the Wolffian duct grows forwards, and extends along the outer side of a mass of mesoblastic tissue which lies mainly behind, but somewhat overlaps the dorsal aspect of the Wolffian body.

This mass of mesoblastic cells may be called the metanephric blastema. Sedgwick, of the accuracy of whose account I have satisfied myself, has shewn that in the Chick it is derived from the intermediate cell mass of the region of about the thirty-first to the thirty-fourth somite. It is at first continuous with, and indistinguishable in structure from, the portion of the intermediate cell mass of the region immediately in front of it, which breaks up into Wolffian tubules. The metanephric blastema remains however quite passive during the formation of the Wolffian tubules in the adjoining blastema ; and on the formation of the ureter breaks off from the Wolffian body in front, and, growing forwards and dorsalwards, places itself on the inner side of the ureter in the position just described.

In the subsequent development of the kidney collecting tubes grow out from the ureter, and become continuous with masses of cells of the metanephric blastema, which then differentiate themselves into the kidney tubules.

The process just described appears to me to prove that the kidney of the A mniota is a specially differentiated posterior section of the primitive mesonephros.

According to the view of Remak and Kolliker the outgrowths from the ureter give rise to the whole of the tubuli uriniferi and the capsules of the Malpighian bodies, the mesoblast around them forming blood-vessels, etc. On the other hand some observers (Kupffer, Bornhaupt, Braun) maintain, in


EXCRETORY ORGANS. 723


accordance with the account given above, that the outgrowths of the ureter form only the collecting tubes, and that the secreting tubuli, etc. are formed in situ in the adjacent mesoblast.

Braun (No. 542) has arrived at the conclusion that in the Lacertilia the tissue, out of which the tubuli of the metanephros are formed, is derived from irregular solid ingrowths of the peritoneal epithelium, in a region behind the Wolffian body, but in a position corresponding to that in which the segmental tubes take their origin. These ingrowths, after separating from the peritoneal epithelium, unite together to form a cord into which the ureter sends the lateral outgrowths already described. These outgrowths unite with secreting tubuli and Malpighian bodies, formed in situ. In Lacertilia the blastema of the kidney extends into a postanal region. Braun's account of the origin of the metanephric blastema does not appear to me to be satisfactorily demonstrated.

The ureter does not long remain attached to the Wolffian duct, but its opening is gradually carried back, till (in the Chick between the 6th and 8th day) it opens independently into the cloaca.

Of the further changes in the excretory system the most important is the atrophy of the greater part of the Wolffian body, and the conversion of the Wolffian duct in the male sex into the vas deferens, as in Amphibia and the Elasmobranchii.

The mode of connection of the testis with the Wolffian duct is very remarkable, but may be derived from the primitive arrangement characteristic of Elasmobranchii and Amphibia.

In the structures connecting the testis with the Wolffian body two parts have to be distinguished, (i) that equivalent to the testicular network of the lower types, (2) that derived from the segmental tubes. The former is probably to be found in peculiar outgrowths from the Malpighian bodies at the base of the testes.

These were first discovered by Braun in Reptilia, and consist in this group of a series of outgrowths from the primary (?) Malpighian bodies along the base of the testis : they unite to form an interrupted cord in the substance of the testis, from which the testicular tubuli (with the exception of the seminiferous cells) are subsequently differentiated. These outgrowths, with the exception of the first two or three, become detached from the Malpighian bodies. Outgrowths similar to those in the male are found in the female, but subsequently atrophy.

Outgrowths homologous with those found by Braun have

46 2


724 AMNIOTA.


been detected by myself (No. 555) in Mammals. It is not certain to what parts of the testicular tubuli they give rise, but they probably form at any rate the vasa recta and rete vasculosum.

In Mammals they also occur in the female, and give rise to cords of tissue in the ovary, which may persist through life.

The comparison of the tubuli, formed out of these structures, with the Elasmobranch and Amphibian testicular network is justified in that both originate as outgrowths from the primary Malpighian bodies, and thence extend into the testis, and come into connection with the true seminiferous stroma.

As in the lower types the semen is transported from the testicular network to the Wolffian duct by parts of the glandular tubes of the Wolffian body. In the case of Reptilia the anterior two or three segmental tubes in the region of the testis probably have this function. In the case of Mammalia the vasa efferentia, i.e. the coni vasculosi, appear, according to the usually accepted view, to be of this nature, though Banks and other investigators believe that they are independently developed structures. Further investigations on this point are required. In Birds a connection between the Wolffian body and the testis appears to be established as in the other types. The Wolffian duct itself becomes, in the males of all Amniota, the vas deferens and the convoluted canal of the epididymis the latter structure (except the head) being entirely derived from the Wolffian duct.

In the female the Wolffian duct atrophies more or less completely.

In Snakes (Braun) the posterior part remains as a functionless canal, commencing at the ovary, and opening into the cloaca. In the Gecko (Braun) it remains as a small canal joining the ureter ; in Blindworms a considerable part of the canal is left, and in Lacerta (Braun) only interrupted portions.

In Mammalia the middle part of the duct, known as Gaertner's canal, persists in the females of some monkeys, of the pig and of many ruminants.

The Wolffian body atrophies nearly completely in both sexes ; though, as described above, part of it opposite the testis persists as the head of the epididymis. The posterior part of the gland from the level of the testis may be called the sexual part of the gland, the anterior part forming the non-sexual part.


EXCRETORY ORGANS. 725

The latter, i.e. the anterior part, is first absorbed ; and in some Reptilia the posterior part, extending from the region of the genital glands to the permanent kidney, persists till into the second year.

Various remnants of the Wolffian body are found in the adults of both sexes in different types. The most constant of them is perhaps the part in the female equivalent to the head of the epididymis and to parts also of the coiled tube of the epididymis, which may be called, with Waldeyer, the epoophoron 1 . This is found in Reptiles, Birds and Mammals ; though in a very rudimentary form in the first-named group. Remnants of the anterior non-sexual part of the Wolffian bodies have been called by Waldeyer parepididymis in the male, and paroophoron in the female. Such remnants are not (Braun) found in Reptilia, but are stated to be found in both male and female Birds, as a small organ consisting of blindly ending tubes with yellow pigment. In some male Mammals (including Man) a parepididymis is found on the upper side of the testis. It is usually known as the organ of Giraldes.

The Mlillerian duct forms, as has been stated, the oviduct in the female. The two ducts originally open independently into the cloaca, but in the Mammalia a subsequent modification of this arrangement occurs, which is dealt with in a separate section. In Birds the right oviduct atrophies, a vestige being sometimes left. In the male the Miillerian ducts atrophy more or less completely.

In most Reptiles and in Birds the atrophy of the Miillerian ducts is complete in the male, but in Lacerta and Anguis a rudiment of the anterior part has been detected by Leydig as a convoluted canal. In the Rabbit (Kolliker) 2 and probably other Mammals the whole of the ducts probably disappears, but in some Mammals, e.g. Man, the lower fused ends of the Miillerian ducts give rise to a pocket opening into the urethra, known as the uterus masculinus ; and in other cases, e.g. the Beaver and the Ass, the rudiments are more considerable, and may be continued into horns homologous with the horns of the uterus (Weber).

The hydatid of Morgani in the male is supposed (Waldeyer) to represent the abdominal opening of the Fallopian tube in the female, and therefore to be a remnant of the Miillerian duct.

Changes in the lower parts of the urinogenital ducts in the Amniota.

The genital cord. In the Monodelphia the lower part of the Wolffian ducts becomes enveloped in both sexes in a special

1 This is also called parovarium (His), and Rosenmiiller's organ.

2 Weber (No. 553) states that a uterus masculinus is present in the Rabbit, but his account is by no means satisfactory, and its presence is distinctly denied by Kolliker.


726


AMNIOTA.


cord of tissue, known as -the genital cord (fig. 407, gc), within the lower part of which the MUllerian ducts are also enclosed. In the male the MUllerian ducts in this cord atrophy, except at their distal end where they unite to form the uterus masculinus. The Wolffian ducts, after becoming the vasa deferentia, remain for some time enclosed in the common cord, but afterwards separate from each other. The seminal vesicles are outgrowths of the vasa deferentia.

In the female the Wolffian ducts within the genital cord atrophy, though rudiments of them are for a long time visible or even permanently persistent. The lower parts of the MUllerian ducts unite to form the vagina and body of the uterus. The junction commences in the middle and extends forwards and backwards ; the stage with a median junction being retained permanently in Marsupials.

The urinogenital sinus and external generative organs. In all the Amniota, there open at first into the common cloaca the alimentary canal dorsally, the allantois ventrally, and the Wolffian and MUllerian ducts and ureters laterally. In Reptilia and Aves the embryonic condition is retained. In both groups the allantois serves as an embryonic urinary bladder, but while it atrophies in Aves, its stalk dilates to form a permanent urinary bladder in Reptilia. In Mammalia the dorsal part of the cloaca with the alimentary tract becomes first of all partially constricted off from the ventral, which then forms a urinogenital sinus (fig. 407, ug). In the course of development the urinogenital sinus becomes, in all Mammalia but the Ornithodelphia, completely separated from the intestinal cloaca, and the two parts obtain separate external openings. The ureters (fig. 407, 3) open higher up than the other ducts into the stalk of the allantois which dilates to form the bladder (4). The stalk connecting the bladder with the ventral wall of the body constitutes the urachus, and loses its lumen before the close of embryonic life. The part of the stalk of the allantois below the openings of the ureters narrows to form the urethra, which opens together with the Wolffian and MUllerian ducts into the urinogenital cloaca.

In front of the urinogenital cloaca there is formed a genital prominence (fig. 407, cp), with a groove continued from the


EXCRETORY ORGANS. 727

urinogenital opening ; and on each side a genital fold (&). In the male the sides of the groove on the prominence coalesce together, embracing between them the opening of the urinogenital cloaca ; and the prominence itself gives rise to the penis,



FIG. 407. DIAGRAM OF THE URINOGENITAL ORGANS OF A MAMMAL AT AN EARLY STAGE. (After Allen Thomson ; from Quain's Anatomy.)

The parts are seen chiefly in profile, but the Miillerian and Wolffian ducts are seen from the front.

3. ureter; 4. urinary bladder ; 5. urachus; of. genital ridge (ovary or testis) ; W. left Wolffian body ; x. part at apex from which coni vasculosi are afterwards developed ; w. Wolffian duct ; m. Miillerian duct ; gc. genital cord consisting of Wolffian and Mullerian ducts bound up in a common sheath ; i. rectum ; ug. urinogenital sinus ; cp. elevation which becomes the clitoris or penis ; Is. ridge from which the labia majora or scrotum are developed.

along which the common urinogenital passage is continued. The two genital folds unite from behind forwards to form the scrotum.

In the female the groove on the genital prominence gradually disappears, and the prominence remains as the clitoris, which is therefore the homologue of the penis : the two genital folds form the labia majora. The urethra and vagina open independently into the common urinogenital sinus.


728 GENERAL CONCLUSIONS.

General conclusions and Summary.

Pronephros. Sedgwick has pointed out that the pronephros is always present in types with a larval development, and either absent or imperfectly developed in those types which undergo the greater part of their development within the egg. Thus it is practically absent in the embryos of Elasmobranchii and the Amniota, but present in the larvae of all other forms.

This coincidence, on the principles already laid down in a previous chapter on larval forms, affords a strong presumption that the pronephros is an ancestral organ ; and, coupled with the fact that it is the first part of the excretory system to be developed, and often the sole excretory organ for a considerable period, points to the conclusion that the pronephros and its duct the segmental duct are the most primitive parts of the Vertebrate excretory system. This conclusion coincides with that arrived at by Gegenbaur and Fiirbringer.

The duct of the pronephros is always developed prior to the gland, and there are two types according to which its development may take place. It may either be formed by the closing in of a continuous groove of the somatic peritoneal epithelium (Amphibia, Teleostei, Lepidosteus), or as a solid knob or rod of cells derived from the somatic mesoblast, which grows backwards between the epiblast and the mesoblast (Petromyzon, Elasmobranchii, and the Amniota).

It is quite certain that the second of these processes is not a true record of the evolution of 'the duct, and though it is more possible that the process observable in Amphibia and the Teleostei may afford some indications of the manner in which the duct was established, this cannot be regarded as by any means certain.

The mode of development of the pronephros itself is apparently partly dependent on that of its duct. In Petromyzon, where the duct does not at first communicate with the body cavity, the pronephros is formed as a series of outgrowths from the duct, which meet the peritoneal epithelium and open into the body cavity ; but in other instances it is derived from the anterior open end of the groove which gives rise to the segmental duct. The open end of this groove may either remain single


EXCRETORY ORGANS. 729

(Teleostci, Ganoidei) or be divided into two, three or more apertures (Amphibia). The main part of the gland in either case is formed by convolutions of the tube connected with the peritoneal funnel or funnels. The peritoneal funnels of the pronephros appear to be segmentally arranged.

The pronephros is distinguished from the mesonephros by developmental as well as structural features. The most important of the former is the fact that the glandular tubules of which it is formed are always outgrowths of the segmental duct ; while in the mesonephros they are always or almost always 1 formed independently of the duct.

The chief structural peculiarity of the pronephros is the absence from it of Malpighian bodies with the same relations as those in the meso- and metanephros; unless the structures found in Myxine are to be regarded as such. Functionally the place of such Malpighian bodies is taken by the vascular peritoneal ridge spoken of in the previous pages as the glomerulus.

That this body is really related functionally to the pronephros appears to be indicated (i) by its constant occurrence with the pronephros and its position opposite the peritoneal openings of this body ; (2) by its atrophy at the same time as the pronephros ; (3) by its enclosure together with the pronephridian stoma in a special compartment of the body-cavity in Teleostei and Ganoids, and its partial enclosure in such a compartment in Amphibia.

The pronephros atrophies more or less completely in most types, though it probably persists for life in the Teleostei and Ganoids, and in some members of the former group it perhaps forms the sole adult organ of excretion.

The cause of its atrophy may perhaps be related to the fact that it is situated in the pericardial region of the body-cavity, the dorsal part of which is aborted on the formation of a closed pericardium ; and its preservation in Teleostei and Ganoids may on this view be due to the fact that in these types its peritoneal funnel and its glomerulus are early isolated in a special cavity.

Mesonephros. The mesonephros is in all instances composed of a series of tubules (segmental tubes) which are developed independently of the segmental duct. Each tubule is

1 According t.o Sedgwick some of the anterior segmental tubes of Aves form an exception to the general rule that there is no outgrowth from the segmental or metanephric duct to meet the segmental tubes.


730 GENERAL CONCLUSIONS.

typically formed of (i) a peritoneal funnel opening into (2) a Malpighian body, from which there proceeds (3) a coiled glandular tube, finally opening by (4) a collecting tube into the segmental duct, which constitutes the primitive duct for the mesonephros as well as for the pronephros.

The development of the mesonephridian tubules is subject to considerable variations.

(1) They may be formed as differentiations of the intermediate cell mass, and be from the first provided with a lumen, opening into the body-cavity, and directly derived from the section of the body-cavity present in the intermediate cell mass; the peritoneal funnels often persisting for life (Elasmobranchii).

(2) They may be formed as solid cords either attached to or independent of the peritoneal epithelium, which after first becoming independent of the peritoneal epithelium subsequently send downwards a process, which unites with it and forms a peritoneal funnel, which may or may not persist (Acipenser, Amphibia).

(3) They may be formed as in the last case, but acquire no secondary connection with the peritoneal epithelium (Teleostei, Amniota). In connection with the original attachment to the peritoneal epithelium, a true peritoneal funnel may however be developed (Aves, Lacertilia).

Physiological considerations appear to shew that of these three methods of development the first is the most primitive. The development of the tubes as solid cords can hardly be primary.

A question which has to be answered in reference to the segmental tubes is that of the homology of the secondarily developed peritoneal openings of Amphibia, with the primary openings of the Elasmobranchii. It is on the one hand difficult to understand why, if the openings are homologous in the two types, the original peritoneal attachment should be obliterated in Amphibia, only to be shortly afterwards reacquired. On the other hand it is still more difficult to understand what physiological gain there could be, on the assumption of the non-homology of the openings, in the replacement of the primary opening by a secondary opening exactly similar to it. Considering the great variations in development which occur in undoubtedly homologous parts I incline to the view that the openings in the two types are homologous.


EXCRETORY ORGANS.


731


In the majority of the lower Vertebrata the mesonephric tubes have at first a segmental arrangement, and this is no doubt the primitive condition. The coexistence of two, three, or more of them in a single segment in Amphibia, Aves and Mammalia has recently been shewn, by an interesting discovery of Eisig, to have a parallel amongst Chaetopods, in the coexistence of several segmental organs in a single segment in some of the Capitellidae.

In connection with the segmental features of the mesonephros it is perhaps worth recalling the fact that in Elasmobranchii as well as other types there are traces of segmental tubes in some of the postanal segments. In the case of all the segmental tubes a Malpighian body becomes established close to the extremity of the tube adjoining the peritoneal opening, or in an homologous position in tubes without such an opening. The opposite extremity of the tube always becomes attached to the segmental duct.

In many of the segments of the mesonephros, especially in the hinder ones, secondary and tertiary tubes become developed in certain types, which join the collecting canals of the primary tubes, and are provided, like the primary tubes, with Malpighian bodies at their blind extremities.

There can it appears to me be little or no doubt that the secondary tubes in the different types are homodynamous if not homologous. Under these circumstances it is surprising to find in what different ways they take their origin. In Elasmobranchii a bud sprouts out from the Malpighian body of one segment, and joins the collecting tube of the preceding segment, and subsequently, becoming detached from the Malpighian body from which it sprouted, forms a fresh secondary Malpighian body at its blind extremity. Thus the secondary tubes of one segment are formed as buds from the segment behind. In Amphibia (Salamandra) and Aves the secondary tubes develop independently in the mesoblast. These great differences in development are important in reference to the homology of the metanephros or permanent kidney, which is discussed below.

Before leaving the mesonephros it may be worth while putting forward some hypothetical suggestions as to its origin and relation to the pro


732 GENERAL CONCLUSIONS.

nephros, leaving however the difficult questions as to the homology of the segmental tubes with the segmental organs of Chastopods for subsequent discussion.

It is a peculiarity in the development of the segmental tubes that they at first end blindly, though they subsequently grow till they meet the segmental duct with which they unite directly, without the latter sending out any offshoot to meet them 1 . It is difficult to believe that peritoneal infundibula ending blindly and unprovided with some external orifice can have had an excretory function, and we are therefore rather driven to suppose that the peritoneal infundibula which become the segmental tubes were either from the first provided each with an orifice opening to the exterior, or were united with the segmental duct. If they were from the first provided with external openings we may suppose that they became secondarily attached to the duct of the pronephros (segmental duct), and then lost their external openings, no trace of these structures being left, even in the ontogeny of the system. It would appear to me more probable that the pronephros, with its duct opening into the cloaca, was the only excretory organ of the unsegmented ancestors of the Chordata, and that, on the elongation of the trunk and its subsequent segmentation, a series of metameric segmental tubes became evolved opening into the segmental duct, each tube being in a sort of way serially homologous with the primitive pronephros. With the segmentation of the trunk the latter structure itself may have acquired the more or less definite metameric arrangement of its parts.

Another possible view is that the segmental tubes may be modified derivatives of posterior lateral branches of the pronephros, which may at first have extended for the whole length of the body-cavity. If there is any truth in this hypothesis it is necessary to suppose that, when the unsegmented ancestor of the Chordata became segmented, the posterior branches of the primitive excretory organ became segmentally arranged, and that, in accordance with the change thus gradually introduced in them, the time of their development became deferred, so as to accord to a certain extent with the time of formation of the segments to which they belonged. The change in their mode of development which would be thereby introduced is certainly not greater than that which has taken place in the case of segmental tubes, which, having originally developed on the Elasmobranch type, have come to develop as they do in the posterior part of the mesonephros of Salamandra, Birds, etc.

Genital ducts. So far the origin and development of the excretory organs have been considered without reference to the modifications introduced by the excretory passages coming to serve as generative ducts. Such an unmodified state of the

1 As mentioned in the note on p. 729 Sedgwick maintains that the anterior segmental tubes of the Chick form an exception to this general statement.


EXCRETORY ORGANS. 733


excretory organs is perhaps found permanently in Cyclostomata 1 and transitorily in the embryos of most forms.

At first the generative products seem to have been discharged freely into the body-cavity, and transported to the exterior by the abdominal pores (vide p. 626).

The secondary relations of the excretory ducts to the generative organs seem to have been introduced by an opening connected with the pronephridian extremity of the segmental duct having acquired the function of admitting the generative products into it, and of carrying them outwards ; so that primitively the segmental duct must have served as efferent duct both for the generative products and the pronepJiric secretion (just as the Wolffian duct still does for the testicular products and secretion of the Wolffian body in Elasmobranchii and Amphibia).

The opening by which the generative products entered the segmental duct can hardly have been specially developed for this purpose, but must almost certainly have been one of the peritoneal openings of the pronephros. 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 Mullerian duct and a dorsal Wolffian duct.

The Mullerian duct was probably continuous with one or more of the abdominal openings of the pronephros which served as generative pores. At first the segmental duct was probably split longitudinally into two equal portions, and this mode of splitting is exceptionally retained in some Elasmobranchii ; but the generative function of the Mullerian duct gradually impressed itself more and more upon the embryonic development, so that, in the course of time, the Mullerian 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 the Elasmobranchii ; while in Aves it has been carried even further, and it seems possible that in some Amniota the Mullerian and segmental

1 It is by no means certain that the transportation outwards of the genital products by the abdominal pores in the Cyclostomata may not be the result of degeneration.


734 GENERAL CONCLUSIONS.

ducts may actually develop independently, as they do exceptionally in individual specimens of Salamandra (Fiirbringer). The abdominal opening no doubt also became specialised. At first it is quite possible that more than one pronephric abdominal funnel may have served for the entrance of the generative products ; this function being, no doubt, eventually restricted to one of them.

Three different types of development of the abdominal opening of the Mullerian duct have been observed.

In Amphibia (Salamandra) the permanent opening of the Mullerian duct is formed independently, some way behind the pronephros.

In Elasmobranchii the original opening of the segmental duct forms the permanent opening of the Mullerian duct, and no true pronephros appears to be formed.

In Birds the anterior of the three openings of the rudimentary pronephros remains as the permanent opening of the Mullerian duct.

These three modes of development very probably represent specialisations of the primitive state along three different lines. In Amphibia the specialisation of the opening appears to have gone so far that it no longer has any relation to the pronephros. It was probably originally one of the posterior openings of this gland.

In Elasmobranchii, on the other hand, the functional opening is formed at a period when we should expect the pronephros to develop. This state is very possibly the result of a differentiation by which the pronephros gradually ceased to become developed, but one of its peritoneal openings remained as the abdominal aperture of the Mullerian 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 Mullerian duct.

The Mullerian duct is usually formed in a more or less complete manner in both sexes. In Ganoids, where the separation between it and the Wolffian duct is not completed to the cloaca, and in the Dipnoi, it probably serves to carry off the generative products of both sexes. In other cases however only the female


EXCRETORY ORGANS.


735


products pass out by it, and the partial or complete formation of the Mullerian duct in the male in these cases needs to be explained. This may be done either by supposing the Ganoid arrangement to have been the primitive one in the ancestors of the other forms, or, by supposing characters acquired primitively by the female to have become inherited by both sexes.

It is a question whether the nature of the generative ducts of Teleostei can be explained by comparison with those of Ganoids. The fact that the Mullerian ducts of the Teleostean Ganoid Lepidosteus attach themselves to the generative organs, and thus acquire a resemblance to the generative ducts of Teleostei, affords a powerful argument in favour of the view that the generative ducts of both sexes in the Teleostei are modified Mullerian ducts. Embryology can however alone definitely settle this question.

In the Elasmobranchii, Amphibia, and Amniota the male products are carried off by the Wolffian duct, and they are transported to this duct, not by open peritoneal funnels of the mesonephros, but by a network of ducts which sprout either from a certain number of the Malpighian bodies opposite the testis (Amphibia, Amniota), or from the stalks connecting the Malpighian bodies with the open funnels (Elasmobranchii). After traversing this network the semen passes (except in certain Anura) through a variable number of the segmental tubes directly to the Wolffian duct. The extent of the connection of the testis with the Wolffian body is subject to great variations, but it is usually more or less in the anterior region. Rudiments of the testicular network have in many cases become inherited by the female.

The origin of the connection between the testis and Wolffian body is still very obscure. It would be easy to understand how the testicular products, after falling into the body-cavity, might be taken up by the open extremities of some of the peritoneal funnels, and how such open funnels might have groove-like prolongations along the mesorchium, which might eventually be converted into ducts. Ontogeny does not however altogether favour this view of the origin of the testicular network. It seems to me nevertheless the most probable view which has yet been put forward.

The mode of transportation of the semen by means of the mesonephric tubules is so peculiar as to render it highly improbable that it was twice acquired, it becomes therefore necessary to suppose that the Amphibia and


736 GENERAL CONCLUSIONS.

Amniota inherited this mode of transportation of the semen from the same ancestors as the Elasmobranchii. It is remarkable therefore that in the Ganoidei and Dipnoi this arrangement is not found.

Either (i) the arrangement (found in the Ganoidei and Dipnoi) of the Miillerian duct serving for both sexes is the primitive arrangement, and the Elasmobranch is secondary, or (2) the Ganoid arrangement is a secondary condition, which has originated at a stage in the evolution of the Vertebrata when some of the segmental tubes had begun to serve as the efferent ducts of the testis, and has resulted in consequence of a degeneration of the latter structures. Although the second alternative is the more easy to reconcile with the affinities of the Ganoid and Elasmobranch types, as indicated by the other features of their organization, I am still inclined to accept the former ; and consider that the incomplete splitting of the segmental duct in Ganoidei is a strong argument in favour of this view.

Metanephros. With the employment of the Wolffian duct to transport the semen there seems to be correlated (i) a tendency of the posterior segmental tubes to have a duct of their own, in which the seminal and urinary fluids cannot become mixed, and (2) a tendency on the part of the anterior segmental tubes to lose their excretory function. The posterior segmental tubes, when connected in this way with a more or less specialised duct, have been regarded in the preceding pages as constituting a metanephros.

This differentiation is hardly marked in the Anura, but is well developed in the Urodela and in the Elasmobranchii ; and in the latter group has become inherited by both sexes. In the Amniota it culminates, according to the view independently arrived at by Semper and myself, (i) in the formation of a completely distinct metanephros in both sexes, formed however, as shewn by Sedgwick, from the same blastema as the Wolffian body, and (2) in the atrophy in the adult of the whole Wolffian body, except the part uniting the testis and the Wolffian duct.

The homology between the posterior metanephridian section of the Wolffian body, in Elasmobranchii and Urodela, and the kidney of the Amniota, is only in my opinion a general one, i.e. in both cases a common cause, viz. the Wolffian duct acting as vas deferens, has resulted in a more or less similar differentiation of parts.

Fiirbringer has urged against Semper's and my view that no satisfactory proof of it has yet been offered. This proof has however, since Fiirbringer wrote his paper, been supplied by Sedgwick's observations. The development of the kidney in the Amniota is no doubt a direct as opposed to a phylogenetic development ; and the substitution of a direct for


EXCRETORY ORGANS. 737


a phylogenetic development has most probably been rendered possible by the fact that the anterior part of the mesonephros continued all the while to be unaffected and to remain as the main excretory organ during foetal life.

The most serious difficulty urged by Fiirbringer against the homology is the fact that the ureter of the metanephros develops on a type of its own, which is quite distinct from the mode of development of the ureters of the metanephros of the Ichthyopsidan forms. It is however quite possible, though far from certain, that the ureter of Amniota may be a special formation confined to that group, and this fact would in no wise militate against the homology I have been attempting to establish.

Comparison of the Excretory organs of the Chordata and Invertebrata.

The structural characters and development of the various forms of excretory organs described in the preceding pages do not appear to me to be sufficiently distinctive to render it possible to establish homologies between these organs on a satisfactory basis, except in closely related groups.

The excretory organs of the Platyelminthes are in many respects similar to the provisional excretory organ of the trochosphere of Polygordius and the Gephyrea on the one hand, and to the Vertebrate pronephros on the other ; and the Platyelminth excretory organ with an anterior opening might be regarded as having given origin to the trochosphere organ, while that with a posterior opening may have done so for the Vertebrate pronephros 1 .

Hatschek has compared the provisional trochosphere excretory organ of Polygordius to the Vertebrate pronephros, and the posterior Chastopod segmental tubes to the mesonephric tubes ; the latter homology having been already suggested independently by both Semper and myself. With reference to the comparison of the pronephros with the provisional excretory organ of Polygordius there are two serious difficulties :

(1) The pronephric (segmental) duct opens directly into the cloaca, while the duct of the provisional trochosphere excretory organ opens anteriorly, and directly to the exterior.

(2) The pronephros is situated within the segmented region of the trunk, and has a more or less distinct metameric arrangement of its parts ; while the provisional trochosphere organ is placed in front of the segmented region of the trunk, and is in no way segmented.

The comparison of the mesonephric tubules with the segmental excretory organs of the Chaetopoda, though not impossible, cannot be satisfactorily admitted till some light has been thrown upon the loss of the supposed external openings of the tubes, and the origin of their secondary connection with the segmental duct.

1 This suggestion has I believe been made by Fiirbringer. B. III. 47


738 BIBLIOGRAPHY.


Confining our attention to the Invertebrata it appears to me fairly clear that Hatschek is justified in holding the provisional trochosphere excretory organs of Polygordius, Echiurus and the Mollusca to be homologous. The atrophy of all these larval organs may perhaps be due to the presence of a well-developed trunk region in the adult (absent in the larva), in which excretory organs, probably serially homologous with those present in the anterior part of the larva, became developed. The excretory organs in the trunk were probably more conveniently situated than those in the head, and the atrophy of the latter in the adult state was therefore brought about, while the trunk organs became sufficiently enlarged to serve as the sole excretory organs.

BIBLIOGRAPHY OF THE EXCRETORY ORGANS. Invertebrata.

(512) H. Eisig. " Die Segmentalorgane d. Capitelliden." Mitth. a. d. zool. Stat. z. Neapel, Vol. I. 1879.

(513) J. Fraipont. " Recherches s. 1'appareil excreteur des Trematodes et d. Cesto'ides." Archives de Biologic, Vol. I. 1880.

(514) B. Hatschek. "Studien lib. Entwick. d. Anneliden." Arbeit, a. d. zool. Instit. Wien, Vol. I. 1878.

(515) B. Hatschek. "Ueber Entwick. von Echiurus," etc. Arbeit, a. d. zool. Instit. Wien, Vol. in. 1880.

EXCRETORY ORGANS OF VERTEBRATA. General.

(516) F. M. Balfour. "On the origin and history of the urinogenital organs of Vertebrates." yournal of Anat. and Phys., Vol. X. 1876.

(517) Max. Furbringer 1 . "Zur vergleichenden Anat. u. Entwick. d. Excretionsorgane d. Vertebraten." Morphol. Jahrbuch, Vol. IV. 1878.

(518) H. Meek el. Zur Morphol. d. Hani- u. Geschlechtnverkz.d. Wirbelthiere, etc. Halle, 1848.

(519) Joh. Miiller. Bildungsgeschichte d. Genitalien, etc. Diisseldorf, 1830.

(520) H. Rathke. " Beobachtungen u. Betrachtungen u. d. Entwicklung d. Geschlechtswerkzeuge bei den Wirbelthieren." N. Schriften d. naturf. Gesell. in Dantzig, Bd. I. 1825.

(521) C. Semper 1 . "Das Urogenitalsystem d. Plagiostomen u. seine Bedeutung f. d. iibrigen Wirbelthiere." Arb. a. d. zool.-zoot. Instit. Wurzburg, Vol. II. 1875 (522) W. Waldeyer 1 . Eierstock u. Ei. Leipzig, 1870.


1 The papers of Furbringer, Semper and Waldeyer contain full references to the literature of the Vertebrate excretory organs.


BIBLIOGRAPHY. 739


ElasmobrancJdi.

(523) A. Schultz. "Zur Entwick. d. Selachiereies." Archiv f. mikr. Anat., Vol. XI. 1875.

Vide also Semper (No. 521) and Balfour (No. 292).

Cyclostomata.

(524) J. Miiller. " Untersuchungen ii. d. Eingeweide d. Fische." Abh. d. k. Ak. Wiss. Berlin, 1845.

(525) W. Miiller. "Ueber d. Persistenz d. Urniere b. Myxine glutinosa." Jenaische Zeitschrift, Vol. VII. 1873.

(526) W. Miiller. "Ueber d. Urogenitalsystem d. Amphioxus u. d. Cyclostomen." Jenaische Zeitschri/t, Vol. IX. 1875.

(527) A. Schneider. Beitrdge z. vergleich. Anat. u. Entwick. d. Wirbelthiere. Berlin, 1879.

(528) W. B. Scott. "Beitrage z. Entwick. d. Petromyzonten." Morphol. Jahrbuch, Vol. vn. 1881.

Teleostei.

(529) J. Hyrtl. "Das uropoetische System d. Knochenfische." Denkschr. d. k. k. Akad. Wiss. Wien, Vol. n. 1850.

(530) A. Rosenberg. Untersuchungen iib. die Entivicklung d. Teleostierniere. Dorpat, 1867.

Vide also Oellacher (No. 72).

Amphibia.

(531) F. H. Bidder. Vergleichend-anatomische u. histologische Untersitchungen ii. die mdnnlichen Geschleehts- und Harnwerkzeuge d. nackten Amphibien. Dorpat, 1846.

(532) C. L. Duvernoy. "Fragments s. les Organes genito-urinaires des Reptiles," etc. Mem. Acad. Sciences. Paris. Vol. xi. 1851, pp. 17 95.

(533) M. Fiirbringer. Zur Entwicklung d. Amphibienniere. Heidelberg, 1877.

(534) F. Leydig. Anatomie d. Amphibien u. Reptilien. Berlin, 1853.

(535) F. Leydig. Lehrbuch d. Hisiologie. Hamm, 1857.

(536) F. Meyer. "Anat. d. Urogenitalsystems d. Selachier u. Amphibien." Sitz. d. naturfor. Gesellsch. Leipzig, 1875.

(537) J. W. Spengel. "Das Urogenitalsystem d. Amphibien." Arb. a. d. zool.- zoot. Instil. Wiirzburg. Vol. III. 1876.

(538) VonWittich. "Harn- u. Geschlechtswerkzeuge d. Amphibien." Zeit. f. wiss. Zool., Vol. IV.

Vide also Gotte (No. 296).

Amniota.

(539) F. M. Balfour and A. Sedgwick. "On the existence of a head -kidney in the embryo Chick," etc. Quart. J. of Micr. Science, Vol. xix. 1878.

(540 ) Banks. On the Wolffian bodies of the fatus and their remains in the adult. Edinburgh, 1864.

472


74O BIBLIOGRAPHY.


(541) Th. Bornhaupt. Untersuchungen iib. die Entwicklung d. Urogenitalsystems beim Hiihnchen. Inaug. Diss. Riga, 1867.

(542) Max Braun. "Das Urogenitalsystem d. einheimischen Reptilien." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg. Vol. iv. 1877.

(543) J. Dansky u. J. Kostenitsch. "Ueb. d. Entwick. d. Keimblatter u. d. WolfFschen Ganges im Hiihnerei." Mini. Acad. Imp. Petersbourg, vn. Series, Vol. xxvil. 1880.

(544) Th. Egli. Beitrage zur Anat. und Entwick. d. Geschlechtsorgane. Inaug. Diss. Zurich, 1876.

(545) E. Gasser. Beitrage zur Entwicklungsgeschichte d. Allantois, der Milllcr'schen Gange u. des Afters. Frankfurt, 1874.

(546) E. Gasser. "Beob. iib. d. Entstehung d. Wolff schen Ganges bei Embryonen von Hiihnern u. Gansen." Arch, fiir mikr. Anat., Vol. xiv. 1877.

(547) E. Gasser. "Beitrage z. Entwicklung d. Urogenitalsystems d. Hiihnerembryonen." Sitz. d. GeseU. zur Befdrderung d. gesam. Naturwiss. Marburg, 1879.

(548) C. Kupffer. " Untersuchting iiber die Entwicklung des Harn- und Geschlechtssystems." Archiv fiir mikr. Anat., Vol. II. 1866.

(549) A. Sedgwick. "Development of the kidney in its relation to the Wolffian body in the Chick." Quart. J. of Micros. Science, Vol. xx. 1880.

(550) A. Sedgwick. "On the development of the structure known as the glomerulus of the head-kidney in the Chick." Quart. J. of Micros. Science, Vol. xx. 1880.

(551) A. Sedgwick. "Early development of the Wolffian duct and anterior Wolffian tubules in the Chick ; with some remarks on the vertebrate excretory system." Quart. J. of Micros. Science, Vol. xxi. 1881.

(552) M. Watson. "The homology of the sexual organs, illustrated by comparative anatomy and pathology." Journal of Anat. and Phys., Vol. xiv. 1879.

(553) E. H. Weber. Zusdtze z. Lehre von Baue u. d. Verrichtungen d. Geschlechtsorgane. Leipzig, 1846.

Vide also Remak (No. 302), Foster and Balfour (No. 295), His (No. 297), Kolliker (No. 298).


CHAPTER XXIV. GENERATIVE ORGANS AND GENITAL DUCTS.

GENERATIVE ORGANS.

THE structure and growth of the ovum and spermatozoon were given in the first chapter of this work, but their derivation from the germinal layers was not touched on, and it is this subject with which we are here concerned. If there are any structures whose identity throughout the Metazoa is not open to doubt these structures are the ovum and spermatozoon ; and the constancy of their relations to the germinal layers would seem to be a crucial test as to whether the latter have the morphological importance usually attributed to them.

The very fragmentary state of our knowledge of the origin of the generative cells has however prevented this test being so far very generally applied.

Porifera. In the Porifera the researches of Schulze have clearly demonstrated that both the ova and the spermatozoa take their origin from indifferent cells of the general parenchyma, which may be called mesoblastic. The primitive germinal cells of the two sexes are not distinguishable ; but a germinal cell by enlarging and becoming spherical gives rise to an ovum ; and by subdivision forms a sperm-morula, from the constituent cells of which the spermatozoa are directly developed.

Ccelenterata. The greatest confusion prevails as to the germinal layer from which the male and female products are derived in the Ccelenterata 1 .

1 E. van Beneden (No. 556) was the first to discover a different origin for the generative products of the two sexes in Hydractinia, and his observations have led to numerous subsequent researches on the subject. For a summary of the observations on the Hydroids vide Weismann (No. 560).


742 CCELENTERATA.


The following apparent modes of origin of these products have been observed.

(1) The generative products of both sexes originate in the ectoderm (epiblast) : Hydra, Cordylophora, Tubularia, all (?) free Gonophores of Hydromedusae, the Siphonophora, and probably the Ctenophora.

(2) The generative products of both sexes originate in the entoderm (hypoblast) : Plumularia and Sertularella, amongst the Hydroids, and the. whole of the Acraspeda and Actinozoa.

(3) The male cells are formed in the ectoderm, and the female in the entoderm : Gonothyraea, Campanularia, Hydractinia, Clava.

In view of the somewhat surprising results to which the researches on the origin of the genital products amongst the Ccelenterata have led, it would seem to be necessary either to hold that there is no definite homology between the germinal layers in the different forms of Ccelenterata, or to offer some satisfactory explanation of the behaviour of the genital products, which would not involve the acceptance of the first alternative.

Though it can hardly be said that such an explanation has yet been offered, some observations of Kleinenberg (No. 557) undoubtedly point to such an explanation being possible.

Kleinenberg has shewn that in Eudendrium the ova migrate freely from the ectoderm into the endoderm, and vice versa ; but he has given strong grounds for thinking that they originate in the ectoderm. He has further shewn that the migration in this type is by no means an isolated phenomenon.

Since it is usually only possible to recognise generative elements after they have advanced considerably in development, the mere position of a generative cell, when first observed, can afford, after what Kleinenberg has shewn, no absolute proof of its origin. Thus it is quite possible that there is really only one type of origin for the generative cells in the Ccelenterata.

Kleinenberg has given reasons for thinking that the migration of the ova into the entoderm may have a nutritive object. If this be so, and there are numerous facts which shew that the position of generative cells is often largely influenced by their nutritive requirements, it seems not impossible


GENERATIVE ORGANS. 743

that the endodermal position of the generative organs in the Actinozoa and acraspedote Medusre may have arisen by a continuously earlier migration of the generative cells from the ectoderm into the endoderm ; and that the migration may now take place at so early a period of the development, that we should be justified in formally holding the generative products to be endodermal in origin.

\Ve might perhaps, on this view, formulate the origin of the generative products in the Ccelenterata in the following way :

Both ova and spermatozoa primitively originated in the ectoderm, but in order to secure a more complete nutrition the cells which give rise to them exhibit in certain groups a tendency to migrate into the endoderm. This migration, which may concern the generative cells of one or of both the sexes, takes place in some cases after the generative cells have become recognisable as such, and very probably in other cases at so early a period that it is impossible to distinguish the generative cells from indifferent embryonic cells.

Very little is known with reference to the origin of the generative cells in the triploblastic Invertebrata.

Chaetopoda and Gephyrea. In the Chaetopoda and Gephyrea, the germinal cells are always developed in the adult from the epithelial lining of the body cavity ; so that their origin from the mesoblast seems fairly established.

If we are justified in holding the body cavity of these forms to be a derivative of the primitive archenteron (vide pp. 356 and 357) the generative cells may fairly be held to originate from a layer which corresponds to the endoderm of the Ccelenterata 1 .

Chaetognatha. In Sagitta the history of the generative cells, which was first worked out by Kowalevsky and Biitschli, has been recently treated with great detail by O. Hertwig 2 .

The generative cells appear during the gastrula stage, as two large cells with conspicuous nuclei, which are placed in the hypoblast lining the archenteron, at the pole opposite the blastopore. These cells soon divide, and at the same time pass out of the hypoblast, and enter the archenteric cavity (fig. 408 - A, ge). The division into four cells, which is not satisfactorily represented ifl my diagram, takes place in such a way that two

1 The Hertwigs (No. 271) state that in their opinion the generative cells arise from the lining of the body cavity in all the forms whose body cavity is a product of the archenteron. We do not know anything of the embryonic development of the generative organs in the Echinodermata, but the adult position of the generative organs in this group is very unfavourable to the Hertwigs' view.

2 O. Hertwig, Die Chcetognathen. Jena, 1880


744


CH^ETOGNATHA.


cells are placed nearer the median line, and two externally. The two inner cells form the eventual testes, and the outer the



FIG. 408. THREK STAGES IN THE DEVELOPMENT OF SAGITTA. (A and C after

Biitschli, and B after Kowalevsky.) The three embryos are represented in the same positions.

A. Represents the gastrula stage.

B. Represents a succeeding stage, in which the primitive archenteron is commencing to be divided into three.

C. Represents a later stage, in which the mouth involution (in) has become continuous with the alimentary tract, and the blastopore is closed.

///. mouth ; al. alimentary canal ; ac. archenteron ; bl.p. blastopore ; pv. perivisceral cavity ; sp, splanchnic mesoblast ; so. somatic mesoblast ; ge. generative organs.

ovaries, one half of each primitive cell thus forming an ovary, and the other a testis.



FIG. 409. Two VIEWS OF A LATE EMBRYO OF SAGITTA. A, from the dorsal

surface. B, from the side. (After Biitschli.)

m. mouth ; al. alimentary canal ; v.g. ventral ganglion (thickening of epiblast) ; <.'/. epiblast ; c.pv. cephalic section of body cavity ; so. somatopleure ; sp. splanchnopleure ; ge. generative organs.


GENERATIVE ORGANS.


745


When the archenteric cavity is divided into a median alimentary tract, and two lateral sections forming the body cavity, the generative organs are placed in the common vestibule into which both the body cavity and alimentary cavity at first open (fig. 408).

The generative organs long retain their character as simple cells. Eventually (fig. 409) the two ovaries travel forwards, and apply themselves to the body walls, while the two testes also become separated by a backward prolongation of the median alimentary tract.

On the formation of the transverse septum dividing the tail from the body, the ovarian cells lie immediately in front of this septum, and the testicular cells in the region behind it.

Polyzoa. In Pedicellina amongst the entoproctous Polyzoa Hatschek finds that the generative organs originate from a pair of specially large mesoblast cells, situated in the space between the stomach and the floor of the vestibule. The two cells undergo changes, which have an obvious resemblance to those of the generative cells of the Chsetognatha. They become surrounded by an investment of mesoblast cells, and divide so as to form two masses. Each of these masses at a later period separates into an anterior and a posterior part. The former becomes the ovary, the latter the testis.

Nematoda. In the Nematoda the generative organs are derived from the division of a single cell which would appear to be mesoblastic 1 .

Insecta. The generative cells have been observed at a very early embryonic stage in several insect forms (Vol. II. p. 404), but the observations so far recorded with reference to them do not enable us to determine with certainty from which of the germinal layers they are derived.

Crustacea. In Moina, one of the Cladocera, Grobben 2 has shewn that the generative organs are derived from a single cell, which becomes differentiated during the segmentation. This cell, which is in close contiguity with the cells from which both the mesoblast and hypoblast originate, subsequently divides ;

1 Fide Vol. n. p. 374; also Gotte, Zool. Anzeiger, No. 80, p. 189.

2 C. Grobben. "Die Entwick. d. Moina rectirostris." Arbeit, a. d. zool. Instil. Wien. Vol. II. 1879.


746


CHORDATA.


sp.c


but at the gastrula stage, and after the mesoblast has become formed, the cells it gives rise to are enclosed in the epiblast, and do not migrate inwards till a later stage. The products of the division of the generative cell subsequently divide into two masses. It is not possible to assign the generative cell of Moina to a definite germinal layer. Grobben, however, thinks that it originates from the division of a cell, the remainder of which gives rise to the hypoblast.

Chordata. In the Vertebrata, the primitive generative cells (often known as primitive ova) are early distinguishable, being imbedded amongst the cells of two linear streaks of peritoneal epithelium, placed on the dorsal side of the body cavity, one on each side of the mesentery (figs. 405 C and 4io,/0). They appear to be derived from the epithelial cells amongst which they lie ; and are characterized by containing a large granular nucleus, surrounded by a considerable body of protoplasm. The peritoneal epithelium in which they are placed is known as the germinal epithelium.

It is at first impossible to distinguish the germinal cells which will become ova from those which will become spermatozoa.

The former however remain within the peritoneal epithelium (fig. 41 1), and become converted into ova in a manner more particularly described in Vol. II. pp. 54 59.

The history of the primitive germinal cells in the male has not been so adequately worked out as in the female.

The fullest history of them is that given by Semper (No. 559) for the Elasmobranchii, the general accuracy of which I can fully support ;



FIG. 410. SECTION THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNGER

THAN 28 F.

sp.c. spinal cord ; W. white matter of spinal cord ; pr. posterior nerve-roots ; ch. notochord ; x. sub-notochordal rod ; ao. aorta ; mp. muscle-plate ; mp'. inner layer of- muscle-plate already converted into muscles ; Vr. rudiment of vertebral body ; st. segmental tube; sd. segmental duct; sp.v. spiral valve ; v. subintestinal vein ; i>.o. primitive generative cells.


GENERATIVE ORGANS.


747


though with reference to certain stages in the history further researches are still required 1 .

In Elasmobranchii the male germinal cells, instead of remaining in the germinal epithelium, migrate into the adjacent stroma, accompanied I believe by some of the indifferent epithelial cells. Here they increase in number, and give rise to masses of variable form, composed partly of true germinal cells, and partly of smaller cells with deeply staining nuclei, which are, I believe, derived from the germinal epithelium.



FIG. 411. TRANSVERSE SECTION THROUGH THE OVARY OF A YOUNG EMBRYO OK SCYLLIUM CANICULA, TO SHEW THE PRIMITIVE GERMINAL CELLS (po) LYING IN THE GERMINAL EPITHELIUM ON THE OUTER SIDE OF THE OVARIAN RIDGE.

These masses next break up into ampullae, mainly formed of germinal cells, and each provided with a central lumen ; and these ampullae attach themselves to tubes derived from the smaller cells, which are in their turn continuous with the testicular network. The spermatozoa are developed from the cells forming the walls of the primitive ampulla;; but the process of their formation does not concern us in this chapter.

In the Reptilia Braun has traced the passage of the primitive germinal cells into the testicular tubes, and I am able to confirm his observations on this point : he has not however traced their further history.

1 Balbiani (No. 554) has also recently dealt with this subject, but I cannot bring my own observations into accord with his as to the structure of the Elasmobranch testis.


MODE OF EXIT OF GENITAL PRODUCTS.


In Mammalia the evidence of the origin of the spermatospores from the germinal epithelium is not quite complete, but there can be but little doubt of its occurrence 1 .

In Amphioxus Langerhans has shewn that the ova and spermatozoa are derived from similar germinal cells, which may be compared to the germinal epithelium of the Vertebrata. These cells are however segmentally arranged as separate masses (vide Vol. II. p. 54).

BIBLIOGRAPHY.

(554) G. Balbiani. Lemons s. la generation des Vcrlebrcs. Paris, 1879.

(555) F. M. Balfour. "On the structure and development of the Vertebrate ovary." Quart, J. of Micr. Science, Vol. xvm.

(556) E. van Beneden. "De la distinction originelle dutecticule et clel'ovaire, etc." Bull. Ac. roy. belgique, Vol. xxxvil. 1874.

(557) N. Kleinenberg. "Ueb. d. Entstehung d. Eier b. Eudendrium." Zcit. f. -wiss. Zool., Vol. xxxv. 1881.

(558) H. Ludwig. "Ueb. d. Eibildung im Theirreiche." Arbeit, a. d. zool.zoot. Inslit. Wilrzburg, Vol. I. 1874.

(559) C. Semper. "Das Urogenilalsystem d. Plagiostomen, etc." Arbeit, a. d. zooL-zoot. Ins tit. Witrzbiirg, Vol. II. 1875.

(560) A. Weismann. "Zur Frage nach dem Ursprung d. Geschlechtszellen bei den Hydroiden." Zool. Anzeiger, No. 55, 1880.

Fitffcalso O. and R. Hertwig (No. 271), Kolliker (No. 298), etc.

GENITAL DUCTS.

The development and evolution of the generative ducts is as yet very incompletely worked out, but even in the light of our present knowledge a comparative review of this subject brings to light features of considerable interest, and displays a fruitful field for future research.

In the Ccelenterata there are no generative ducts.

In the Hydromedusae and Siphonophora the generative products are liberated by being dehisced directly into the surrounding medium ; while in the Acraspeda, the Actinozoa and the Ctenophora, they are dehisced into parts of the gastrovascular system, and carried to the exterior through the mouth.

The arrangement in the latter forms indicates the origin of

1 An entirely different view of the origin of the sperm cells has been adopted by Balbiani, for which the reader is referred to his Memoir (No. 554).


GENITAL DUCTS.


749


the methods of transportation of the genital products to the exterior in many of the higher types.

It has been already pointed out that the body cavity in a very large number of forms is probably derived from parts of a gastrovascular system like that of the Actinozoa.

When the part of the gastrovascular system into which the generative products were dehisced became, on giving rise to the body cavity, shut off from the exterior, it would be essential that some mode of transportation outwards of the generative products should be constituted.

In some instances simple pores (probably already existing at the time of the establishment of a closed body cavity) become the generative ducts. Such seems probably to have been the case in the Chaetognatha (Sagitta) and in the primitive Chordata.

In the latter forms the generative products are sometimes dehisced into the peritoneal cavity, and thence transported by the abdominal pores to the exterior (Cyclostomata and some Teleostei, vide p. 626). In Amphioxus they pass by dehiscence into the atrial cavity, and thence through the gill slits and by the mouth, or by the abdominal pore (?) to the exterior. The arrangement in Amphioxus and the Teleostei is probably secondary, as possibly also is that in the Cyclostomata ; so that the primitive mode of exit of the generative products in the Chordata is still uncertain. It is highly improbable that the generative ducts of the Tunicata are primitive structures.

A better established and more frequent mode of exit of the generative products when dehisced into the body cavity is by means of the excretory organs. The generative products pass from the body cavity into the open peritoneal funnels of such organs, and thence through their ducts to the exterior. This mode of exit of the generative products is characteristic of the Chaetopoda, the Gephyrea, the Brachiopoda and the Vertebrata, and probably also of the Mollusca. It is moreover quite possible that it occurs in the Polyzoa, some of the Arthropoda, the Platyelminthes and some other types.

The simple segmental excretory organs of the Polychaeta, the Gephyrea and the Brachiopoda serve as generative canals, and in many instances they exhibit no modification, or but a very slight one, in connection with their secondary generative


750 DERIVATION FROM EXCRETORY ORGANS.

function ; while in other instances, e.g. Bonellia, such modification is very considerable.

The generative ducts of the Oligochaeta are probably derived from excretory organs. In the Terricola ordinary excretory organs are present in the generative segments in addition to the generative ducts, while in the Limicola generative ducts alone are present in the adult, but before their development excretory organs of the usual type are found, which undergo atrophy on the appearance of the generative ducts (Vedjovsky).

From the analogy of the splitting of the segmental duct of the Vertebrata into the Miillerian and Wolffian ducts, as a result of a combined generative and excretory function (vide p. 728), it seems probable that in the generative segments of the Oligochasta the excretory organs had at first both an excretory and a generative function, and that, as a secondary result of this double function, each of them has become split into two parts, a generative and an excretory. The generative part has undergone in all forms great modifications. The excretory parts remain unmodified in the Earthworms (Terricola), but completely abort on the development of the generative ducts in the Limicola. An explanation may probably be given of the peculiar arrangements of the generative ducts in Saccocirrus amongst the Polychaeta (vide Marion and Bobretzky), analogous to that just offered for the Oligochaeta.

The very interesting modifications produced in the excretory organs of the Vertebrata by their serving as generative ducts were fully described in the last chapter ; and with reference to this part of our subject it is only necessary to call attention to the case of Lepidosteus and the Teleostei.

In Lepidosteus the Mullerian duct appears to have become attached to the generative organs, so that the generative products, instead of falling directly into the body cavity and thence entering the open end of a peritoneal funnel of the excretory organs, pass directly into the Mullerian duct without entering the body cavity. In most Teleostei the modification is more complete, in that the generative ducts in the adult have no obvious connection with the excretory organs.

The transportation of the male products to the exterior in all the higher Vertebrata, without passing into the body cavity, is in principle similar to the arrangement in Lepidosteus.

The above instances of the peritoneal funnels of an excretory organ becoming continuous with the generative glands, render it highly probable that there may be similar instances amongst the In vertebrata.


GENITAL DUCTS.


751


As has been already pointed out by Gegenbaur there are many features in the structure of the genital ducts in the more primitive Mollusca, which point to their having been derived from the excretory organs. In several Lamellibranchiata 1 (Spondylus, Lima, Pecten) the generative ducts open into the excretory organs (organ of Bojanus), so that the generative products have to pass through the excretory organ on their way to the exterior. In other Lamellibranchiata the genital and excretory organs open on a common papilla, and in the remaining types they are placed close together.

In the Cephalopoda again the peculiar relations of the generative organs to their ducts point to the latter having primitively had a different, probably an excretory, function. The glands are not continuous with the ducts, but are placed in special capsules from which the ducts proceed. The genital products are dehisced into these capsules and thence pass into the ducts.

In the Gasteropoda the genital gland is directly continuous with its duct, and the latter, especially in the Pulmonata and Opisthobranchiata, assumes such a complicated form that its origin from the excretory organ would hardly have been suspected. The fact however that its opening is placed near that of the excretory organ points to its being homologous with the generative ducts of the more primitive types.

In the Discophora, where the generative ducts are continuous with the glands, the structure both of the generative glands and ducts points to the latter having originated from excretory organs.

It seems, as already mentioned, very possible that there are other types in which the generative ducts are derived from the excretory organs. In the Arthropoda for instance the generative ducts, where provided with anteriorly placed openings, as in the Crustacea, Arachnida and the Chilognathous Myriapoda, the Pcecilopoda, etc., may possibly be of this nature, but the data for deciding this point are so scanty that it is not at present possible to do more than frame conjectures.

The ontogeny of the generative ducts of the Nematoda and

1 For a summary of the facts on this subject vide Bronn, Klassen u. Ordnungen d. Thierreichs, Vol. in. p. 404.


752 DERIVATION FROM EXCRETORY ORGANS.

the Insecta appears to point to their having originated independently of the excretory organs.

In the Nematoda the generative organs of both sexes originate from a single cell (Schneider, Vol. I. No. 390).

This cell elongates and its nuclei multiply. After assuming a somewhat columnar form, it divides into (i) a superficial investing layer, and (2) an axial portion.

In the female the superficial layer is only developed distinctly in the median part of the column. In the course of the further development the two ends of the column become the blind ends of the ovary, and the axial tissue they contain forms the germinal tissue of nucleated protoplasm. The superficial layer gives rise to the epithelium of the uterus and oviduct. The germinal tissue, which is originally continuous, is interrupted in the middle part (where the superficial layer gives rise to the uterus and oviduct), and is confined to the two blind extremities of the tube.

In the male the superficial layer, which gives rise tc the epithelium of the vas deferens, is only formed at the hinder ond of the original column. In other respects the development takes place as in the female.

In the Insecta again the evidence, though somewhat conflicting, indicates that the generative ducts arise very much as in Nematodes, from the same primitive mass as the generative organs. In both of these types it would seem probable that the generative organs were primitively placed in the body cavity, and attached to the epidermis, through a pore in which their products passed out ; and that, acquiring a tubular form, the peripheral part of the gland gave rise to a duct, the remainder constituting the true generative gland. It is quite possible that the generative ducts of such forms as the Platyelminthes may have had a similar origin to those in Insecta and Nematoda, but from the analogy of the Mollusca there is nearly as much to be said for regarding them as modified excretory organs.

In the Echinodermata nothing is unfortunately known as to the ontogeny of the generative organs and ducts. The structure of these organs in the adult would however seem to indicate that the most primitive type of echinoderm generative organ consists of a blind sack, projecting into the body cavity, and opening by


GENITAL DUCTS. 753


a pore to the exterior. The sack is lined by an epithelium, continuous with the epidermis, the cells of which give rise to the ova or spermatozoa. The duct of these organs is obviously hardly differentiated from the gland ; and the whole structure might easily be derived from the type of generative organ characteristic of the Hydromedusae, where the generative cells are developed from special areas of the ectoderm, and, when ripe, pass directly into the surrounding medium.

If this suggestion is correct we may suppose that the generative ducts of the Echinodermata have a different origin to those of the majority of 1 the remaining triploblastica.

Their ducts have been evolved in forms in which the generative products continued to be liberated directly to the exterior, as in the Hydromedusae ; while those of other types have been evolved in forms in which the generative products were first transported, as in the Actinozoa, into the gastrovascular canals 2 .

1 It would be interesting to have further information about Balanoglossus.

2 These views fit in very well with those already put forward in Chapter xm. on the affinities of the Echinodermata.


B. III.


48


CHAPTER XXV.

THE ALIMENTARY CANAL AND ITS APPENDAGES, IN THE CHORDATA.

THE alimentary canal in the Chordata is always formed of three sections, analogous to those so universally present in the Invertebrata. These sections are (i) the mesenteron lined by hypoblast ; (2) the stomodaeum or mouth lined by epiblast, and (3) the proctodaeum or anal section lined like the stomodaeum by epiblast.

Mesenteron.

The early development of the epithelial wall of the mesenteron has already been described (Chapter XI.). It forms at first a simple hypoblastic tube extending from near the front end of the body, where it terminates blindly, to the hinder extremity where it is united with the neural tube by the neurenteric canal (fig. 420, ne). It often remains for a long time widely open in the middle towards the yolk-sack.

It has already been shewn that from the dorsal wall of the mesenteron the notochord is separated off nearly at the same time as the lateral plates of mesoblast (pp. 292 300).

The subnotochordal rod. At a period slightly subsequent to the formation of the notochord, and before any important differentiations in the mesenteron have become apparent, a remarkable rod-like body, which was first discovered by Gotte, becomes split off from the dorsal wall of the alimentary tract in all the Ichthyopsida. This body, which has a purely provisional existence, is known as the subnotochordal rod.


MESENTERON.


755


It develops in Elasmobranch embryos in two sections, one situated in the head, and the other in the trunk.

The section in the trunk is the first to appear. The wall of the alimentary canal becomes thickened along the median dorsal line (fig. 412, r), or else produced into a ridge into which there penetrates a narrow prolongation of the lumen of the alimentary canal. In either case the cells at the extreme summit become gradually constricted off as a rod, which lies immediately dorsal to the alimentary tract, and ventral to the notochord (fig. 413, *).



FIG. 412. TRANSVERSE SECTION THROUGH THE TAIL REGION OF A PRISTIURUS EMBRYO OF THE SAME AGE AS FIG. 28 E.

df. dorsal fin ; sp.c. spinal cord ; //. body cavity ; sp. splanchnic layer of mesoblast ; so. somatic layer of mesoblast; mp'. portion of splanchnic mesoblast commencing to be differentiated into muscles ; ch. notochord ; x. subnotochordal rod arising as an outgrowth of the dorsal wall of the alimentary tract ; al. alimentary tract.


FIG. 413. TRANSVERSE SECTION THROUGH THE TRUNK OF AN EMBRYO SLIGHTLY OLDER THAN FIG. 28 E.

nc. neural canal ; pr. posterior root of spinal nerve; x. subnotochordal rod; ao. aorta; sc. somatic mesoblast; sp. splanchnic mesoblast; mp. muscle-plate; mp'. portion of muscle-plate converted into muscle ; Vv. portion of the vertebral plate which will give rise to the vertebral bodies ; al. alimentary tract.


In the hindermost part of the body its mode of formation differs somewhat from that above described. In this part the alimentary wall is' very thick, and undergoes no special growth prior to the formation of the subnotochordal rod ; on the contrary, a small linear portion of the wall becomes scooped out along the median dorsal line, and eventually separates from the remainder as the rod in question. In the trunk the splitting off of the rod takes place from before backwards, so that the anterior part of it is formed before the posterior.

The section of the subnotochordal rod in the head would appear to develop in the same way as that in the trunk, and the splitting off from the throat proceeds from before backwards.

482


756 MESENTERY.


On the formation of the dorsal aorta, the subnotochordal rod becomes separated from the wall of the gut and the aorta interposed between the two (fig. 367, *).

When the subnotochordal rod attains its fullest development it terminates anteriorly some way in front of the auditory vesicle, though a little behind the end of the notochord ; posteriorly it extends very nearly to the extremity of the tail and is almost co-extensive with the postanal section of the alimentary tract, though it does not reach quite so far back as the caudal vesicle (fig. 424, b x). Very shortly after it has attained its maximum size it begins to atrophy in front. We may therefore conclude that its atrophy, like its development, takes place from before backwards. During the later embryonic stages not a trace of it is to be seen. It has also been met with in Acipenser, Lepidosteus, the Teleostei, Petromyzon, and the Amphibia, in all of which it appears to develop in fundamentally the same way as in Elasmobranchii. In Acipenser it appears to persist in the adult as the subvertebral ligament (Bridge, Salensky). It has not yet been found in a fully developed form in any amniotic Vertebrate, though a thickening of the hypoblast, which may perhaps be a rudiment of it, has been found by Marshall and myself in the Chick (fig. 1 10, x).

Eisig has instituted an interesting comparison between it and an organ which he has found in a family of Chaetopods, the Capitellidas. In these forms there is a tube underlying the alimentary tract for nearly its whole length, and opening into it in front, and probably behind. A remnant of such a tube might easily form a rudiment like the subnotochordal rod of the Ichthyopsida, and as Eisig points out the prolongation into the latter during its formation of the lumen of the alimentary tract distinctly favours such a view of its original nature. We can however hardly suppose that there is any direct genetic connection between Eisig's organ in the Capitellidas and the subnotochordal rod of the Chordata.


Splanchnic mesoblast and mesentery- The mesentcron consists at first of a simple hypoblastic tube, which however becomes enveloped by a layer of splanchnic mesoblast. This layer, which is not at first continued over the dorsal side of the mesenteron, gradually grows in, and interposes itself between the hypoblast of the mesenteron, and the organs above. At the same time it becomes differentiated into two layers, viz. an outer cpithelioid layer which gives rise to part of the peritoneal epithelium, and an inner layer of undifferentiated cells which in time becomes converted into the connective tissue and muscular walls of the mesenteron. The connective tissue layers become first formed, while of the muscular layers the circular is the first to make its appearance.


ALIMENTARY CANAL. 757

Coincidently with their differentiation the connective tissuestratum of the peritoneum becomes established.

The Mesentery. Prior to the splanchnic mesoblast growing round the alimentary tube above, the attachment of the latter structure to the dorsal wall of the body is very wide. On the completion of this investment the layer of mesoblast suspending the alimentary tract becomes thinner, and at the same time the alimentary canal appears to be drawn downwards and away from the vertebral column.

In what may be regarded as the thoracic division of the general pleuroperitoneal space, along that part of the alimentary canal which will form the oesophagus, this withdrawal is very slight, but it is very marked in the abdominal region. In the latter the at first straight digestive canal comes to be suspended from the body above by a narrow flattened band of mesoblastic tissue. This flattened band is the mesentery, shewn commencing in fig. 117, and much more advanced in fig. 1 19, M. It is covered on either side by a layer of flat cells, which form part of the general peritoneal epithelioid lining, while its interior is composed of indifferent tissue.

The primitive simplicity in the arrangement of the mesentery is usually afterwards replaced by a more complicated disposition, owing to the subsequent elongation and consequent convolution of the intestine and stomach.

The layer of peritoneal epithelium on the ventral side of the stomach is continued over the liver, and after embracing the liver, becomes attached to the ventral abdominal wall (fig. 380). Thus in the region of the liver the body cavity is divided into two halves by a membrane, the two sides of which are covered by the peritoneal epithelium, and which encloses the stomach dorsally and the liver ventrally. The part of the membrane between the stomach and liver is narrow, and constitutes a kind of mesentery suspending the liver from the stomach : it is known to human anatomists as the lesser omentum.

The part of the membrane connecting the liver with the anterior abdominal wall constitutes the fa lei form or suspensory ligament of the liver. It arises by a secondary fusion, and is not a remnant of a primitive ventral mesentery (vide pp. 624 and 625).


758 MESENTERY.


The mesentery of the stomach, or mesogastrium, enlarges in Mammalia to form a peculiar sack known as the greater omentum.

The mesenteron exhibits very early a trifold division. An anterior portion, extending as far as the stomach, becomes separated off as the respiratory division. On the formation of the anal invagination the portion of the mesenteron behind the anus becomes marked off as the postanal division, and between the postanal section and the respiratory division is a middle portion forming an intestinal and cloacal division.

The respiratory division of the mesenteron.

This section of the alimentary canal is distinguished by the fact that its walls send out a series of paired diverticula, which meet the skin, and after a perforation has been effected at the regions of contact, form the branchial or visceral clefts.

In Amphioxus the respiratory region extends close up to the opening of the hepatic diverticulum, and therefore to a position corresponding with the commencement of the intestine in higher types. In the craniate Vertebrata the number of visceral clefts has become reduced, but from the extension of the visceral clefts in Amphioxus, combined with the fact that in the higher Vertebrata the vagus nerve, which is essentially the nerve of the branchial pouches, supplies in addition the walls of the oesophagus and stomach, it may reasonably be concluded, as has been pointed out by Gegenbaur, that the true respiratory region primitively included the region which in the higher types forms the oesophagus and stomach.

In Ascidians the respiratory sack is homologous with the respiratory tract of Amphioxus.

The details of the development of the branchial clefts in the different groups of Vertebrata have already been described in the systematic part of this work.

In all the Ichthyopsida the walls of a certain number of clefts become folded ; and in the mesoblast within these folds a rich capillary network, receiving its blood from the branchial arteries, becomes established. These folds constitute the true internal gills.


ALIMENTARY CANAL.


759


In addition to internal gills external branchial processes covered by epiblast are placed on certain of the visceral arches in the larva of Polypterus, Protopterus and many Amphibia. The external gills have probably no genetic connection with the internal gills.

The so-called external gills of the embryos of Elasmobranchii are merely internal gills prolonged outwards through the gill clefts.

The posterior part of the primitive respiratory division of the mesenteron becomes, in all the higher Vertebrata, the oesophagus and stomach. With reference to the development of these parts the only point worth especially noting is the fact that in Elasmobranchii and Teleostei their lumen, though present in very young embryos, becomes at a later stage completely filled up, and thus the alimentary tract in the regions of the oesophagus and stomach becomes a solid cord of cells (fig. 23 A, ces)\ as already suggested (p. 61) it seems not impossible that this feature may be connected with the fact that the cesophageal region of the throat was at one time perforated by gill clefts.

In addition to the gills two important organs, viz. the thyroid body and the lungs, take their origin from the respiratory region of the alimentary tract.

Thyroid body. In the Ascidians the origin of a groovelike diverticulum of the ventral wall of the branchial sack, bounded by two lateral folds, and known as the endostyle or hypopharyngeal groove, has already been described (p. 18). This groove remains permanently open to the pharyngeal sack,



FIG. 414. DIAGRAMMATIC VERTICAL SECTION OF A JUST-HATCHED LARVA

OF PETROMYZON. (From Gegenbaur ; after Calberla.)

o. mouth ; 6. olfactory pit ; v. septum between stomodteum and mesenteron ; h. thyroid involution ; n. spinal cord ; ch. notochord; c. heart ; a. auditory vesicle.


760


THE THYROID BODY.



and would seem to serve as a glandular organ secreting mucus. As was first pointed out by W. Miiller there is present in Amphioxus a very similar and probably homologous organ, known as the hypopharyngeal groove.

In the higher Vertebrata this organ never retains its primitive condition in the adult state. In the larva of Petromyzon there is, however, present a ventral groove-like diverticulum of the throat, extending from about the second to the fourth visceral cleft. This organ is shewn in longitudinal section in fig. 414, h, and in transverse section in fig. 415, and has been identified by W. Muller (Nos. 565 and 566) with the hypopharyngeal groove of Amphioxus and Ascidians. It does not, however, long retain its primitive condition, but its opening becomes gradually reduced to a pore, placed between the third and fourth of the permanent clefts (fig. 416, tli). This opening is retained throughout the Ammoccete condition, but the organ becomes highly complicated, with paired anterior and posterior horns and a median spiral portion. In the adult the connection with the pharynx is obliterated, and the organ is partly absorbed and partly divided up into a series of glandular follicles, and eventually forms the thyroid body.

From the consideration of the above facts W. Muller was led to the conclusion tJiat the tJiyroid body of the Craniata was derived from the endostyle or Jiypopharyngeal groove. In all the higher Vertebrata the thyroid body arises as a diverticulum of the ventral wall of the throat in the region either of the mandibular or hyoid arches (fig. 417, Tk}, which after being segmented off becomes divided up into follicles.

In Elasmobranch embryos it appears fairly early as a diverticulum from the ventral surface of the throat in the region of the niandibular arc/i, extending from the border of the mouth to the point where the ventral aorta divides into the two aortic branches of the mandibular arch (fig. 417, Th}.


FIG. 415. DIAGRAMMATIC TRANSVERSE SECTIONS THROUGH THE BRANCHIAL REGION OF YOUNG LARV.K OF PETROMYZON. (From Gegenbaur ; after Calberla.)

d. branchial region of throat.


ALIMENTARY CANAL.


761


Somewhat later it becomes in Scyllium and Torpedo solid, though still retaining its attachment to the wall of the oesophagus. It continues to grow in length, and becomes divided up into a number of solid branched lobules separated by connective tissue septa. Eventually its connection with the throat becomes lost, and the lobules develop a lumen. In Acanthias the lumen of the gland is retained (W. Miiller) till after its detachment from the


-- "


Pti



FIG. 416. DIAGRAMMATIC VERTICAL SECTION THROUGH THE HEAD OF A LARVA OF PETROMYZON.

The larva had been hatched three days, and was 4 '8 mm. in length. The optic and auditory vesicles are supposed to be seen through the tissues. The letter tv pointing to the base of the velum is where Scott believes the hyomandibular cleft to be situated.

c.h. cerebral hemisphere ; th. optic thalamus; in. infundibulum ; pn. pineal gland ; mb. mid-brain ; cb, cerebellum ; md. medulla oblongata ; au.v. auditory vesicle ; op. optic vesicle; ol. olfactory pit; m. mouth; br.c. branchial pouches; th. thyroid involution; v.ao. ventral aorta; ht. ventricle of heart ; ch. notochord.

throat. It preserves its embryonic position through life. In Amphibia it originates, as in Elasmobranchii, from the region of the mandibular arch ; but when first visible it forms a double epithelial wall connecting the throat with the nervous layer of the epidermis. It subsequently becomes detached from the epidermis, and then has the usual form of a diverticulum from the throat. In most Amphibians it becomes divided into two lobes, and so forms a paired body. The peculiar connection between the thyroid diverticulum and the epidermis in Amphibia has been noted by Gotte in Bombinator, and by Scott and Osborn in Triton. It is not very easy to see what meaning this connection can have.

In the Fowl (W. Miiller) the thyroid body arises at the end of the second or beginning of the third day as an outgrowth from the hypoblast of the throat, opposite the point of origin of the anterior arterial arch. This outgrowth becomes by the fourth day a solid mass of cells, and by the fifth ceases to be connected with the epithelium of the throat, becoming at the same time bilobed. By the seventh day it has travelled somewhat backwards, and the two lobes have completely separated from each other. By


762


THE THYROID BODY.


the ninth day the whole is invested by a capsule of connective tissue, which sends in septa dividing it into a number of lobes or solid masses of cells, and by the sixteenth day it is a paired body composed of a number of hollow branched follicles, each with a ' membrana propria,' and separated from each other by septa of connective tissue. It finally travels back to the point of origin of the carotids.

Amongst Mammalia the thyroid arises in the Rabbit (Kolliker) and Man (His) as a hollow diverticulum of the throat at the bifurcation of the foremost pair of aortic arches. It soon however becomes solid, and is eventually detached from the throat and comes to lie on the ventral side of the larynx or windpipe. The changes it undergoes are in the main similar to those in the lower Vertebrata. It becomes partially constricted into two lobes, which remain however united by an isthmus 1 . The fact that the thyroid sometimes arises in the region of the first and sometimes in that of the second cleft is probably to be explained



Tli


FIG. 417. SECTION THROUGH THE HEAD OF AN ELASMOBRANCH EMBRYO, AT THE LEVEL OF THE AUDITORY INVOLUTION.

Th. rudiment of thyroid body ; aup. auditory pit ; aim. ganglion of auditory nerve ; iv. v. roof of fourth ventricle ; a.c.v. anterior cardinal vein ; aa. aorta ; f.aa aortic trunk of mandibular arch ; //. head cavity of mandibular arch ; Ivc. alimentary pouch which will form the first visceral cleft.


by its rudimentary character.

The Thymus gland. The thymus gland may conveniently be dealt with here, although its origin is nearly as obscure as its function. It has usually been held to be connected with the lymphatic system. Kolliker was the first to shew that this view was probably erroneous, and he attempted to prove that it was derived in the Rabbit from the walls of one of the visceral clefts, mainly on the ground of its presenting in the embryo an epithelial character.

1 Wolfler (No. 571) states that in the Pig and Calf the thyroid body is formed as a pair of epithelial vesicles, which are developed as outgrowths of the walls of the first pair of visceral clefts. He attempts to explain the contradictory observations of other embryologists by supposing that they have mistaken the ventral ends of visceral pouches for an unpaired outgrowth of the throat. Stieda (No. 569) also states that in the Pig and Sheep the thyroid arises as a paired body from the epithelium of a pair of visceral clefts, at a much later period than would appear from the observations of His and Kolliker. In view of the comparative development of this organ it is difficult to accept either Wolfler's or Stieda's account. Wolfler's attempt to explain the supposed errors of his predecessors is certainly not capable of being applied in the case of Elasmobranch Fishes, or of Petromyzon ; and I am inclined to think that the method of investigation by transverse sections, which has been usually employed, is less liable to error than that by longitudinal sections which he has adopted.


ALIMENTARY CANAL. 763


Stieda (No. 569) has recently verified Kolliker's statements. He finds that in the Pig and the Sheep the thymus arises as a paired outgrowth from the epithelial remnants of a pair of visceral clefts. Its two lobes may at first be either hollow (Sheep) or solid (Pig), but eventually become solid, and unite in the median line. Stieda and His hold that in the adult gland, the so-called corpuscles of Hassall are the remnants of the embryonic epithelial part of the gland, and that the lymphatic part of it is of mesoblastic origin ; but Kolliker believes the lymphatic cells to be direct products of the embryonic epithelial cells.

The posterior visceral clefts in the course of their atrophy give rise to various more or less conspicuous bodies of a pseudo-glandular nature, which have been chiefly studied by Remak 1 .

Swimming bladder and lungs. A swimming bladder is present in all Ganoids and in the vast majority of Teleostei. Its development however is only imperfectly known.

In the Salmon and Carp it arises, as was first shewn by Von Baer, as an outgrowth of the alimentary tract, shortly in front of the liver. In these forms it is at first placed on the dorsal side and slightly to the right, and grows backwards on the dorsal side of the gut, between the two folds of the mesentery.

The absence of a pneumatic duct in the Physoclisti would appear to be due to a post-larval atrophy.

In Lepidosteus the air-bladder appears to arise, as in the Teleostei, as an invagination of the dorsal wall of the oesophagus.

In advanced embryos of Galeus, Mustelus and Acanthias, MikluchoMaclay detected a small diverticulum opening on the dorsal side of the oesophagus, which he regards as a rudiment of a swimming bladder. This interpretation must however be regarded as somewhat doubtful.

The lungs. The lungs originate in a nearly identical way in all the Vertebrate forms in which their development has been observed. They are essentially buds or processes of the ventral wall of the primitive oesophagus.

At a point immediately behind the region of the visceral clefts the cavity of the alimentary canal becomes compressed laterally, and at the same time constricted in the middle, so that its transverse section (fig. 418 i) is somewhat hourglass-shaped, and shews an upper or dorsal chamber d, joining on to a lower or ventral chamber / by a short narrow neck.

1 For details on these organs vide Kolliker, Entwicklungsgeschichte, p. 88 1.


764


THE LUNGS.



The hinder end of the lower tube enlarges (fig. 418 2), and then becomes partially divided into two lobes (fig. 418 3). All these parts at first freely communicate, but the two lobes, partly by their own growth, and partly by a process of constriction, soon become isolated posteriorly; while in front they open into the lower chamber of the oesophagus (fig. 422).

By a continuation forwards of the process of constriction the lower chamber of the oesophagus, carrying with it the two lobes above mentioned, becomes gradually transformed into an independent tube, opening in front by a narrow slit-like aperture into the oesophagus. The single tube in front is the rudiment of the trachea and larynx, while the two diverticula behind become (fig. 419, Ig) the bronchial tubes and lungs.

While the above changes are taking place in the hypoblastic walls of the alimentary tract, the splanchnic mesoblast surrounding these structures becomes very much thickened ; but otherwise bears no marks of the internal changes which are going on, so that the above formation of the lungs and trachea cannot be seen from the surface. As the paired diverticula of the lungs grow backwards, the mesoblast around them takes however the form of two lobes, into which they gradually bore their way.

There do not seem to be any essential differences in the mode of formation of the above structures in the types so far observed, viz. Amphibia, Aves and Mammalia. Writers differ as to whether the lungs first arise as


FlG. 418. FOUR DIAGRAMS ILLUSTRATING THE FORMATION OF THE LUNGS.

(After Gotte.)

a. mesoblast; b. hypoblast; d. cavity of digestive canal ; /. cavity of the pulmonary diverticulum.

In (i) the digestive canal has commenced to be constricted into an upper and lower canal ; the former the true alimentary canal, the latter the pulmonary tube; the two tubes communicate with each other in the centre.

In (2) the lower (pulmonary) tube has become expanded.

In (3) the expanded portion of the tube has become constricted into two tubes, still communicating with each other and with the digestive canal.

In (4) these are completely separated from each other and from the digestive canal, and the mesoblast has also begun to exhibit externally changes corresponding to the internal changes which have been going on.


ALIMENTARY CANAL.


765


re


paired diverticula, or as a single diverticulum ; and as to whether the rudiments of the lungs are established before those of the trachea. If the above account is correct it would appear that any of these positions might be maintained. Phylogenetically interpreted the ontogeny of the lungs appears however to imply that this organ was first an unpaired structure and has become secondarily paired, and that the trachea was relatively late in appearing.

The further development of the lungs is at first, in the higher types at any rate, essentially similar to that of a racemose gland. From each primitive diverticulum numerous branches are given off In Aves and Mammalia (fig. 355) they are mainly confined to the dorsal and lateral parts. These branches penetrate into the surrounding mesoblast and continue to give rise to secondary and tertiary branches. In the meso


At


FIG. 419. SECTION THROUGH THE CARDIAC REGION OF AN EMBRYO OF LACERTA MURALIS OF 9 MM. TO SHEW THE MODE OF FORMATION OF THE PERICARDIAL CAVITY.

ht. heart ; pc . pericardial cavity ; al. alimentary tract; Ig. lung; /. liver; pp. body cavity; md. open end of Mullerian duct; wd. Wolffian duct ; vc. vena cava inferior ; ao. aorta; ch. notochord; me, medullary cord.


blast around them numerous capillaries make their appearance, and the further growth of the bronchial tubes is supposed by Boll to be due to the mutual interaction of the hitherto passive mesoblast and of the hypoblast.

The further changes in the lungs vary somewhat in the different forms.

The air sacks are the most characteristic structures of the avian lung. They are essentially the dilated ends of the primitive diverticula or of their main branches.

In Mammalia (Kolliker, No. 298) the ends of the bronchial tubes become dilated into vesicles, which may be called the primary air-cells. At first, owing to their development at the ends of the bronchial branches, these are confined to the surface of the lungs. At a later period the primary air-cells divide each into two or three parts, and give rise to secondary air-cells, while at the same time the smallest bronchial tubes, which continue all the while to divide, give rise at all points to fresh air-cells. Finally the bronchial tubes cease to become more branched, and the air-cells belonging to each minute lobe come in their further growth to open into a common chamber.


766 THE CLOACA.


Before the lungs assume their function the embryonic air-cells undergo a considerable dilatation.

The trachea and larynx. The development of the trachea and larynx does not require any detailed description. The larynx is formed as a simple dilatation of the trachea. The cartilaginous structures of the larynx are of the same nature as those of the trachea.

It follows from the above account that the whole pulmonary structure is the result of the growth by budding of a system of branched hypoblastic tubes in the midst of a mass of mesoblastic tissue, the hypoblastic elements giving rise to the epithelium of the tubes, and the mesoblast providing the elastic, muscular, cartilaginous, vascular, and other connective tissues of the tracheal and bronchial walls.

There can be no doubt that the lungs and air-bladder are homologous structures, and the very interesting memoir of Eisig on the air-bladder of the Chaetopoda 1 shews it to be highly probable that they are the divergent modifications of a primitive organ, which served as a reservoir for gas secreted in the alimentary tract, the gas in question being probably employed for respiration when, for any reason, ordinary respiration by the gills was insufficient.

Such an organ might easily become either purely respiratory, receiving its air from the exterior, and so form a true lung ; or mainly hydrostatic, forming an air-bladder, as in Ganoidei and Teleostei.

It is probable that in the Elasmobranchii the air-bladder has become aborted, and the organ discovered by Micklucho-Maclay may perhaps be a last remnant of it.

The middle division of the mesenteron. The middle division of the mesenteron, forming the intestinal and cloacal region, is primitively a straight tube, the intestinal region of which in most Vertebrate embryos is open below to the yolksack.

Cloaca. In the Elasmobranchii, the embryos of which probably retain a very primitive condition of the mesenteron, this region is not at first sharply separated from the postanal section behind. Opposite the point where the anus will even 1 H. Eisig, " Ueb. d. Vorkommen eines schwimmblasenahnlichen Organs bei Anneliden." Mittheil. a. d. zool. Station z. Neafel, Vol. II. 1881.


ALIMENTARY CANAL.


767


tually appear a dilatation of the mesenteron arises, which comes in contact with the external skin (fig. 28 E, an}. This dilatation becomes the hypoblastic section of the cloaca. It communicates behind with the postanal gut (fig. 424 D), and in front with the intestine ; and may be defined as the dilated portion of the alimentary tract which receives the genital and urinary ducts and opens externally by the proctodczum.

In Acipenser and Amphibia the cloacal region is indicated as a ventral diverticulum of the mesenteron even before the closure of the blastopore. It is shewn in the Amphibia at an early stage in fig. 73, and at a later period, when in contact with the skin at the point where the anal invagination is about to appear, in fig. 420.



FIG. 420. LONGITUDINAL SECTION THROUGH AN ADVANCED EMBRYO OF

BOMBINATOR. (After Gotte.)

m. mouth ; an. anus ; /. liver ; ne. neurenteric canal ; me. medullary canal ; ch. notochord ; pn. pineal gland.

In the Sauropsida and Mammalia the cloaca appears as a dilatation of the mesenteron, which receives the opening of the allantois almost as soon as the posterior part of the mesenteron is established.

The eventual changes which it undergoes have been already dealt with in connection with the urinogenital organs.

Intestine. The region in front of the cloaca forms the intestine. In certain Vertebrata it nearly retains its primitive character as a straight tube ; and in these types its anterior part is characterised by the presence of a peculiar fold, which in a highly specialised condition is known as the spiral valve. This structure appears in its simplest form in Ammocoetes. It


768 THE INTESTINE.


there consists of a fold in the wall of the intestine, giving to the lumen of this canal a semilunar form in section, and taking a half spiral.

In Elasmobranchii a similar fold to that in Ammoccetes first makes its appearance in the embryo. This fold is from the first not quite straight, but winds in a long spiral round the intestine. In the course of development it becomes converted into a strong ridge projecting into the lumen of the intestine (fig. 388, /). The spiral it makes becomes much closer, and it thus acquires the form of the adult spiral valve. A spiral valve is also found in Chimaera and Ganoids. No rudiment of such an organ is found in the Teleostei, the Amphibia, or the higher Vertebrata.

The presence of this peculiar organ appears to be a very primitive Vertebrate character. The intestine of Ascidians exhibits exactly the same peculiarity as that of Ammoccetes, and we may probably conclude from embryology that the ancestral Chordata were provided with a straight intestine having a fold projecting into its lumen, to increase the area of the intestinal epithelium.

In all forms in which there is not a spiral valve, with the exception of a few Teleostei, the intestine becomes considerably longer than the cavity which contains it, and therefore necessarily more or less convoluted.

The posterior part usually becomes considerably enlarged to form the rectum or in Mammalia the large intestine.

In Elasmobranchii there is a peculiar gland opening into the dorsal side of the rectum, and in many other forms there is a caecum at the commencement of the rectum or of the large intestine.

In Teleostei, the Sturgeon and Lepidosteus there opens into the front end of the intestine a number of caecal pouches known as the pancreatic caeca. In the adult Sturgeon these pouches unite to form a compact gland, but in the embryo they arise as a series of isolated outgrowths of the duodenum.

Connected with the anterior portion of the middle region of the alimentary canal, which may be called the duodenum, are two very important and constant glandular organs, the liver and the pancreas.


ALIMENTARY CANAL.


769


ITlf



The liver. The liver is the earliest formed and largest glandular organ in the embryo.

It appears in its simplest form in Amphioxus as a single unbranched diverticulum of the alimentary tract, immediately behind the respiratory region, which is directed forwards and placed on the left side of the body.

In all true Vertebrata the gland has a much more complicated structure. It arises as a ventral outgrowth of the duodenum (fig. 420, /). This outgrowth may be at first single, and then grow out into two lobes, as in Elasmobranchii (fig. 421) and Amphibia, or have from the first the form of two somewhat unequal diverticula, as in Birds (fig. 422), or again as in the Rabbit (Kolliker) one diverticulum may be first formed, and a second one appear somewhat later. The hepatic diverticula, whatever may be their primitive form, grow into a special thickening of the splanchnic mesoblast.

From the primitive diverticula there are soon given off a number of hollow buds (fig. 421) which rapidly increase in length and number, and form the so-called hepatic cylinders. They soon anastomose and unite together, and so constitute an irregular network. Coincidently with the formation of the hepatic network the united vitelline and visceral vein or veins (u.v\ in their passage through the liver, give off numerous branches, and gradually break up into a plexus of channels which form a secondary network amongst the hepatic cylinders. In Amphibia these channels are stated by Gotte to be lacunar, but in Elasmobranchii, and probably Vertebrata generally, they arc from the first provided with distinct though delicate walls. B. in. 49


FIG. 421. SECTION THROUGH THE VENTRAL PART OF THE TRUNK OF A YOUNG EMBRYO OF SCYLLIUM AT THE LEVEL OF THE UMBILICAL CORD.

b. pectoral fin ; ao. dorsal aorta ; cav. cardinal vein; ua. vitelline artery ; nv. vitelline vein united with subintestinal vein ; al. duodenum ; /. liver ; sd. opening of segmental duct into the body-cavity ; mp. muscle-plate ; urn. umbilical canal.


770


THE LIVER.


It is still doubtful whether the hepatic cylinders are as a rule hollow or solid. In Elasmobranchii they are at first provided with a large lumen, which though it becomes gradually smaller never entirely vanishes. The same seems to hold good for Amphibia and some Mammalia. In Aves the lumen of the cylinders is even from the first much more difficult to see, and the cylinders are stated by Remak to be solid, and he has been followed in this matter by Kolliker. In the Rabbit also Kolliker finds the cylinders to be solid.

The embryonic hepatic network gives rise to the parenchyma of the adult liver, with which in its general arrangement it closely agrees. The blood-channels are at first very large, and have a very irregular arrangement ; and it is not till comparatively late that the hepatic lobules with their characteristic vascular structures become established.

The biliary ducts are formed either from some of the primitive hepatic cylinders, or, as would seem to be the case in Elasmobranchii and Birds (fig. 422), from the larger diverticula of the two primitive outgrowths.

The gall-bladder is so inconstant, and the arrangement of the ducts opening into the intestine so variable, that no general statements can be made about them. In Elasmobranchii the primitive median diverticulum (fig. 421) gives rise to the ductus choledochus. Its anterior end dilates to form a gall-bladder.

In the Rabbit a ductus choledochus is formed by a diverticulum from the intestine at the point of insertion of the two primitive lobes. The gall-bladder arises as a diverticulum of the right primitive lobe.

The liver is relatively very large during embryonic life and has, no doubt, important functions in connection with the circulation.



r


FIG. 422. DIAGRAM OF THE DIGESTIVE TRACT OF A CHICK UPON THE FOURTH DAY. (After Gotte.)

The black line indicates the hypoblast. The shaded part around it is the splanchnic mesoblast.

Ig. lung ; st. stomach ; p. pancreas ; /. liver.


ALIMENTARY CANAL.


771


The pancreas. So far as is known the development of the pancreas takes place on a very constant type throughout the series of craniate Vertebrata, though absent in some of the Teleostean fishes and Cyclostomata, and very much reduced in most Teleostei and in Petromyzon.

It arises nearly at the same time as the liver in the form of a hollow outgrowth from the dorsal side of the intestine nearly opposite but slightly behind the hepatic outgrowth (fig. 422, /). It soon assumes, in Elasmobranchii and Mammalia, somewhat the form of an inverted funnel, and from the expanded dorsal part of the funnel there grow out numerous hollow diverticula into the passive splanchnic mesoblast.

As the ductules grow longer and become branched, vascular processes grow in between them, and the whole forms a compact glandular body in the mesentery on the dorsal side of the alimentary tract. The funnel-shaped receptacle loses its origi nal form, and elongating, assumes the character of a duct.

From the above mode of development it is clear that the glandular cells of the pancreas are derived from the hypoblast.

Into the origin of the varying arrangements of the pancreatic ducts it is not possible to enter in detail. In some cases, e.g. the Rabbit (Kolliker), the two lobes and ducts arise from a division of the primitive gland and duct. In other cases, e.g. the Bird, a second diverticulum springs from the alimentary tract. In a large number of instances the primitive condition with a single duct is retained.

Postanal section of the mesenteron. In the embryos of all the Chordata there is a section of the mesenteron placed behind the anus. This section invariably atrophies at a comparatively early period of embryonic life ; but it is much better developed in the lower forms than in the higher. At its posterior extremity it is primitively continuous with the neural tube (fig. 420), as was first shewn by Kowalevsky.

The canal connecting the neural and alimentary canals has already been described as the neurenteric canal, and represents the remains of the blastopore.

In the Tunicata the section of the mesenteron, which in all probability corresponds to the postanal gut of the Vertebrata, is that immediately

492



772 POSTANAL SECTION OF THE MESENTERON.

following the dilated portion which gives rise to the branchial cavity

and permanent intestine. It has already

been shewn that from the dorsal and

lateral portions of this section of the

primitive alimentary tract the notochord

and muscles of the Ascidian tadpole are

derived. The remaining part of its walls

forms a solid cord of cells (fig. 423, al'},

which either atrophies, or, according to

Kowalevsky, gives rise to blood-vessels.

In Amphioxus the postanal gut, FIG. 423. TRANSVERSE OPTICAL

.hough distinctly developed, is no, very % long, and atrophies at a comparatively (After Kowalevsky.) early period. The sect i on ; s f rom an embryo of

In Elasmobranchii this section of the the same age as fig. 8 iv.

alimentary tract is very well developed, ch - notochord ; nc neural 1 canal ;

. , , me. mesoblast ; of. hypoblast of and persists for a considerable period of ta ji <

embryonic life. The following is a history of its development in the genus Scyllium.

Shortly after the stage when the anus has become marked out by the alimentary tract sending down a papilliform process towards the skin, the postanal gut begins to develop a terminal dilatation or vesicle, connected with the remainder of the canal by a narrower stalk.

The walls both of the vesicle and stalk are formed of a fairly columnar epithelium. The vesicle communicates in front by a narrow passage with the neural canal, and behind is continued into two horns corresponding with the two caudal swellings previously spoken of (p. 55). Where the canal is continued into these two horns, its walls lose their distinctness of outline, and become continuous with the adjacent mesoblast.

In the succeeding stages, as the tail grows longer and longer, the postanal section of the alimentary tract grows with it, without however undergoing alteration in any of its essential characters. At the period of the maximum development, it has a length of about -J of that of the whole alimentary tract.

Its features at a stage shortly before the external gills have become prominent are illustrated by a series of transverse sections through the tail (fig. 424). The four sections have been selected for illustration out of a fairly-complete series of about one hundred and twenty.

Posteriorly (A) there is present a terminal vesicle (alv) '25 mm. in diameter, which communicates dorsally by a narrow opening with the neural canal (nc) ; to this is attached a stalk in the form of a tube, also lined by columnar epithelium, and extending through about thirty sections (B al}. Its average diameter is about '084 mm., and its walls are very thick. Overlying its front end is the subnotochordal rod (x), but this does not extend as far back as the terminal vesicle.

The thick-walled stalk of the vesicle is connected with the cloacal section


ALIMENTARY CANAL.


773


of the alimentary tract by a very narrow thin-walled tube (C of). This for the most part has a fairly uniform calibre, and a diameter of not more than 035 mm. Its walls are formed of flattened epithelial cells. At a point not far from the cloaca it becomes smaller, and its diameter falls to -03 mm. In



cl.al


FIG. 424. FOUR SECTIONS THROUGH THE POSTANAL PART OF THE TAIL OF AN EMBRYO OF THE SAME AGE AS FIG. 28 F.

A. is the posterior section.

nc . neural canal ; al. postanal gut ; alv. caudal vesicle of postanal gut ; x. subnotochordal rod; mp. muscle-plate; ch. notochord; cl.al. cloaca; ao. aorta; v.cau, caudal vein.

front of this point it rapidly dilates again, and, after becoming fairly wide, opens on the dorsal side of the cloacal section of the alimentary canal just behind the anus (D al}.

Very shortly after the stage to which the above figures belong, at a point a little behind the anus, where the postanal section of the canal was thinnest in the previous stage, it becomes solid, and a rupture here occurs in it at a slightly later period.

The atrophy of this part of the alimentary tract having once commenced proceeds rapidly. The posterior part first becomes reduced to a small rudiment near the end of the tail. There is no longer a terminal vesicle, nor a neurenteric canal. The portion of the postanal section of the alimentary tract, just behind the cloaca, is for a short time represented by a small rudiment of the dilated part which at an earlier period opened into the cloaca.

In Teleostei the vesicle at the end of the tail, discovered by Kupffer,


774 THE STOMOD/EUM.


(fig- 34> hyv) is probably the equivalent of the vesicle at the end of the postanal gut in Elasmobranchii.

In Petromyzon and in Amphibia there is a well-developed postanal gut connected with a neurenteric canal which gradually atrophies. It is shewh in the embryo of Bombinator in fig. 420.

Amongst the amniotic Vertebrata the postanal gut is less developed than in the Ichthyopsida. A neurenteric canal is present for a short period



FIG. 425. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR END OF AN EMBRYO BlRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS.

ep. epiblast ; Sp.c. spinal canal ; ch. notochord ; n.e. neurenteric canal ; hy. hypoblast ; p.a.g, postanal gut ; pr. remains of primitive streak folded in on the ventral side ; al. allantois ; me. splanchnic mesoblast ; an. point where anus will be formed ; p.c. perivisceral cavity ; am. amnion ; so. somatopleure ; sp. splanchnopleure.

in various Birds (Gasser, etc.) and in the Lizard, but disappears very early. There is however, as has been pointed out by Kolliker, a well-marked postanal gut continued as a narrow tube from behind the cloaca into the tail both in the Bird (fig. 425, p.a.g.} and Mammals (the Rabbit), but especially in the latter. It atrophies early as in lower forms.

The morphological significance of the postanal gut and of the neurenteric canal has already been spoken of in Chapter xii., p. 323.


The anterior section of the permanent alimentary tract is formed by an invagination of epiblast, constituting a more or less considerable pit, with its inner wall in contact with the blind anterior extremity of the alimentary tract.

In Ascidians this pit is placed on the dorsal surface (fig. 9, o), and becomes the permanent oral cavity of these forms. In the larva of Amphioxus it is stated to be formed unsymmetrically


THE STOMOD/EUM.


775



(vide p. 5), but further observations on its development are required.

In the true Vertebrata it is always formed on the ventral surface of the head, immediately behind the level of the forebrain (fig. 426), and is deeper in Petromyzon (fig. 416, ;) than in any other known form.

From the primary buccal cavity or stomodaeum there grows out the pituitary pit (fig. 426, pt\ the development of which has already been described (p. 435).

The wall separating the stomodaeum from the mesenteron always becomes perforated, usually at an early stage of development, and though in Petromyzon the boundary between the two cavities remains indicated by the velum, yet in the higher Vertebrata all trace of this boundary is lost, and the original limits of the primitive buccal cavity become obliterated ; while a secondary buccal cavity, partly lined by hypoblast and partly by epiblast, becomes established.

This cavity, apart from the organs which belong to it, presents important variations in structure. In most Pisces it retains a fairly simple character, but in the Dipnoi its outer boundary becomes extended so as to enclose the ventral opening of the nasal sack, which thenceforward constitutes the posterior nares.

In Amphibia and Amniota the posterior nares also open well within the boundary of the buccal cavity.

In the Amniota further important changes take place.

In the first place a plate grows inwards from each of the superior maxillary processes (fig. 427, /), and the two plates, meeting in the middle line, form a horizontal septum dividing the front part of the primitive buccal cavity into a dorsal respiratory section (), containing the opening of the posterior nares, and a ventral cavity, forming the permanent mouth. The


FIG. 426. LONGITUDINAL SECTION THROUGH THE BRAIN OF A YOUNG PRISTIURUS EMBRYO.

r.unpaired rudimentofthecerebral hemispheres \pn. pineal gland ; /w.infundibulum ; //.ingrowth from mouth to form the pituitary body ; mb. mid-brain ; cb. cerebellum ; ch. notochord; al. alimentary tract; Zaa. artery of mandibular arch.


THE TEETH.



two divisions thus formed open into a common cavity behind. The horizontal septum, on the development within it of an osseous plate, constitutes the hard palate.

An internasal septum (fig. 427, e) may more or less completely divide the dorsal cavity into two canals, continuous respectively with the two nasal cavities.

In Mammalia a posterior prolongation of the palate, in which an osseous plate is not formed, constitutes the soft palate.

The second change in the Amniota, which also takes place in some Amphibia, is caused by the section of the mesenteron into which the branchial pouches open, becoming, on the atrophy of these structures, converted into the posterior part of the buccal cavity.

The organs derived from the buccal cavity are the tongue, the various salivary glands, and the teeth ; but the latter alone will engage our attention here.

The teeth. The teeth are to be regarded as a special product of the oral mucous membrane. It has been shewn by Gegenbaur and Hertwig that in their mode of development they essentially resemble the placoid scales of Elasmobranchii, and that the latter structures extend in Elasmobranchii for a certain distance into the cavity of the mouth.

As pointed out by Gegenbaur, the teeth are therefore to be regarded as more or less specialised placoid scales, whose presence in the mouth is to be explained by the fact that the latter structure is lined by an invagination of the epidermis. The most important developmental point of difference between teeth and placoid scales consists in the fact, that in the case of the former there is a special ingrowth of epiblast to meet a connective tissue papilla which is not found in the latter.


FIG. 427. DIAGRAM SHEWING THE DIVISION OF THE PRIMITIVE BUCCAL CAVITY INTO THE RESPIRATORY SECTION ABOVE AND THE TRUE MOUTH BELOW. (From Gegenbaur.)

p. palatine plate of superior maxillary process; m. permanent mouth ; n. posterior part of nasal passage; e. internasal septum.


Although the teeth are to be regarded as primitively epiblastic structures, they are nevertheless found in Teleostei and Ganoidei on the hyoid


THE STOMOD/KUM.


777


and branchial arches ; and very possibly the teeth on some other parts of the mouth are developed in a true hypoblastic region.

The teeth are formed from two distinct organs, viz. an epithelial cap and a connective tissue papilla.

The general mode of development, as has been more especially shewn by the extended researches of Tomes, is practically the same for all Vertebrata, and it will be convenient to describe it as it takes place in Mammalia.

Along the line where the teeth are about to develop, there is formed an epithelial ridge projecting into the subjacent connective tissue, and derived from the innermost columnar layer of the oral epithelium. At the points where a tooth is about to be formed this ridge undergoes special changes. It becomes in the first place somewhat thickened by the development of a number of rounded cells in its interior ; so that it becomes constituted of (i) an external layer of columnar cells, and (2) a central core of rounded cells ; both of an epithelial nature. In the second place the organ gradually assumes a dome-shaped form (fig. 428, e), and covers over a papilla of the subepithelial connective tissue (p] which has in the meantime been developed.

From the above epithelial structure, which may be called the enamel organ, and from the papilla it covers, which maybe spoken of as the dental papilla, the whole tooth is developed. After these parts have become established there is formed round the rudiment of each tooth a special connective tissue capsule ; known as the dental capsule.

Before the dental capsule has become definitely formed the enamel organ and the dental papilla undergo important changes. The rounded epithelial cells forming the core of the enamel organ undergo a peculiar transformation into a tissue closely resembling ordinary embryonic connective tissue, while at the same time the epithelium adjoining the dental papilla and covering the inner surface of the enamel organ, acquires a somewhat different structure to the epithelium on the outer side of the organ. Its cells become very markedly columnar, and form a very regular cylindrical epithelium. This layer alone is concerned in forming the enamel. The cells of the outer epithelial layer of the enamel organ become somewhat flattened, and the surface of the layer is raised into a series of short papilla? which project into the highly vascular tissue of the dental sheath. Between



FIG. 428. DIAGRAM SHEWING THE DEVELOPMENT OF THE TEETH. (From Gegenbaur.)

p. dental papilla ; e. enamel organ.


778 THE PROCTOD/EUM.

the epithelium of the enamel organ and the adjoining connective tissue there is everywhere present a delicate membrane known as the membrana praeformativa.

The dental papilla is formed of a highly vascular core and a non-vascular superficial layer adjoining the inner epithelium of the enamel organ. The cells of the superficial layer are arranged so as almost to resemble an epithelium.

The first formation of the hard structures of the tooth commences at the apex of the dental papilla. A calcification of the outermost layer of the papilla sets in, and results in the formation of a thin layer of dentine. Nearly simultaneously a thin layer of enamel is deposited over this, from the inner epithelial layer of the enamel organ (fig. 428). Both enamel and dentine continue to be deposited till the crown of the tooth has reached its final form, and in the course of this process the enamel organ is reduced to a thin layer, and the whole of the outer layer of the dental papilla is transformed into dentine while the inner portion remains as the pulp.

The root of the tooth is formed later than the crown, but the enamel organ is not prolonged over this part, so that it is only formed of dentine.

By the formation of the root the crown of the tooth becomes pushed outwards, and breaking through its sack projects freely on the surface.

The part of the sack which surrounds the root of the tooth gives rise to the cement, and becomes itself converted into the periosteum of the dental alveolus.

The general development of the enamel organs and dental papillae is shewn in the diagram (fig. 428). From the epithelial ridge three enamel organs are represented as being developed. Such an arrangement may occur when teeth are successively replaced. The lowest and youngest enamel organ (e) has assumed a cap-like form enveloping a dental papilla, but no calcification has yet taken place.

In the next stage a cap of dentine has become formed, while in the still older tooth this has become covered by a layer of enamel. As may be gathered from this diagram, the primitive epithelial ridge from which the enamel organ is formed is not necessarily absorbed on the formation of a tooth, but is capable of giving rise to fresh enamel organs. When the enamel organ has reached a certain stage of development, its connection with the epithelial ridge is ruptured (fig. 428).

The arrangement represented in fig. 428, in which successive enamel organs are formed from the same epithelial ridge, is found in most Vertebrata except the Teleostei. In the Teleostei, however (Tomes), a fresh enamel organ grows inwards from the epithelium for each successively formed tooth.

The Proctodceuni.

In all Vertebrata the cloacal section of the alimentary tract which receives the urinogenital ducts is placed in communication


THE PROCTOD/EUM.


779


with the exterior by means of an epiblastic invagination, constituting a proctodseum.

This invagination is not usually very deep, and in most instances the boundary wall between it and the hypoblastic cloaca is not perforated till considerably after the perforation of the stomodseum ; in Petromyzon, however, its perforation is effected before the mouth and pharynx are placed in communication.

The mode of formation of the proctodaeum, which is in general extremely simple, is illustrated by fig. 420 an.

In most forms the original boundary between the cpiblast of the proctodaeum and the hypoblast of the primitive cloaca becomes obliterated after the two have become placed in free communication.



FIG. 429. DIAGRAMMATIC LONGITUDINAL SECTION THROUGH THE POSTERIOR END OF AN EMBRYO BlRD AT THE TIME OF THE FORMATION OF THE ALLANTOIS.

ep. epiblast ; Sp.c. spinal canal ; ch. notochord ; n.e. neurenteric canal ; hy, hypoblast ; p.a.g. postanal gut ; pr. remains of primitive streak folded in on the ventral side ; al. allantois ; me. mesoblast ; an. point where anus will be formed ; p.c. perivisceral cavity ; am. amnion ; so. somatopleure ; sp. splanchnopleure.

In Birds the formation of the proctodseum is somewhat more complicated than in other types, owing to the outgrowth from it of the bursa Fabricii.

The proctodseum first appears when the folding off of the tail end of the embryo commences (fig. 429, an} and is placed near the front (originally the apparent hind) end of the primitive streak. Its position marks out the front border of the postanal section of the gut.

The bursa Fabricii first appears on the seventh day (in the chick), as a dorsal outgrowth of the proctodaeum. The actual perforation of the septum between the proctodeeum and the cloacal section of the alimentary tract is not effected till about the fifteenth day of fcetal life, and the approxi


780 BIBLIOGRAPHY.


mation of the epithelial layers of the two organs, preparatory to their absorption, is partly effected by the tunneling of the mesoblastic tissue between them by numerous spaces.

The hypoblastic section of the cloaca of birds, which receives the openings of the urinogenital ducts, is permanently marked off by a fold from the epiblastic section or true proctodaeum, with which the bursa Fabricii communicates.

BIBLIOGRAPHY. Alimentary Canal and its appendages.

(561) B. Afanassiew. "Ueber Bau u. Entwicklung d. Thymus d. Saugeth." Archivf. mikr. Anat. Bd. xiv. 1877.

(562) Fr. Boll. Das Princip d. Wachsthums. Berlin, 1876.

(563) E. Gasser. "Die Entstehung d. Cloakenoffnung bei Hiihnerembryonen." Archivf. Anat. u. Physiol., Anat. Abth. 1880.

(564) A. Gotte. Beilrdge zur Entivicklungsgeschichle d. Darmkanah im Hiihnchen. 1867.

(565) W. Millie r. "Ueber die Entwickelung der Schilddriise." Jenaische Zeitschrift, Vol. vi. 1871.

(566) W. Miiller. "Die Hypobranchialrinne d. Tunicaten." Jenaische Zeitschrift, Vol. VII. 1872.

(567) S. L. Schenk. "Die Bauchspeicheldriise d. Embryo." Anatomischphysiologische Untcrsuchungen. 1872.

(568) E. Selenka. " Beitrag zur Entwicklungsgeschichte d. Luftsacke d. Huhns." Zeit.f. wiss. Zool. 1866.

(569) L. Stieda. Untersuch. iib. d. Entwick. d. Glandula Thymus, Glandula thyroidea,u. Glandula car otica. Leipzig, 1881.

(570) C. Fr. Wolff. " De formatione intestinorum." Nov. Comment. Akad. Petrop. 1766.

(571) H. Wolfler. Ueb. d. Entwick. u. d. Bau d. Schilddriise. Berlin, 1880. Vide also Kolliker (298), Gotte (296), His (232 and 297), Foster and Balfour (295),

Balfour (292), Remak (302), Schenk (303), etc.

Teeth.

(572) T. H. Huxley. "On the enamel and dentine of teeth." Quart. J. of Micros. Science, Vol. in. 1855.

(573) R. Owen. Odontography . London, 1840 1845.

(574) Ch. S. Tomes. Manual of dental anatomy, human and comparative. London, 1876.

(575) Ch. S. Tomes. " On the development of teeth." Quart. J. of Micros. Science, Vol. xvi. 1876.

(576) W. Waldeyer. " Structure and development of teeth." Strieker's Histology. 1870.

Vide also Kolliker (298), Gegenbaur (294), Hertwig (306), etc.


INDEX TO VOLUME III.


Abdominal muscles, 675

Abdominal pore, 626, 749

Acipenser, development of, 102; affinities of, 1 1 8 ; comparison of gastrula of, 279 ; pericardial cavity of, 627

Actinotrocha, 373

Air-bladder of Teleostei, 77; Lepidosteus, 117; blood supply of, 645 ; general account of, 763 ; homologies of, 766

Alciope, eye of, 480

Alisphenoid region of skull, 569

Alimentary canal and appendages, development of, 754

Alimentary tract ofAscidia, 18; Molgula, 22; Pyrosoma, 24; Salpa, 31 ; Elasmobranchii, 52; Teleostei, 75; Petromyzon, 93, 97; Acipenser, no; Amphibia, 129, 136; Chick, 167; respiratory region of, 754; temporary closure of oesophageal region of, 759

Allantois, development of in Chick, 191, 198; blood-vessels of in Chick, 193; Lacerta, 205, 209; early development of in Rabbit, 229, of Guinea-pig, 264; origin of, 309. See also ' Placenta ' and 'Bladder

Alternation of generations in Ascidians, origin of, 35 ; in Botryllus, 35 ; Pyrosoma, 36; Salpa, 36; Doliolum, 36

Alytes, branchial chamber of, 136; yolksack of, 139; branchiae, 141 ; Miillerian duct of, 710

Amblystoma, ovum of, 120; larva of, 142,

H3

Amia, ribs of, 561

Ammocoetes, 95; metamorphosis of, 97;

eye of, 498 Amnion, early development of in Chick,

185; later history of in Chick, 196;

Lacerta, 204, 210; Rabbit, 229; origin

of, 3.07. 39

Amphibia, development of, 120; viviparous, 121; gastrula of, 277; suctorial mouth of, 317; cerebellum of, 426; infundibulum of, 431; pineal gland of, 433; cerebrum of, 439; olfactory lobes of, 444; nares of, 553; notochord and its sheath, 548; vertebral column of, 554; ribs of, 561 ; branchial arches of, 574; mandibular and hyoid arches of, 582 ; columella of, 582 ; pectoral girdle of, 605; pelvic girdle of, 607; limbs of, 619; heart of, 638; arterial system of, f>45 ; venous system of, 655 ; excretory


system of, 707 ; vasa efierentia of, 711; liver of, 769; postanal gut of, 774; stomodaeum of, 778

Amphiblastula larva of Porifera, 344

Amphioxus, development of, i ; gastrula of, 275 ; formation of mesoblast of, 292 ; development of notochord of, 293; head of, 314; spinal nerves of, 461; olfactory organ of, 462 ; venous system of, 651; transverse abdominal muscle f> 673; generative cells of, 748; liver of, 769; postanal gut of, 772; stomodaeum of, 777

Amphistylic skulls, 578

Angular bone, 594

Anterior abdominal vein, 653

Anura, development of, 121; epiblast of, 125; mesoblast of, 128; notochord of, 128; hypoblast of, 129; general growth of embryo of, 131; larva of, 134; vertebral column of, 556 ; mandibular arch of, 584

Anus of Amphioxus, 7 ; Ascidia, 18; Pyrosoma, 28 ; Salpa, 31 ; Elasmobranchii, 57; Amphibia, 130, 132; Chick, 167; primitive, 324

Appendicularia, development of, 34

Aqueductus vestibuli, 519

Aqueous humour, 497

Arachnida, nervous system of, 409; eye of, 481

Area, embryonic, of Rabbit, 218; epiblast

of, 219; origin of embryo from, 228

area opaca of Chick, 150; epiblast,

hypoblast, and mesoblast of, 159 area pellucida of Chick, 150; of Lacerta, 202

area vasculosa of Chick, 194; mesoblast of, 1 60; of Lizard, 209; Rabbit, 228, 229

Arteria centralis retinas, 503

Arterial system of Petromyzon, 97; constitution of in embryo, 643 ; of Fishes, 644; of Amphibia, 645; of Amniota, 647

Arthropoda, head of, 313 ; nervous system of, 409 ; eye of, 480 ; excretory organs of, 688

Articular bone of Teleostei, 581 ; of Sauropsida, 588

Ascidia, development of, 9

Ascidians. See 'Tunicata'

Ascidiozooids, 25

Atrial cavity of Amphioxus, 7; Ascidia, 18; Pyrosoma, 24


7 82


INDEX.


Atrial pore of Amphioxus, 7; Ascidia, 20; Pyrosoma, 28 ; Salpa, 32

Auditory capsules, ossifications in, 595, 59.6

Auditory involution of Elasmobranchii, 57; Teleostei, 73; Petromyzon, 89, 92; Acipenser, 106; Lepidosteus, 114; Amphibia, 127; Chick, 170

Auditory nerve, development of, 459

Auditory organs, of Ascidia, 15; of Salpa, 31; of Ammocoetes, 98; Ganoidei, 108, 114; of Amphibia, 127; of Aves, 170; general development of, 512; of aquatic forms, 512; of land forms, 513; of Ccelenterata, 513; of Mollusca, 515; of Crustacea, 516; of Vertebrata, 517; of Cyclostomata, 89, 92, 518; of Teleostei, Lepidosteus and Amphibia, 518; of Mammalia, 519; accessory structures of, 527; ofTunicata, 528

Auriculo-ventricular valves, 642

Autostylic skulls, 579

Aves, development of, 145; cerebellum of, 426; midbrain of, 427; infundibulum of, 431; pineal gland of, 434; pituitary body of, 436; cerebrum of, 439 ; olfactory lobes of, 444 ; spinal nerves of, 449 ; cranial nerves of, 455 ; vagus of, 458; glossopharyngeal of, 458; vertebral column of, 557; ossification of vertebral column of, 558; branchial arches of, 572, 573; pectoral girdle of, 603; pelvic girdle of, 608; heart of, 637 ; arterial system of, 647 ; venous system of, 658; muscle-plates of, 670; excretory organs of, 714; mesonephros of, 715; pronephros of, 718; Miillerian duct of, 718, 720; nature of pronephros of, 721 ; connection of Miillerian duct with Wolffian in, 720 ; kidney of, 722; lungs of, 764; liver of, 769; postanal gut of, 774

Axolotl, 142, 143; ovum of, 120; midbrain of, 427; mandibular arch of, 583

Basilar membrane, 524

Basilar plate, 565

Basipterygium, 612

Basisphenoid region of skull, 569

Bilateral symmetry, origin of, 373-376

Bile duct, 770

Bladder, Amphibia, 131 ; of Amniota, 726

Blastodermic vesicle, of Rabbit, first development of, 217; of 7th day, 222; Guinea-pig, 263; meaning of, 291

Blastoderm of Pyrosoma, 24; Elasmobranchii, 41; Chick, 150; Lacerta 202

Blastopore, of Amphioxus, 2; of Ascidia, II ; Elasmobranchii, 42, 54, 62 ; Petromyzon, 87; Acipenser, 104 ; Amphibia, 125, 130; Chick, 153; Rabbit, 216; true Mammalian, 226; comparative history of closure of, 284, 288; summary of fate of, 340; relation of to primitive anus, 324


Blood-vessels, development of, 633

Body cavity, of Ascidia, 2 1 ; Molgula, 2 1 ; Salpa, 31; Elasmobranchii, 47 ; of Teleostei, 75 ; Petromyzon, 94 ; Chick, 169; development of in Chordata, 325; views on origin of, 356 360, 377; of Invertebrata, 623; of Chordata, 624; of head, 676

Bombinator, branchial chamber of, 136; vertebral column of, 556

Bonellia, excretory organs of, 687

Bones, origin of cartilage bones, 542 ; origin of membrane bones, 543; development of, 543; homologies of membrane bones, 542 ; homologies of cartilage bones, 545

Brachiopoda, excretory organs of, 683 ; generative ducts of, 749

Brain, of Ascidia, IT, 15; Elasmobranchii, 56, 59, 60; Teleostei, 77; Petromyzon, 89, 92 ; Acipenser, 105 ; Lepidosteus, 113; early development of in Chick, 170; flexure of in Chick, 175; later development of in Chick, 176; Rabbit, 229, general account of development of, 419; flexureof, 420; histogeny of, 422

Branchial arches, prseoral, 570; disappearance of posterior, 573; dental plates of in Teleostei, 574; relation of to head cavities, 571 ; see ' Visceral arches'

Branchial chamber of Amphibia, 136

Branchial clefts, of Amphioxus, 7 ; of Ascidia, 18, 20; Molgula, 23; Salpa, 32; of Elasmobranchii, 57, 59 01; Teleostei, 77; Petromyzon, 91, 96; Acipenser, 105; Lepidosteus, 114, 116; Amphibia, 132, 133; Chick, 178; Rabbit, 231; praeoral, 312, 318; of Invertebrata, 326; origin of, 326

Branchial rays, 574

Branchial skeleton, development of, 572, 592; of Petromyzon, 96, 312, 571; of Ichthyopsida, 572; dental plates of in Teleostei, 574; relation of to head cavities, 572

Branchiae, external of Elasmobranchii, 6r, 62; of Teleostei, 77; Acipenser, 107; Amphibia, 127, 133, 135

Brood-pouch, of Salpa, 29 ; Teleostei, 68, Amphibia, 12 1

Brown tubes of Gephyrea, 686

Bulbus arteriosus, of Pishes, 638 ; Amphibia, 639

Bursa Fabricii, 167, 779

Canalis auricularis, 639 Canalis reuniens, 521 Capitellidre, excretory organs of, 683 Carcharias, placenta of, 66 Cardinal vein, 652 Carnivora, placenta of, 250 Carpus, development of, 620 Cartilage bones of skull, 595 ; homologies of, 595


INDEX.


783


Cat, placenta of, 250

Caudal swellings of Elasmobranchii, 46,

55; Teleostei, 72; Chick, 162, 170 Cephalic plate of Elasmobranchii, 55 Cephalochorda, development of, i Cephalopoda, eyes of, 473 477 Cerebellum, Petromyzon, 93; Chick, 176;

general account of development of, 424,

425

Cerebrum of Petromyzon, 93, 97; Chick, 175 ; general development of, 429, 438; transverse fissure of, 443 Cestoda, excretory organs of, 68 1 Cetacea, placenta, 255 Chtetognatha, nervous system of, 349; eye of, 479 ; generative organs of, 743 ; generative ducts of, 749 Chcetopoda, head of, 313; eyes of, 479; excretory organs of, 683; generative organs of, 743 ; generative ducts of, 749 Charybdnea, eye of, 472 Cheiroptera, placenta of, 244 Cheiropterygium, 618; relation of to ich thyopterygium, 621

Chelonia, development of, 210; pectoral girdle of, 603 ; arterial system of, 649 Chick, development of, 145 ; general growth of embryo of, 1 70 ; rotation of embryo of, 173; fcetal membranes of, 185; epiblast of, 150, 166; optic nerve and choroid fissure of, 500

Chilognatha, eye of, 481

Chilopoda, eye of, 481

Chimasra, lateral line of, 539 ; vertebral column of, 548; nares of, 533

Chiromantis, oviposition of, 121

Chorda tympani, development of, 460

Chordata, ancestor of, 311; branchial system of, 312; evidence from Ammocuetes, 312; head of, 312; mouth of, 318; table of phylogeny of, 327

Chorion, 237; villi of, 237, 257

Choroid coat, Ammoccetes, 99; general account of, 487

Choroid fissure, of Vertebrate eye, 486, 493 ; of Ammocoetes, 498 ; comparative development of, 500; of Chick, 501; of Lizards, 501 ; of Elasmobranchii, 502 ; of Teleostei, 503 ; Amphibia, 503 ; Mammals, 503, 504

Choroid gland, 320

Choroid pigment, 489

Choroid plexus, of fourth ventricle, 425 ; of third ventricle, 432 ; of lateral ventricle, 442

Ciliated sack of Ascidia, 18; Pyrosoma, 26; Salpa, 31

Ciliary ganglion, 461

Ciliary muscle, 490

Ciliary processes, 488; comparative development of, 506

Clavicle, 600

Clitoris, development of, 727

Clinoid ridge, 569

Cloaca, 766


Coccygeo-mesenteric vein, 66 1

Cochlear canal, 519

Coecilia, development of, 143; pronephros of, 707; mesonephros of, 709; Mill lerian duct of, 710

Coelenterata, larvae of, 367 ; eyes of, 47 1 ; auditory organs of, 513; generative organs of, 741

Columella auris, 529; of Amphibia, 582 ; of Sauropsida, 588

Commissures, of spinal cord, 417; of brain, 431, 432, 439, 443

Coni vasculosi, 724

Conus arteriosus, of Fishes, 638; of Amphibia, 638

Coracoid bone, 599

Cornea, of Ammocretes, 99 ; general development of, 495 ; corpuscles of, 496 ; comparative development of, 499; of Mammals, 499

Coronoid bone, 595

Corpora geniculata interna, 428

Corpora quadrigemina, 428

Corpora striata, development of, 437

Corpus callosum, development of, 443

Corti, organ of, 522; structure of, 525; fibres of, 525 ; development of, 526

Cranial flexure, of Elasmobranchii, 58, 60; of Teleostei, 77; Petromyzon, 93, 94; of Amphibia, 131, 132; Chick, 174; Rabbit, 231; characters of, 321; significance of, 322

Cranial nerves, development of, 455; relation of to head cavities, 461 ; anterior roots of, 462 464; view on position of roots of, 466

Crocodilia, arterial system of, 649

Crura cerebri, 429

Crustacea, nervous system of, 41 1 ; eye of, 481; auditory organs of, 515; generative cells of, 745 ; generative ducts of,

75

Cupola, 524

Cutaneous muscles, 676

Cyathozooid, 25

Cyclostomata, auditory organs of, 517; olfactory organ of, 532; notochord and vertebral column of, 546, 549; abdominal pores of, 626 ; segmental duct of, 700 ; pronephros of, 700 ; mesonephros of, 700 ; generative ducts of, 733, 749 ; venous system of, 651 ; excretory organs of, 700

Cystignathus, oviposition of, 122

Dactylethra, branchial chamber of, 136;

branchise of, 136; tadpole of, 140 Decidua reflexa, of Rat, 242 ; of Insecti vora, 243; of Man, 245 Deiter's cells, 526 Dental papilla, 777 Dental capsule, 777 Dentary bone, 595 Dentine, 780 Descemet's membrane, 496


784


INDEX.


Diaphragm, 631 ; muscle of, 676

Dipnoi, nares of, 534; vertebral column of, 548; membrane bones of skull of, 592 ; heart of, 638 ; arterial system of, 645 ; excretory system of, 707 ; stomodseum of, 777

Diptera, eye of, 481

Discophora, excretory organs of, 687

Dog, placenta of, 248

Dohni, on relations of Cyclostomata, 84 ; on ancestor of Chordata, 311, 319

Doliolum, development of, 28

Ductus arteriosus, 649

Ductus Botalli, 648

Ductus Cuvieri, 654

Ductus venosus Arantii, 663

Dugong, heart of, 642

Dysticus, eye of, 481

Ear, see ' Auditory organ '

Echinodermata, secondary symmetry of larva of, 380; excretory organs of, 689 ; generative ducts of, 752

Echinorhinus, lateral line of, 539; vertebral column of, 548

Echiurus, excretory organs of, 686

Ectostosis, 543

Edentata, placenta of, 248, 250, 256

Eel, generative ducts of, 703

Egg-shell of Elasmobranchii, 40 ; Chick, 146

Elasmobranchii, development of, 40; viviparous, 40; general features of development of, 55 ; gastrulaof, 281 ; development of mesoblast of, 294 ; notochord of, 294 ; meaning of formation of mesoblast of, 295; restiform tracts of, 425 ; optic lobes of, 427 ; cerebellum of, 425 ; pineal gland of, 432 ; pituitary body of, 435 ; cerebrum of, 438 ; olfactory lobes of, 444 ; spinal nerves, 449 ; cranial nerves of, 457; sympathetic nervous system of, 466; nares of, 533; lateral line of, 539; vertebral column of, 549 ; ribs of, 560 ; parachordals of, 567 ; mandibular and hyoid arches of, 576 ; pectoral girdle of, 600 ; pelvic girdle of, 607; limbs of, 609; pericardial cavity of, 627; arterial system of, 644 ; venous system of, 65 1 ; muscle-plates of, 668 ; excretory organs of, 690 ; constitution of excretory organs in adult of, 697; spermatozoa of, 747 ; swimming-bladder of, 763 ; intestines of, 767 ; liver of, 769; postanal gut of, 772

Elrcoblast of Pyrosoma, 28; Salpa, 30

Elephant, placenta of, 249

Embolic formation of gastrula, 333

Enamel organ, 777

Endolymph of ear, 522

Endostosis, 543

Endostyle of Ascidia, 18, 759; Pyrosoma, 25; Salpa, 32

Epiblast, of Elasmobranchii, 47 ; Teleostei, 71, 75; Petromyzon, 86; Lcpid


osteus, 112; Amphibia, 122, 125; Chick, 149, 166; Lacerta, 203; Rabbit, 216, 219; origin of in Rabbit, 221 ; comparative account of development of, 300

Epibolic formation of gastrula, 334

Epichordal formation of vertebral column, 556

Epicrium glutinosum, 143

Epidermis, in Ccelenterata, 393; protective structures of, 394

Epididymis, 724

Epigastric vein, 653

Episkeletal muscles, 676

Episternum, 602

Epoophoron, 725

Ethmoid bone, 597

Ethmoid region of skull, 570

Ethmopalatine ligament of Elasmobranchs, 576

Euphausia, eye of, 483

Eustachian tube, of Amphibia, 135; Chick, 1 80; Rabbit, 232; general development of, 528

Excretory organs, general constitution of, 680; of Platyelminthes, 680; of Mollusca, 681; of Polyzoa, 682; of Brachiopoda, 683 ; of Choetopoda, 683 ; of Gephyrea, 686 ; of Discophora, 687 ; of Arthropoda, 688; of Nematoda, 689; of Echinodermata, 689 ; constitution of in Craniata, 689; of Elasmobranchii, 690; constitution of in adult Elasmobranch, 697; of Petromyzon, 700; of Myxine, 701 ; of Teleostei, 701 ; of Ganoidei, 704; of Dipnoi, 707; of Amphibia, 707; of Amniota, 713; comparison of Vertebrate and Invertebrate, 737

Excretory system, of Elasmobranchii, 49 ; Teleostei, 78; Petromyzon, 95, 98; Acipenser, 99; Amphibia, 133

Exoccipital bone, 595

Exoskeleton, dermal, 393 395 ; epidermal, 393396

External generative organs, 726

Extra-branchial skeleton, 572

Eye, of Ascidia, 16; Salpa, 31; Elasmobranchii, 56, 57, 58; Teleostei, 73; Petromyzon, 92, 98; Aves, i/o; Rabbit, 229; general development of, 470; evolution of, 470, 471; simple, 480; compound, 481 ; aconous, 482; pseudoconous, 482 ; of Invertebrata, 471; of Vertebrata, 483 ; comparative development of Vertebrate, 497 ; of Ammoccetes, 497 ; of Tunicata, 507 ; of Chordata, general views on, 508 ; accessory eyes of Fishes, 509; muscles of, 677

Eyelids, development of, 506

Falciform ligament, 757

Falx cerebri, 439

Fasciculi terctes, of Elasmobranchii. 426

Feathers, development of, 396


INDEX.


785


Fenestra rotunda and ovalis, 529

Fertilization, of Amphioxus, 2 ; of Urochorda, 9; Salpa, 29; Elasmobranchii, 46; of Teleostei, 68; Petromyzon, 84 ; Amphibia, 120; Chick, 145 ; Reptilia, 202 ; meaning of, 331

Fifth nerve, development of, 460

Fifth ventricle, 443

Fins, of Elasmobranchii, 62 ; Teleostei, 78; Petromyzon, 94, 95; Acipenser, 109; Lepidosteus, 118; relation of paired to unpaired, 611, 612 ; development of pelvic, 614; development of pectoral, 615; views on nature of paired fins, 616

Fissures of spinal cord, 417

Foetal development, 360 ; secondary variations in, 361

Foot, 618

Foramen of Munro, 430, 438

Foramen ovale, 642

Forebrain, of Elasmobranchii, 55, 59, 60; Petromyzon, 93 ; general development of, 428

Formative cells, of Chick, 154

Fornix, development of, 443

Fornix of Gottsche, 428

Fourth nerve, 464

Frontals, 592

Fronto-nasal process of Chick, 179

Gaertner's canals, 724

Gall-bladder, 770

Ganoidei, development of, 102; relations of, 118; nares of, 534; notochord of, 546 ; vertebral column of, 546, 553 ; ribs of, 561 ; pelvic girdle of, 606; arterial system of, 645 ; excretory organs of, 704; generative ducts of, 734

Gastropoda, eye of, 472

Gastrula, of Amphioxus, 2; of Ascidia, lo; Elasmobranchii, 43, 44 ; Petromyzon, 86; Acipenser, 103; Amphibia, 123; comparative development of, in Invertebrata, 275 ; comparison of Mammalian, 291 ; phylogenetic meaning of, 333 ; ontogeny of (general), 333 ; phylogeny of, 338 343 ; secondary types of, 34!

Geckos, vertebral column of, 557

Generative cells, development of, 74! ; origin of in Ccelenterata, 741 ; of Invertebrata, 743 ; of Vertebrata, 746

Generative ducts, of Teleostei, 704, 735 ; of Ganoids, 704; of Cyclostomata, 733; origin of, 733 ; of Lepidosteus, 735, 750 ; development and evolution of, 748 ; of Ccelenterata, 748 ; of Sagitta, 749 ; of Tunicata, 749 ; Cheetopoda, Gephyrea, etc., 749; of Mollusca, 751; of Discophora, 751 ; of Echinodermata,

75*

Generative system of Elasmobranchii, 51 Gephyrea, nervous system of, 412; excretory organs of, 686 ; generative cells of, 743 ; generative ducts of, 749

B. III.


Germinal disc, of Elasmobranchii, 40; Teleostei, 68 ; Chick, 147

Germinal epithelium, 746

Germinal layers, summary of organs <lrrived from, in Vertebrata, 304 ; historical account of views of, 332 ; homologies of in the Metazoa, 345

Germinal wall of Chick, 152, 159; structure and changes of, 160

Geryonia, auditory organ of, 5 r 5

Gill of Salpa, 31

Giraldes, organ of, 725

Glands, epidermic, development of, 397

Glomerulus, external, of Chick, 716

Glossopharyngeal nerve, development of,

45 6 > 457 Grey matter of spinal cord, 417; of brain,

423 Growth in length of Vertebrate embryo,

306 Guinea-pig, primitive streak of, 223;

notochord of, 226 ; placenta of, 242 ;

development of, 262 Gymnophiona, see ' Ccecilia '

Habenula perforata, 525

Hairs, development of, 396

Halichrerus, placenta of, 250

Hand, 619

Head, comparative account of, 313; segmentation of, 314

Head cavities, of Elasmobranchii, 50 ; Petromyzon, 90, 96; Amphibia, 127; general development of, 676

Head-fold of Chick, 157, 167

Head kidney, see ' Pronephros '

Heart, of Pyrosoma, 25; Elasmobranchii, 50, 58 ; Petromyzon, 94, 97 ; Acipenser, 106; Chick, 170 ; first appearance of in Rabbit, 230; general development of, 633 ; of Fishes, 635, 637 ; of Mammalia, 638; of Birds, 637, 639; meaning of development of, 637 ; of Amphibia, 638 ; of Amniota, 639 ; change of position of, 643

Hind-brain, Elasmobranchii, 55, 59, 60 ; Petromyzon, 93 ; general account of, 424

Hippocampus major, development of, 442

Hirudo, development of blood-vessels of, 633 ; excretory organs of, 688

Horse, placenta of, 253

Hyaloid membrane, 492

Hylodes, oviposition of, 1 21 ; metamorphosis of, -1 37

Hyobranchial cleft, 572

Hyoid arch, of Chick, 179; general account of, 572, 575 ; modifications of, e !73> 577 > f Elasmobranchii, 576; of Teleostei, 577 ; of Amphibia, 582 ; of Sauropsida, 588; of Mammalia,

589

Hyomandibular bar of Elasmobranchii, 576, 577 ; of Teleostei, 579 ; of Amphibia, 582

50


86


INDEX.


Hyomandibular cleft, of Fetromyzon, 91 ; Chick, 179 ; general account of, 572

Hyostylic skulls, 582

Hypoblast of Elasmobranchii, 5! ; Teleostei, 71, 75; Petromyzon, 86; Acipenser, 104; Lepidosteus, 113; Amphibia, 122, 129; Chick, 151, 167 ; Lacerta, 203; Rabbit, 215, 216, 219 ; origin of in Rabbit, 220

Hyposkeletal muscles, 675

Ilyrax, placenta of, 249

Incus, 529, 590

Infraclavicle, 600

Infundibulum of Petromyzon, 92 ; Chick, 175 ; general development of, 430

Insectivora, placenta of, 243

Insects, nervous system of, 410 ; eye of, 481; generative organs of, 745; generative ducts of, 751

Intercalated pieces of vertebral column,

55 1

Interclavicle, homologies of, 602

Intermediate cell-mass of Chick, 183

Intermuscular septa, 672

Interorbital septum, 570

Interrenal bodies, 665

Iris, 489 ; comparative development of,

506

Iris of Ammoccetes, 98 Island of Reil, 444

Jacobson's organ, 537 Jugal bone, 594

Kidney, see ' Metanephros '

Labia majora, development of, 727

Labial cartilages, 597

Labium tympanicum, 525 ; vestibulare,

5 2 5

Lacertilia, general development of, 202 ; nares of, 537 ; pectoral girdle of, 603 ; pelvic girdle of, 607 ; arterial system of, 649

Lacrymal bone, 593

Lacrymal duct, 506

Lacrymal glands, 506

Lremargus, vertebral column of, 548

Lagena, 524

Lamina spiralis, 524

Lamina terminalis, 438

Larva of Amphioxus, 2 ; of Ascidia, 1 5 it ; Teleostei, 81 ; Petromyzon, 89, 95; Lepidosteus, 117, 318; Amphibia, 134, 142; types of, in the Invertebrata, 363

Larvre, nature, origin, and affinities of, 360 386; secondary variations of less likely to be retained, 362 ; ancestral history more fully recorded in, 362 ; secondary variations in development of, 363 ; ontogenetic record of secondary variations in, 361; of freshwater and land animals, 362; types of, 36.2; phosphorescence of, 364; of Coelenterata,


367 ; table of, 365 ; of Invertebrata, 367 et seq.

Larynx, 766

Lateral line sense organs, 538 ; comparison of, with invertebrate, 538 ; development of, in Teleostei, 538 ; development of, in Elasmobranchii, 539

Lateral ventricle, 438 ; anterior cornu of, 440 ; descending cornu of, 440 ; choroicl plexus of, 443

Layers, formation of, in Elasmobrancliii, 41, 56 ; Teleostei, 71 ; Petromyzon, 85 ; Acipenser, 103 ; Lepidosteus, 1 1 1 ; Amphibia, 121; Chick, 150, 152; Lacerta, 202; Rabbit, 215 227; comparison of Mammalia with lower forms, 226, 289; comparison of formation of in Vertebrata, 275; origin and homologies of, in the Metazoa, 331

Leech, see ' Hirudo '

Lemuridre, placenta, 256

Lens, of Elasmobranchii, 57, 58 ; Petromyzon, 94, 99; Acipenser, 106 ; Lepidosteus, 115 ; Amphibia, 127 ; Chick, 177 ; of Vertebrate eyes, 485 ; general account of, 493 ; capsule of, 493 ; comparative development of, 499 ; of Amphibia, Teleostei, Lepidosteus, 499

Lepidosteus, development of, 1 1 1 ; larva of, 117; relations of, 119; spinal nerves of, 455; ribs of, 561 ; generative ducts of, 704, 735 ; swimming-bladder of,

763

Ligamentum pectinatum, 490

Ligamentum suspensorium, 557, 558

Ligamentum vesicse medium, 239

Limbs, of Elasmobranchii, 59 ; Teleostei, 80 ; first appearance of in Chick, 184 ; Rabbit, 232 ; muscles of, 673 ; of Fishes, 609; relation of, to unpaired fins of Fishes, 611, 612; of Amphibia, 61 8

Liver of Teleostei, 78 ; Petromyzon, 95, 96; Acipenser, no; Amphibia 130; general account of, 769

Lizard, development of, 202; general growth of embryo of, 208 ; Mullerian duct of, 721

Lizzia, eye of, 471

Lobi inferiores, 431

Lungs of Amphibia, 137 ; development of, 763 ; homology of, 766

Lymphatic system, 664

Malleus, 529, 591 ; views on, 591 Malpighian bodies, development of accessory in Elasmobranchs, 695 Mammalia, development of, 214; comparison of gastrula of, 291 ; cerebellum of, 427 ; infundibulum of, 431 ; pineal gland of, 434; pituitary body of, 436; cerebrum of, 439 ; spinal nerves of, 449 ; sympathetic of, 466; vertebral column of, 558; branchial arches of, 573, 574; mandibular and hyoid arches of, 589 ; pectoral girdle of, 604; pelvic girdle of,


INDEX.


787


608 ; heart of, 636 ; arterial system of, 647; venous system of, 661 ; muscleplates of, 671 ; mesonephros of, 714; testicular network of, 724 ; urinogenital sinus of, 727 ; spermatozoa of, 747 ; lungs of, 765 ; intestines of, 768 ; liver of> 769; postanal gut of, 774; stomodseum of, 775

Mammary gland, development of, 398 Man, placenta of, 244 ; general account of development of, 265 ; characters of embryo of, 270

Mandibular arch of Elasmobranchii, 62, 576; Petromyzon, 91 ; Acipenser, 106, 116; Chick, 179; general account of,

572, 575; modification of to form jaws,

573, 575; of Teleostei, 580; of Amphibia, 582; Sauropsida, 588; Mammalia, 589

Mandibular bar, evolution of, 311, 321

Manis, placenta of, 256

Marsupial bones, 608

Marsupialia, foetal membranes of, 240 ; cerebellum of, 426 ; corpus callosum of, ' 443 ; uterus of, 726

Maxilla, 594

Meatus auditorius externus, of Chick, 181; development of, 527

Meckelian cartilage, of Elasmobranchii, 576; of Teleostei, 581 ; of Amphibia, 584, 585; of Sauropsida, 588 ; of Mammalia, 590

Mediastinum anterior and posterior, 630

Medulla oblongata, of Chick, 176 ; general development of, 425

Medullary plate of Amphioxus, 4, 5 ; of Ascidia, n; Elasmobranchii, 44, 47, 55; Teleostei, 72; Petromyzon, 88; Acipenser, 104; Lepidosteus, 1 1 1 ; Amphibia, 126, 127, 131; Chick, 159; Lacerta, 204; Rabbit, 223, 227, 228; primitive bilobed character of, 303, 317

Medusae, auditory organs of, 513

Membrana capsulo-pupillaris, 494, 504,

507

Membrana elastica externa, 546

Membrana limitans of retina, 491

Membrana tectoria, 522, 525

Membrane bones, of Amphibia, 582 ; of Sauropsida, 588; of Mammalia, 590; of mandibular arch, 593 ; of pectoral girdle, 599, 602 ; origin of, 592 ; homologies of, 593

Membranous labyrinth, development of in Man, 519

Menobranchus, branchial arches of, 142

Mesenteron of Elasmobranchii, 43 ; Teleostei, 75 ; Petromyzon, 85 ; Acipenser, 104; Amphibia, 123, 124, 129; Chick, 167; general account of, 754

Mesentery, 626, 756

Mesoblast, of Amphioxus, 6 ; Ascidia, 17, 20; Pyrosoma, 24; Salpa, 30; Elasmobranchii, 44, 47; Teleostei, 75; Petromyzon, 86; Acipenser, 105; Lepi


dosteus, 113; Amphibia, 125, 128, 129; of Chick, 154, 167; double origin of in Chick, 154, 158, 159; origin of from lips of blastopore in Chick, 158; of area vasculosa of Chick, iOo; Lacerta, 203; origin of in Rabbit, 218, 223; of area vasculosa in Rabbit, 227; comparative account of formation of, 292 ; discussion of development of in Vertebrata, 297 ; meaning of development of in Amniota, 298; phylogenetic origin of, 346 ; summary of ontogeny of, 349 352 ; views on ontogeny of, 352 360

Mesoblastic somites, of Amphioxus, 6 ; Elasmobranchii, 48, 55 ; Petromyzon, 88 ; Acipenser, 105 ; Lepidosteus, 114; Amphibia, 129, 131; Chick, 161, 1 80; Rabbit, 228; development of in Chordata, 325; meaning of development of, 331; of head, 676

Mesogastrium, 758

Mesonephros, of Teleostei, 78, 702; Petromyzon, 95, 98, 700; Acipenser, 1 10, 705; Amphibia, 134, 708; Chick, 184, 714; general account of, 690 ; development of in Elasmobranchs, 691 ; of Cyclostomata, 700 ; Ganoidei, 705 ; sexual and non-sexual part of in Amphibia, 710; of Amniota, 713, 724; summary and general conclusions as to, 729; relation of to pronephros, 731

Mesopterygium, 616

Metagenesis of Ascidians, 34

Metamorphosis of Amphibia, 137, 140

Metanephros, 690; development of in Elasmobranchii, 697; of Amphibia, 712; of Amniota, 713; of Chick, 722; of Lacertilia, 723; phylogeny of, 736

Metapterygium, 616

Metapterygoid, of Elasmobranchii, 576; of Teleostei, 581

Metazoa, evolution of, 339, 342 ; ancestral form of, 333, 345

Mid-brain, of Elasmobranchii, 55, 58, 59; Petromyzon, 92; general account of development of, 427

Moina, generative organs of, 745

Molgula, development of, 22

Mollusca, nervous system of, 414 ; eyes of, 472; auditory organs of, 515; excretory organs of, 68 1

Monotremata, foetal membranes of, 240 ; cerebellum of, 426; corpus callosum of, 443 ; cerebrum of, 443 ; urinogenital sinus of, 726

Mormyrus, generative ducts of, 704

Mouth, of Amphioxus, 7; of Ascidia, 18; Pyrosoma, 27; Salpa, 31; Elasmobranchii, 57, 60, 61, 62; Petromyzon, 92, 94, 95, 99; Acipenser, 107; Lepidosteus, 118; Amphibia, 129, 132, "134; Rabbit, 231 ; origin of, 317

Mouth, suctorial, of Petromyzon, 99; Acipenser, 107; Lepidosteus, 116, 317; Amphibia, 133, 141, 317


88


INDEX.


Mullerian duct, 690; of Elasmobranchs, 693 ; of Ganoids, 704 ; of Amphibia, 710; of Aves, 717,720; opening of into cloaca, 727; origin of, 733; summary of development of, 733; relation of to pronephros, 733

Muscle-plates, of Amphioxus, 6; Elasmobranchii, 49, 668 ; Teleostei, 670 ; Petromyzon, 94; Chick, 183, 670; general development of, 669 ; of Amphibia, 670; Aves, 670; of Mammalia, 671; origin of muscles from, 672

Muscles, of Ascidia, II, 17; development of from muscle-plates, 672; of limbs, 673 ; of head, 676 ; of branchial arches, 678; of eye, 678

Muscular fibres, epithelial origin of, 667

Muscular system, development of, 667; of Chordata, 668

Mustelus, placenta of, 66

Myoepithelial cells, 667

Mysis, auditory organ of, 517

Myxine, ovum of, loo; olfactory organ of, 533 ; portal sinus of, 652 ; excretory system of, 701

Nails, development of, 397

Nares, of Acipenser, 108; of Ichthyopsida, 534; development of in Chick, 535; development of in Lacertilia, 537; development of in Amphibia, 537

Nasal bones, 592

Nasal pits, Acipenser, 108; Chick, 176; general development of, 531

Nematoda, excretory organs of, 689 ; generative organs of, 745 ; generative ducts of, 752

Nemertines, nervous system of, 311 ; excretory organs of, 68 1

Nerve cord, origin of ventral, 378

Nerves, spinal, 449 ; cranial, 455 466

Nervous system, central, general account of development of in Vertebrata, 415 ; conclusions as to, 445; sympathetic, 466

Nervous system, of Amphioxus, 4; Ascidia, 15, 16; Molgula, 22; Pyrosoma, 24, 25; Salpa, 30, 31; Elasmobranchii, 44; Teleostei, 77 ; Petromyzon, 89, 93; Acipenser, 105; Amphibia, 126; comparative account of formation of central, 301; of Sagitta, 349; origin of in Ccelenterata, 349; of pneoral lobe, 377, 380; evolution of, 400405; development of in Invertebrates, 406; of Arthropoda, 408; of Gephyrea, 412; Mollusca, 414

Neural canal, of Ascidia, 10; Teleostei, 72; Petromyzon, 88; Acipenser, 105; Lepidosteus, 114; Amphibia, 126, 131 ; Chick, 1 66, 171 ; Lacerta, 208; closure of in Frog and Amphioxus, 279; closure of in Elasmobranchii, 284; phylogcuctic origin of, 316

Neural crest, 449, 456, 457


Neurenteric canal, of Amphioxus, 4, 5 ; Ascidia, lo; Elasmobranchii, 54; Petromyzon, 88 ; Acipenser, 105 ; Lepidosteus, 113; Aves, 162; Lacerta, 203, 206; general account of, 323; meaning of, 3 2 3

Newt, ovum of, 120; development of, I2 55 general growth of, 141

Notidanus, vertebral column of, 548; branchial arches of, 572

Notochord of Amphioxus, 6; Ascidia, II, 17; Elasmobranchii, 51; Teleostei, 74; Petromyzon, 86, 94; Acipenser, 104; Lepidosteus, 113; Amphibia, 128, 129; Chick, 157; canal of, in Chick, 163; Lacerta, 204, 205; Guinea-pig, 226; comparative account of formation of, 292, 325; sheath of, 545; later histological changes in, 546; cartilaginous sheath of, 547; in head, 566; absence of in region of trabeculas, 567

Notodelphys, brood-pouch of, 121 ; branchiae of, 140

Nototrema, brood-pouch of, 121

Nucleus pulposus, 559

Oceania, eye of, 471

Occipital bone, 595

CEsophagus, solid, of Elasmobranchii, 61, 759; of Teleostei, 78

Olfactory capsules, 571

Olfactory lobes, development of, 444

Olfactory nerves, Ammoccetes, 99; general development of, 464

Olfactory organ, of aquatic forms, 531; Insects and Crustacea, 531; of Tunicata, 532 ; of Amphioxus, 532 ; of Vertebrata, 533; Petromyzon, 533; of Myxine, 533

Olfactory sacks, of Elasmobranchii, 60; Teleostei, 73; Petromyzon, 92, 97; Acipenser, 106, 108; Lepidosteus, 116; Chick, 176

Oligochreta, excretory organs of, 683

Olivary bodies, 426

Omentum, lesser and greater, 757

Onchidium, eye of, 473

Opercular bones, 593

Operculum, of Teleostei, 77; Acipenser, 107; Lepidosteus, 117, 118; Amphibia,

r 3.5.

Ophidia, development of, 210; arterial system of, 649 ; venous system of, 656

Optic chiasma, 430, 493

Optic cup, retinal part of, 488 ; ciliary portion of, 489

Optic lobes, 428

Optic nerve, development of, 492 ; comparative development of, 500

Optic thalami, development of, 431

Optic vesicle, of Elasmobranchii, 57 59; Teleostei, 74, 499 ; Petromyzon, 89, 92 ; Acipenser, 106; Lepidosteus, 115; Chick, 170; Rabbit, 229; general development of, 429 ; formation of secon


INDKX.


7*9


dary, 487 ; obliteration of cavity of, 488 ; comparative development of, 499; of Lepidosteus and Teleostei, 499. See also ' Eye '

Ora serrata, 488

Orbitosphenoid region of skull, 570

Organs, classification of, 391 ; derivation of from germinal layers, 392

Orycteropus, placenta of, 249

Otic process of Axolotl, 583; of Frog, 585 et seq.

Otoliths, 512

Oviposition, of Amphioxus, i ; Elasmobranchii, 40; Teleostei, 68; Petromyzon, 84; Amphibia, 121; Reptilia, 202

Ovum, of Amphioxus, i; Pyrosoma, 23; Elasmobranchii, 40; Teleostei, 68; Petromyzon, 83 ; Myxine, loo; Acipenser, 102; Lepidosteus, in; Amphibia, 120; Chick, 146; Reptilia, 202 ; Mammalia, 214; of Porifera, 741; migration of in Ccelenterata, 742; Vertebrata, 746

Palatine bone, of Teleostei, 580; origin of, 594

Pancreas, Acipenser, no; general development of, 770

Pancreatic caeca, of Teleostei, etc. 768

Papillae, oral, of Acipenser, 108; Lepidosteus, n6

Parachordals, 565, 566

Parasphenoid bone, 594

Parepididymis, 725

Parietal bones, 592

Paroophorori, 725

Parovarium, 725

Pectoral girdle, 599 ; of Elasmobranchs, 600; of Teleostei, 600; of Amphibia and Amniota, 60 1 ; comparison of with pelvic, 608

Pecten, eye of, 479

Pecten, of Ammoccetes, 498; of Chick, 501 ; Lizard, 501 ; Elasmobranchs, 501

Pedicle, of Axolotl, 484 ; of Frog, 485

Pelobates, branchial apertures of, 136; vertebral column of, 556

Pelodytes, branchial chamber of, 135

Pelvic girdle, 606; of Fishes, 606; Amphibia and Amniota, 607 ; of Lacertilia, 607 ; of Mammalia, 608 ; comparison with pectoral, 608

Penis, development of, 727

Peribranchial cavity, of Amphioxus, 7; of Ascidia, 18; Pyrosoma, 24

Pericardial cavity, of Pyrosoma, 26 ; Elasmobranchii, 49 ; Petromyzon, 94; general account of, 626; of Fishes, 627 ; of Amphibia, Sauropsida and Mammalia, 628

Perichordal formation of vertebral column, 5^6

Perilymph of ear, 523 Periotic capsules, ossifications in, 595, 596


Peripatus, nervous system of, 409 ; eye of 480 ; excretory organs of, 688

Peritoneal membrane, 626

Petromyzon, development of, 83; affinities of, 83, 84; general development of, 87; hatching of, 89; comparison of gastrula of, 280; branchial skeleton of, 312, 572; cerebellum of, 425; pineal gland of, 434 ; pituitary body of, 436 ; cerebrum of, 439; auditory organ of, 517; olfactory organ of, 533; comparison of oral skeleton of with Tadpole, 586; pericardial cavity of, 627; abdominal pores of, 626 ; venous system of, 651 ; excretory organs of, 700; segmental duct of, 700; pronephros of, 700; mesonephros of, 700 ; thyroid body of, 760; postanalgut of, 774; stomodx-um

of, 775

Phosphorescence of larvae, 364

Phylogeny, of the Chordata, 327; of the Metazoa, 384

Pig, placenta of, 251; mandibular and hyoid arches of, 589

Pineal gland, of Petromyzon, 93 ; Chick, 175; general development of, 432; nature of, 432, 434

Pipa, brood-pouch of, 121 ; metamorphosis of, 139; yolk-sack of, 140; vertebral column of, 556

Pituitary body, of Rabbit, 231 ; general development of, 435 ; meaning of, 436 ; Placenta, of Salpa, 29; Elasmobranchii, 66; of Mammalia, 232; villi of, 235 ; deciduate and non-deciduate, 239; comparative account of, 239 259 ; characters of primitive type of, 240; zonary, 248; non-deciduate, 250; histology of, 257; evolution of, 259

Placoid scales, 395

Planorbis, excretory organs of, 68 1

Planula, structure of, 367

Pleural cavities, 631

Pleuronectidae, development of, 80

Pneumatoccela, characters of, 327

Polygordius, excretory organs of, 684

Polyophthalmus, eye of, 479

Polypedates, brood-pouch of, 121

Polyzoa, excretory organs of, 682 ; generative cells of, 745 ; generative ducts

of, 751

Pons Varolii, 426, 427

Pori abdominales, Ammoccetes, 99

Porifera, ancestral form of, 345 ; development of generative cells of, 74!

Portal vein, 653

Postanal gut of Elasmobranchii, 58, 59, 60; Teleostei, 75; Chick, 169; general account of, 323, 772

Prsemaxilla, 594

Praeopercular bone, 593

Prrcoral lobe, ganglion of, 377, 380

Prefrontals, 597

Presphenoid region of skull, 570

Primitive groove of Chick, 1 55


790


INDEX.


Primitive streak, of Chick, 152, 161; meaning of, 153; origin of mesoblast form in Chick, 154; continuity of hypoblast with epiblast at anterior end of, in Chick, 156; comparison of with blastopore, 165 ; fate of, in Chick, 165 ; of Lacerta, 203; of Rabbit, 221; of Guinea-pig, 223 ; fusion of layers at, in Rabbit, 224; comparison of with blastopore of lower forms, 226, 287 ; of Mammalia, 290

Processus falciformis of Ammoccetes, 498 ; of Elasmobranch, 502 ; of Teleostei , 503 Proctodseum, 778

Pronephros, of Teleostei, 78, 701 ; Petromyzon, 95, 99, 700; Acipenser, 106, no; Amphibia, 134, 707; general account of, 689 ; of Cyclostomata, 700 ; of Myxine, 701 ; Ganoidei, 705 ; of Amniota, 714; of Chick, 718; summary of and general conclusions as to, 728; relation of, to mesonephros, 731 ; cause of atrophy of, 729 Prootic, 596, 597 Propterygium, 616 Proteus, branchial arches of, 142 Protochordata, characters of, 327 Protoganoidei, characters of, 328 Protognathostomata, characters of, 328 Protopentadactyloidei, characters of, 329 Protovertebrata, characters of, 328 Pseudis, Tadpole of, 139; vertebral

column of, 556

Pseud ophryne, yolk-sack of, 140; Tadpole of, 140 Pterygoid bone, of Teleostei, 581; origin

of, 597

Pterygoquadrate bar, of Elasmobranchii, 576; of Teleostei, 581; Axolotl, 584; F r g, 584; ofSauropsida, 588; of Mammalia, 589

Pulmonary artery, origin of, 645 ; of Amphibia, 645 ; of Amniota, 649

Pulmonary vein, 655

Pupil, 489

Pyrosoma, development of, 23

Quadrate bone of Teleostei, 581 ; of Axolotl, 584; Frog, 585; Sauropsida, 588

Quadratojugal bone, 594

Rabbit, development of, 214; general growth of embryo of, 227 ; placenta of, 248

Radiate symmetry, passage from to bilateral symmetry, 373 376

Raja, caudal vertebras of, 553

Rat, placenta of, 242

Recessus labyrinthi, 519

Reissner's membrane, 524

Reptilia, development of, 202; viviparous, 202; cerebellum of, 426; infundibulum of, 431; pituitary body of, 436; cerebrum of, 439; vertebral column of,


556; arterial system of, 648; venous system of, 656; mesonephros of, 713; testicular network of, 723; spermatozoa of, 747

Restiform tracts of Elasmobranchii and Teleostei, 425

Retina, histogenesis of, 490

Retinulse, 482

Rhabdom, 482

Rhinoderma, brood-pouch of, 121; metamorphosis of, 1 39

Ribs, development of, 560

Roseniniiller's organ, 725

Rotifera, excretory organs of, 680

Round ligament of liver, 663

Ruminantia, placenta of, 253

Sacci vasculosi, 437

Sacculus hemisphericus, 519; of Mammals, 519, 520

Sagitta. See ' Chaetognatha'

Salpa, sexual development of, 29; asexual development of, 33

Salamandra, larva of, 142; vertebral column of, 553; limbs of, 619; mesonephros of, 708; Miillerian duct of, 710

Salmonidse, hypoblast of, 71; generative ducts of, 704

Sauropsida, gastrula of, 286; meaning of primitive streak of, 288; blastopore of, 289 ; mandibular and hyoid arches of, 588 ; pectoral girdle of, 60 1

Scala, vestibuli, 522; tympani, 523; media, 522

Scales, general development of, 396 ; development of placoid scales, 395

Scapula, 599

Sclerotic, 488

Scrotum, development of, 727

Scyllium, caudal vertebrse of, 553; mandibular and hyoid arches of, 578; pectoral girdle of, 600; limbs of, 610; pelvic fin of, 614; pectoral fin of, 615

Segmental duct, 690 ; development of in Elasmobranchs, 690; of Cyclostomata, 700; of Teleostei, 701; of Ganoidei, 704, 705 ; of Amphibia, 707 ; of Amniota, 713

Segmental organs, 682

Segmental tubes, 690 ; development of in Elasmobranchs, 691 ; rudimentary anterior in Elasmobranchs, 693 ; development of secondary, 731

Segmentation cavity, of Elasmobranchii, 42 44; Teleostei, 69, 85, 86; Amphibia, 122, 125

Segmentation, meaning of, 331

Segmentation of ovum, in Amphioxus, 2 ; Ascidia, 9 ; Molgula, 22 ; Pyrosoma, 23; Salpa, 30; Elasmobranchii, 40; Telostei, 69; Petromyzon, 84; Acipenser, IOT, Lcpidosteus, in; Amphibia, 122, 124; Newt, 125; Chick, 146; Lizard, 202: Rabbit, 214


INDEX.


791


Semicircular canals, 519

Sense organs, comparative account of development of, 304

Septum lucidum, 443

Serous membrane, Lacerta, 209; of Rabbit, 237

Seventh nerve, development of, 459

Shell-gland of Crustacea, 689

Shield, embryonic, of Chick, 151 ; of Lacerta, 202

SimiadiK, placenta of, 247

Sinus rhomboidalis, of Chick, 162

Sinus venosus, 637

Sirenia, placenta of, 255

Sixth nerve, 463

Skate, mandibular and hyoid arches of,

577

Skeleton, elements of found in Vertebrata, 542

Skull, general development of, 564 ; historical account of, 564 ; development of cartilaginous, 566; cartilaginous walls of, 570; composition of primitive cartilaginous cranium, 565

Somatopleure, of Chick, 170

Spelerpes, branchial arches of, 142

Spermatozoa, of Porifera, 741; of Vertebrata, 746

Sphenoid bone, 595

Sphenodon, hyoid arch of, 588

Spinal cord, general account of, 415; white matter of, 415; central canal of, 417, 418; commissures of, 417; grey matter of, 417; fissures of, 418

Spinal nerves, posterior roots of, 449; anterior roots of, 453

Spiracle, of Elasmobranchii, 62 ; Acipenser, 105; Amphibia, 136

Spiral valve. See 'Valve'

Spleen, 664

Splenial bone, 595

Squamosal bone, 593

Stapes, 529; of Mammal, 590

Sternum, development of, 562

Stolon of Doliolum, 29 ; Salpa, 33

Stomodaeum, 774

Stria vascularis, 524

Styloid process, 591

Sub-intestinal vein, 65 1 ; meaning of,

651

Syngnathus, brood-pouch of, 68 Subnotochordal rod, of Elasmobranchii,

54; Petromyzon, 94; Acipenser, no;

Lepidosteus, 115; general account of,

754; comparison of with siphon of

Chsetopods, 756

Subzonal membrane, 237; villi of, 236 Sulcus of Munro, 432 Supraclavicle, 600 Suprarenal bodies, 664 Supra-temporal bone, 593 Swimming bladder, see Air bladder Sylvian aqueduct, 428 Sylvian fissure, 444 Sympathetic ganglia, development of, 467


Tadpole, 134, 139, 140; phylogenetic meaning of, 137; metamorphosis of, 137; m can ing of suctorial mouth of, 585

Tail of Teleostei, 80; Acipenser, 109; Lepidosteus, 109; Amphibia, 132

Tarsus, development of, 620

Teeth, horny provisional, of Amphibia, 136; general development of, 776; origin of, 777

Teleostei, development of, 68; viviparous, 68; comparison of formation of layers in, 286; restiform tracts of, 425 ; mid-brain of, 425 ; infundibulum of, 431 ; cerebrum of, 439; nares of, 534; lateral line of, 538; notochord and membrana elastica of, 549 ; vertebral column of, 553; ribs of, 561; hyoid and mandibular arches of, 579; pectoral girdle of, 601 : pelvic girdle of, 606; limbs of, 618; heart of, 637; arterial system of, 645; muscle-plates of, 670; excretory organs of, 701 ; generative ducts of, 704, 735, 749; swimming bladder of, 763 ; postanal gut of,

Teredo, nervous system of, 414

Test of Ascidia, 14; Salpa, 31

Testicular network, of Elasmobranchs, 697 ; of Amphibia, 712 ; Reptilia, 723 ; of Mammals, 724

Testis of Vertebrata, 746

Testis, connection of with Wolffian body, in Elasmobranchii, 697; in Amphibia, 710; in Amniota, 723; origin of, 735

Thalamencephalon of Chick, 175; general development of, 430

Third nerve, development of, 461

Thymus gland, 762

Thyroid gland, Petromyzon, 92 ; general account of, 759; nature of, 760; development of in Vertebrata, 761

Tooth. See 1 Teeth'

Tori semicirculares, 428

Tornaria, 372

Trabeculas, 565, 567; nature of, 568

Trachea, 766

Trematoda, excretory organs of, 68 1

Triton alpestris, sexual larva of, 143

Triton, development of limbs of, 619} urinogenital organs of, 7 12

Truncus arteriosus, 638; of Amphibia, 638; of Birds, 639

Turiicata, development of mesoblast of, 293; test of, 394; eye of, 507; auditory organ of, 530; olfactory organ of, 532; generative duct of, 749 ; intestine of, 767; postanal gut of, 771; stomodseum of, 775

Turbellaria, excretory organs of, 68 1

Tympanic annulus of *'rog, 587

Tympanic cavity, of Amphibia, 135; Chick, 1 80; Rabbit, 232; general development of, 528; of Mammals, 591

Tympanic membrane, of Chick, 180; general development of, 528


792


INDEX.


Tympanohyal, 591

Umbilical canal of Elasmobranchii, 54,

57, 58, 59

Umbilical cord, 238; vessels of, 239

Ungulata, placenta of, 250

Urachus, 239, 726

Ureters, of Elasmobranchii, 696; development of, 723

Urethra, 727

Urinary bladder of Amphibia, "Jii; of Amniota, 726

Urinogenital organs, see Excretory organs

Urinogenital sinus of Petromyzon, 700; of Sauropsida, 726; of Mammalia, 727

Urochorda, development of, 9

Uterus, development of, 726; of Marsupials, 726

Uterus masculinus, 726

Utriculus, 519

Uvea of iris, 489

Vagus nerve, development of, 456, 457; intestinal branch of, 458; branch of to lateral line, 459

Valve, spiral, of Petromyzon, 97; Acipenser, no; general account of, 767

Valves, semilunar, 641; auriculo-ventricular, 642

Vasa efferentia, of Elasmobranchs, 697 ; of Amphibia, 711; general origin of, 724

Vascular system, of Amphioxus, 8; Petromyzon, 97; Lepidosteus, 116; general development of, 632

Vas deferens, of Elasmobranchii, 697 ; of Amniota, 723

Vein, sub-intestinal of Petromyzon, 97 ; Acipenser, no; Lepidosteus, 116

Velum of Petromyzon, 9 1

Vena cava inferior, development of, 655

Venous system of Petromyzon, 97; general development of, 651; of Fishes, 651 ; of Amphibia and Amniota, 655 ; of Reptilia, 656; of Ophidia, 656; of Aves, 658; of Mammalia, 661

Ventricle, fourth, of Chick, 176; history of, 424

Ventricle, lateral, 438, 440; fifth, 443

Ventricle, third, of Chick, 175

Vertebral bodies, of Chick, 183

Vertebral column, development of, 545, 549; epichordal and perichordal development of in Amphibia, 556

Vespertilionidse, early development of, 217

Vieussens, valve of, 426

Villi, placental, of zona radiata, 235 ; subzonal membrane, 235; chorion, 237;


Man, 246; comparative account of, 2 575 of young human ovum, 265, 269

Visceral arches, Amphioxus, 7 ; Elasmobranchii, 57 60; Teleostei, 77; Acipenser, 1 06; Lepidosteus, 116; Amphibia, 133; Chick, 177; Rabbit, 231; prseoral, 570; relation of to head cavities, 572; disappearance of posterior, 573; dental plates of in Teleostei, 574

Visual organs, evolution of, 470

Vitelline arteries of Chick, 195

Vitelline veins of Chick, 195

Vitreous humour, of Ammoccetes, 98 ; general development of, 494; blood* vessels of in Mammals, 503 ; mesoblastic ingrowth in Mammals, 503

Vomer, 594

White matter, of spinal cord, 415; of brain, 423

Wolffian body, see ' Mesonephros '

Wolffian duct, first appearance of in Chick, 183; general account of, 690; of Elasmobranchs, 693 ; of Ganoids, 704; of Amphibia, 710; of Amniota, 713; atrophy of in Amniota, 724

Wolffian ridge, 185

Yolk blastopore, of Elasmobranchii, 64

Yolk, folding off of embryo from, in Elasmobranchii, 55; in Teleostei, 76; Acipenser, 106; Chick, 168, 170

Yolk nuclei, of Elasmobranchii, 41, 53; Teleostei, 69, 75

Yolk, of Elasmobranchii, 40; Teleostei, 68; Petromyzon, 96; Acipenser, 109; Amphibia, 122, 129; Chick, 146; influence of on formation of layers, 278; influence of on early development,

341, 342

Yolk-sack, Amphibia, 131, 140, 141; enclosure of, 123

.Yolk-sack, development of in Rabbit, 227; of Mammalia reduced, 227; circulation of in Rabbit, 233 ; enclosure of in Sauropsida, 289

Yolk-sack, enclosure of, Petromyzon, 86

Yolk-sack, Lepidosteus, 118

Yolk-sack of Chick, enclosure of, 160; stalk of, 174; general account of, 193; circulation of, 195 ; later history of, 198

Yolk-sack of Elasmobranchii, enclosure of, 62, 283; circulation of, 64

Yolk-sack of Lacerta, 209 ; circulation of, 209

Yolk-sack, Teleostei, 75, 81; enclosure of, 75 ; circulation of, 81

Zona radiata, villi of, 237 Zonula of Zinn, 495


BIBLIOGRAPHY.


CEPHALOPODA.

(1) A. Kowalevsky. " Entwicklungsgeschichte des Amphioxus lanceolatus." Mem. Acad. Imper. des Sciences de St Pttersbourg, Series vn. Tom. XI. 1867.

(2) A. Kowalevsky. "Weitere Studien iiber die Entwicklungsgeschichte des Amphioxus lanceolatus." Archiv f. mikr. Anat., Vol. xui. 1877.

(3) Leuckart u. Pagenstecher. " Untersuchungen tiber niedere Seethiere." Mutter's Archiv, 1858.

(4) Max Schultze. " Beobachtung junger Exemplare von Amphioxus." Zeit. f. wiss. Zool., Bd. in. 1851.

(5) A. M. Marshall. "On the mode of Ovi position of Amphioxus." your, of Anat. and Phys., Vol. x. 1876.

UROCHORDA.

(6) P. J. van Beneden. " Recherches s. 1'Embryogenie, 1'Anat. et la Physiol. des Ascidies simples." Mem. Acad. Roy. de Belgique, Tom. xx.

(7) W. K. Brooks. "On the development of Salpa." Bull, of the Museum of Comp. Anat. at Harvard College, Cambridge, Mass.

(8) H. Fol. Eludes surles Appendiculaires du detroit de Mcssine . Geneve et Bale, 1872.

(9) Ganin. "Neue Thatsachen a. d. Entwicklungsgeschichte d. Ascidien." Zeit.f. wiss. Zool., Vol. XX. 1870.

(10) C. Gegenbaur. " Ueber den Entwicklungscyclus von Doliolum nebst Bemerkungen iiber die Larven dieser Thiere." Zeit.f. wiss. Zool., Bd. vu. 1856.

(11) A. Giard. "Etudes critiques des travaux d'embryogenie relatifs a la parente des Vertebres et des Tuniciers." Archiv Zool. experiment., Vol. I. 1872.

(12) A. Giard. " Recherches sur les Synascidies. " Archiv Zool. exper., Vol. I. 1872.

(13) O. Hertwig. "Untersuchungen lib. d. Bau u. d. Entwicklung des Cellulose-Mantels d. Tunicaten." Jenaische Zeitschrift, Bd. vn. 1873.

(14) Th. H. Huxley. " Remarks upon Appendicularia and Doliolum. " Phil. Trans., 1851.

(15) Th. H.Huxley. " Observations on the anatomy and physiology of Salpa and Pyrosoma." Phil. Trans., 1851.

(16) Th. H. Huxley. "Anatomy and development of Pyrosoma." Linnean Trans., 1860, Vol. XXIII.

(17) Keferstein u. Ehlers. Zoologische Beitrage, 1861. Doliolum.

(18) A. Kowalevsky. "Entwicklungsgeschichte d. einfachen Ascidien." Mem. Acad. Pctersbourg, VII. serie, T. x. 1866.

(19) A. Kowalevsky. "Beitrag z. Entwick. d. Tunicaten." Nachrichtcn d. konigl. Gesell.zu Gottingen. 1868.

(20) A. Kowalevsky. "Weitere Studien iib. d. Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. vn. 1871.

(21) A. Kowalevsky. "Ueber Knospung d. Ascidien." Archiv f. mikr. Anat., Vol. X. 1874.

(22) A. Kowalevsky. "Ueber die Entwicklungsgeschichte d. Pyrosoma." Archiv f. mikr. Anat., Vol. xi. 1875.

(23) A. Krohn. "Ueber die Gattung Doliolum u. ihre Arten." Archiv f. Natnrgeschichte, Bd. xvm. 1852.

B. Hi. a


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(24) A. Krohn. "Ueber die Entwicklung d. Ascidien." Mailer's Archiv, 1852.

(25) A. Krohn. "Ueber die Fortpfianzungsverhaltnisse d. Botrylliden. " Archiv f. Naturgeschichte, Vol. xxxv. 1869.

(26) A. Krohn. "Ueber die fruheste Bildung d. Botryllenstocke." Archiv f. Naturgeschichte, Vol. xxxv. 1869.

(27) C. Kupffer. " Die Stammverwandschaft zwischen Ascidien u. Wirbelthieren." Archiv f, mikr. Anat., Vol. vi. 1870.

(28) C. Kupffer. "Zur Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. vm. 187-2.

(29) H. Lacaze Duthiers. "Recherches sur 1'organisation et 1'Embryogenie des Ascidies (Molgula tubulosa)." Comptes rendus, May 30, 1870, p. 1154.

(30) H. Lacaze Duthiers. "Les Ascidies simples des Cotes de France" (Development of Molgula). Archiv Zool. exper., Vol. ill. 1874.

(31) R. Leuckart. "Salpa u. Verwandte." Zoologischc Untcrsuchungen, Heft u.

(32) E. Metschnikoff. " Observations sur le developpement de quelques animaux (Botryllus and Simple Ascidians)." Still, d. fAcad. Petersbottrg, Vol. xm. 1869.

(33) H. Milne-Edwards. "Observations s. 1. Ascidies composees des cotes de la Manche." Memoir es d. V Instittit, T. xvm. 1842.

(34) W. Salensky. "Ueber d.embryonaleEntwicklungsgeschichtederSalpen." Zeit.f. wiss. Zool., B. xxvn. 1877.

(35) W. Salensky. "Ueber die Knospung d. Salpen." Morphol. Jahrbuch, Bd. in. 1877.

(36) W. Salensky. "Ueber die Entwicklung d. Hoden u. iiber den Generationswechsel d. Salpen." Zeit.f. wiss. Zool., Bd. xxx. Suppl. 1878.

(37) C. Semper. " Ueber die Entstehung d. geschichteten Cellulose-Epidermis d. Ascidien." Arbeit, a. d. zool.-zoot. Instit. Wiirzburg, Vol. ri. 1875.

(38) Fr. Todaro. Sopra lo sviluppo e F anatomia delle Salpc. Roma, 1875.

(39) Fr. Todaro. "Sui primi fenomeni dello sviluppo delle Salpe." Realc Accadcmia dci Lincei, Vol. iv. 1880.


ELASMOBRANCHII.

(40) F. M. Balfour. " A preliminary account of the development of the Elasmobranch Fishes." Quart. J. of Micr. Science, Vol. xiv. 1876.

(41) F. M. Balfour. "A Monograph on the development of Elasmob ranch Fishes." London, 1878. Reprinted from the Journal of Anat. and Fhysiol. for 1876, 1877, and 1878.

(42) Z. Gerbe. " Recherches sur la segmentation de la cicatrule et la formation des prodnits adventifs de Pceuf des Plagiostomes et particulierement des Rates." Vide also Journal de FAnatomie et de la Physiologic, 1872.

(43) W. His. " Ueb. d. Bildung v. Haifischenembryonen." Zeit. fur Anat. u. Entwick., Vol. 11. 1877.

(44) A. Kowalevsky. "Development of Acanthias vulgaris and Mustelus Irevis. " (Russian.) Transactions of the Kiew Society of Naturalists, Vol. I. 1870.

(45) R. Leuckart. "Ueber die allmahlige Bildung d. Korpergestalt bei d. Rochen." Zeit. f. wiss. Zool., Bd. II., p. 258.

(46) Fr. Ley dig. Rochen u. Hate. Leipzig, 1852.

(47) A. W. Malm. " Bidrag till kannedom om utvecklingen af Rajae." Kongl. vetenskaps akademiens fo'rhandlingar. Stockholm, 1876.

(48) Joh. M tiller. Clatter Haie des Aristoteles und iiber die Verschiedenheitcn unler den Haifachen und Rochen in der Entivicklung des Eies. Berlin, 1840.

(49) S. L. Schenk. " Die Eier von Raja quadrimaculata innerhalb der Eileiter." Sitz. der k. Akad. Wien, Vol. LXXIII. 1873.

(50) Alex. Schultz. " Zur Entwicklungsgeschichte des Selachiereies. " Archiv fiir micro. Anat., Vol. XI. 1875.

(51) Alex. Schultz. " Beitrag zur Entwicklungsgeschichte d. Knorpelfische. " Archiv fiir micro. Anat., Vol. xni. 1877.


BIBLIOGRAPHY.


Ill


(52) C. Semper. "Die Stammesverwandschaft d. Wirbelthiere u. Wirlwllosen. Arbeit, a. d. zool.-zoot. Instit. Wiirzburg, Vol. II. 1875.

(53) C. Semper. " Das Urogenitalsystem d. Plagiostomen, etc." Arbeit, a. d. zool.-zoot. Instit. Wiirzburg, Vol. n. 1875.

(54) Wyman. " Observations on the Development of Raja batis." Memoirs of the American Academy of Arts and Sciences, Vol. ix. 1864.


TELEOSTEI.

(55) Al. Agassiz. " On the young Stages of some Osseous Fishes. I. Development of the Tail." Proceedings of the American Academy of Arts and Sciences, Vol. xin. Presented Oct. n, 1877.

(56) Al. Agassiz. "II. Development of the Flounders." Proceedings of the American Acad. of Arts arid Sciences, Vol. xiv. Presented June, 1878.

(57) K. E. v. Baer. Untersuchungen ilber die Entwicklungsgeschichte der Fische. Leipzig, 1835.

(58) Ch. van Bambeke. "Premiers effets de la fecondation sur les cufs de Poissons: sur 1'origine et la signification du feuillet muqueux on glandulaire chez les Poissons Osseux." Comptes Rendus des Seances de f Academic des Sciences, Tome

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LXXIV.

(59)

Osseux. ' Vol. XL.

(60)


E. v. Beneden. "A contribution to the history of the Embryonic development of the Teleosteans." Quart. J. of Micr. Sci., Vol. xvm. 1878.

(61) E. Calberla. " Zur Entwicklung des Medullarrohres u. d. Chorda dorsalis d. Teleostier u. d. Petromyzonten." Morphologisches Jahrbuch, Vol. III. 1877.

(62) A. Gotte. "Beitrage zur Entwicklungsgeschichte der Wirbelthiere." Archiv f. mikr. Anat., Vol. IX. 1873.

(63) A. Gotte. " Ueber d. Entwicklung d. Central-Nervensystems der Teleostier." Archiv f. mikr. Anat., Vol. xv. 1878.

(64) A. Gotte. " Entwick. d. Teleostierkeime." Zoologischer Anzeiger, No. 3. 1878.

(65) W. His. " Untersuchungen Uber die Entwicklung von Knochenfischen, etc." Zeit.f. Anat. it. Entwicklungsgeschichte, Vol. I. 1876.

(66) W. His. "Untersuchungen Uber die Bildung des Knochenfischembryo (Salmen)." Archiv f. Anat. u. Physiol., 1878.

(67) E. Klein. "Observations on the early Development of the Common 'Trout." Quart. J. of Micr. Science, Vol. XVI. 1876.

~^* (68) C. Kupffer. " Beobachtungen Uber die Entwicklung der Knochenfische." Archiv f. mikr. Anat., Bd. iv. 1868.

(69) C. Kupffer. Ueber Laichen u. Entwicklung des Ostsee-Herings. Berlin, 1878.

(70) M. Lereboullet. "Recherches sur le developpement du brochet de la perche et de 1'ecrevisse." Annales des Sciences Nat., Vol. I., Series iv. 1854.

(71) M. Lereboullet. " Recherches d'Embryologie comparee sur le developpement de la Truite." An. Sci. Nat., quatrieme serie, Vol. XVI. 1861.

(72) T. Oellacher. " Beitrage zur Entwicklungsgeschichte der Knochenfische nach Beobachtungen am Bachforellenei." Zeit. f. wiss. Zool., Vol. xxn., 1872, and' Vol. xxni., 1873.

(72*) H. Rathke. Abh. z. Bildung u. Entwick. d. Menschen u. Thiere. Leipzig, 1832-3. Part n. Blennius.

(73) Reineck. " Ueber die Schichtung des Forellenkeims." Archiv f. mikr. Anat., Bd. V. 1869.

(74) S. Strieker. "Untersuchungen Uber die Entwicklung der Bachforelle." Sitzungsberichte der Wiener k. Akad. d. Wiss., 1865. Vol. LI. Abth. 2.

(75) Carl Vogt. " Embryologie des Salmones." Histoire Naturelle des Poissons de F Europe Centrale. L. Agassiz. 1842.

(76) C.Weil. " Beitrage zur Kenntniss der Knochenfische." Silzungsbcr. doWiener kais. Akad. der Wiss., Bd. i.xvi. 1872.

a 2


BIBLIOGRAPHY.


CYCLOSTOMATA.

(77) E. Calberla. " Der Befruchtungsvorgang beim Petromyzon Planeri." Zeit.f. iviss. Zool., Vol. xxx. 1877.

(78) E. Calberla. "Ueb. d. Entwicklung d. Medullarrohres u. d. Chorda clorsalis d. Teleostier u. d. Petromyzonten." Morpholog. Jahrbuch, Vol. in. 1877.

(79) C. Kupffer u. B. Benecke. Der Vorgang d. Befruchtimg am Ei d. Neunaugen. Konigsberg, 1878.

(80) Aug. Muller. " Ueber die Entwicklung d. Neunaugen." Miiller s Archiv, 1856.

(81) Aug. Muller. Beobachtungen iib. d. Befruchtungserscheinungen im Ei d. Neunaugen. Konigsberg, 1864.

(82) W. Muller. "Das Urogenitalsystem d. Amphioxus u. d. Cyclostomen. ' Jcnaische Zeitschrift, Vol. IX. 1875.

(83) Ph. Owsjannikoff. "Die Entwick. von d. Flussneunaugen. " ^ Vorlauf. Mittheilung. Melanges Biologiqttcs tires du Bulletin de VAcad. Imp. St Pttersbourg, Vol. vn. 1870.

(84) Ph. Owsjannikoff. On the development of Petromyzon fiuviatihs (Russian).

(85) Anton Schneider. Beitrdge z. vergleich. Anat. a. Entwick. d. Wirbelthiere. Quarto. Berlin, 1879.

(86) M. S. Schultze. "Die Entwickl. v. Petromyzon Planeri." Gekronte Preisschrift. Haarlem, 1856.

(87) W. B. Scott. " Vorlaufige Mittheilung iib. d. Entwicklungsgeschichte d. Petromyzonten." Zoologischer Anzeiger, Nos. 63 and 64. ill. Jahrg. 1880.

GANOIDEI. A cipenseridce.

(88) Knock. "Die Beschr. d. Reise z. Wolga Behufs d. Sterlettbefruchtung. " Bull. Soc. Nat. Moscow, 1871.

(89) A. Kowalevsky, Ph. Owsjannikoff, and N. Wagner. "Die Entwick. d. Store." Vorlauf. Mittheilung. Melanges Biologizes tires du Bulletin d. VAcad. Imp. St Petersbowg, Vol. VII. 1870.

(90) W. Salensky. "Development of the Sterlet (Acipenser ruthenus)." 2 Parts. Proceedings of the Society of Naturalists in the imperial University of Kasan. 1878 and 9 (Russian). Part I., abstracted in Hoffmann and Schwalbe's Jahresbcricht for 1878.

(91) W. Salensky. " Zur Embryologie d. Ganoiden (Acipenser)." Zoologischer Anzeiger, Vol. I., Nos. n, 12, 13.

Lepidosteidce.

(92) Al. Agassiz. "The development of Lepidosteus." Proc. Amer. Acad. of Arts and Sciences, Vol. xm. 1878.

AMPHIBIA.

(93) Ch. van Bambeke. " Recherches sur le developpement du Pelobate brun." Mc/noires coitronncs, etc. de I 1 Acad. roy. de Belgique, 1868.

(94) Ch. van Bambeke. "Recherches sur 1'embryologie des Batraciens." /!iill,-tin dc V Acad. roy. de Belgique, 1875.

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AVES.

(117) K. E. vonBaer. " Ueb. Entwickhmgsgeschichte d. Thiere." Konigsberg, 18281837.

(118) F. M. Balfour. "The development and growth of the layers of the Blastoderm," and "On the disappearance of the Primitive Groove in the Embryo Chick." Quart. J. of Micros. Science, Vol. xin. 1873.

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(120) M. Braun. "Aus d. Entwick. d. Papageien; I. Riickenmark ; II. Entwicklung d. Mesoderms; III. Die Verbindungen zwischen Riickenmark u. Darm bei Vogeln." Verh. d. phys.-med. Ges. zu Wurzbtirg. N. F. Bd. XIV. and xv. 1879 and 1880.

(121) J. Disse. " Die Entwicklung des mittleren Keimblattes im Htirmerei. Archiv fur mikr. Anat., Vol. xv. 1878.

(122) J. Disse. "Die Entstehung d. Blutes u. d. ersten Gefasse im Hiihnerei.' Archiv f. mikr. Anat., Vol. xvi. 1879.

(123) Fr. Durante. "Sulla struttura della macula germinativa delle uova di Gallina." Ricerche nel Laboratorio di Anatomia della R. Universita di Roma.

(124) E. Dursy. Der Primitivstreif des Hiihnchens. 1867.

(125) M. Duval. "Etude sur la ligne primitive de 1'embryon de Poulet. Annales des Sciences Naturelles, Vol. vn. 1879.

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(127) Gasser. "Der Primitivstreifen bei Vogelembryonen." Schrifteti d. Gescll. zur Befbrd. d. gesammten Naturwiss. zu Marburg, Vol. II. Supplement l. 1879.

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(131) W. His. Unsere Kbrperform tmd das physiol. Problem ihrer Entstehung. Leipzig, 1875.

(132) W. His. "Der Keimwall des Hiihnereies u. d. Entstehung d. parablastischen Zellen." Zeit.f. Anat.u. Entwicklungsgeschichte. Bd. I. 1876.

(133) W. His. " Neue Untersuchungen iib. die Bildung des Hiihnerembryo I." Archiv f. Anat. u. Phys. 1877.

(134) E. Klein. "Das mittlere Keimblatt in seiner Bezieh. z. Entwick. d. ers. Blutgefiisse und Blutkorp. im Hiihnerembryo." Sitzungsber. Wien. Akad., Vol. LXIII. 1871.

(135) A. K6 Hiker. Entwicklungsgeschichte d. Menschen u. d. hbheren 7'hii'rc. Leipzig, 1879.

(136) C. Kupffer. " Die Entsteh. d. Allantois u. d. Gastrula d. Wirbelth." Zoolog. Anzeiger, Vol. II. 1879, PP- 5 2O > 593> 612.

(137) C. Kupffer and B. Benecke. " Photogramme z. Ontogenie d. Vogel." Nov. Act. d. k. Leop.-Carol.-Deutschen Akad. d. Naturforscher, Vol. XLI. 1879.

(138) J. Oellacher. "Untersuchungen tiber die Furchung u. Blatterbildung im Hiihnerei." Strieker's Studien. 1870.

(139) C. H. Pander. Beitrage z. Entwick. d. Hiinchens im Eie. Wiirzburg, 1817.

(140) A. Rauber. " Ueber die Etnbryonalanlage des Hiihnchens." Centralblatt fur d. medic. Wissenschaften. 1874 75.

(141) A. Rauber. Ueber die Stellung des Hiihnchens im Entwickhingsplan. 1876.

(142) A. Rauber. " Primitivrinne und Urmund. Beitrage zur Entwicklungsgeschichte des Hiihnchens." Morphol. Jahrbuch, B. II. 1876.

(143) A. Rauber. Primitivslreifen und Neurula der Wirbelthiere in normalcr und pathologischer Beziehung. 1877.

(144) R. Remak. Untersuch. iib. d. Entwicklung d. Wirbelthiere. Berlin, 185055.

(145) S. L. Schenk. "Beitrage z. Lehre v. d. Organanlage im motorischen Keimblatt. Sitz. Wien. Akad., Vol. LVII. 1860.

(146) S. L. Schenk. " Beitrage z. Lehre v. Amnion." Archiv f. mikr. Anat., Vol. vii. 1871.

(147) S. L. Schenk. Lehrbuch d. vergleich. Embryol. d. Wirbelthiere. Wien, 1874.

(148) S. Strieker. " Mittheil. iib. d. selbststiindigen Bewegungen embryonaler Zellen." Sitz. Wien. Akad., Vol. XLIX. 1864.

(149) S. Strieker. "Beitrage zur Kenntniss des Hiihnereies." Wiener Sitzungsber., Vol. LIV. 1866.

(150) H. Virchow. Ueber d. Epithel d. Dottersackes im Hiihnerei. Inaug. Diss. Berlin, 1875.

(151) W. Waldeyer. "Ueber die Keimblatter und den Primitivstreifen bei der Entwicklung des Hiihnerembryo." Zeitschrift fiir ratioudle Medicin. 1869.

(152) C. F. Wolff. Theoria generationis. Halse, 1759.

(153) C. F. Wolff. Ueb. d. Bildung d. Darmcanals im bebriitcten Hiinchen. Halle, 1812.

REPTILIA.

(154) C. Kupffer and Benecke. Die erste Entwicklung am Ei d. Keptilien. Konigsberg, 1878.


BIBLIOGRAPHY, vii


(155) C. Kupffer. "Die Entstehung d. Allantois u. <1. Gastrula d. Wirbclthiere." Zoologischer Anzeiger, Vol. II. 1879, pp. 520, 593, 612.

Lacertilia.

(156) F. M. Balfour. " On the early Development of the Lacertilia, together with some observations, etc." Quart. J. of Micr. Science, Vol. xix. 1879.

(157) Emmert u. Hochstetter. " Untersuchung lib. d. Entwick. d. Eidechsen in ihren Eiern." Reil's Archiv, Vol. X. 1811.

(158) M. Lereboullet. "Developpement de la Truite, du Lc/ard et du Limnee. II. Embryologie du Lezard." An. Sci. Nat., Ser. iv., Vol. xxvn. 1862.

(159) W. K. Parker. "Structure and Devel. of the Skull in Lacertilia. Phil. Trans., Vol. 170, p. 2. 1879.

(160) H. Strahl. " Ueb. d. Canalis myeloentericus d. Eidechse." Schrift. d. Gesell. z. Be/or, d. gesam. Naturwiss. Marburg. July 23, 1880.

Ophidia.

(161) H. Dutrochet. " Recherches s. 1. en veloppes du foetus." Mem. d. Soc. Mcd. if Emulation, Paris, Vol. vm. 1.816.

(162) W. K. Parker. "On the skull of the common Snake." Phil. Trans. , Vol. 169, Part II. 1878.

(163) H. Rathke. EntTvick. d. Natter. Konigsberg, 1839.

Chelonia.

(164) L. Agassiz. Contributions to the Natural History of the United Slates, Vol. u. 1857. Embryology of the Turtle.

(165) W. K. Parker. "On the development of the skull and nerves in the green Turtle." Proc. of the Roy. Soc., Vol. xxvin. 1879. Vide also Nature, April 14, 1879, and Challenger Reports, Vol. I. 1880.

(166) H. Rathke. Ueb. d. Entwicklung d. Schildkroten. Braunschweig, 1848.

Crocodilia.

(167) H. Rathke. Ueber die Entwicklung d. Krokodile. Braunschweig, 1866.

MAMMALIA.

(168) K. E. von Baer. Ueb. Entwicklungsgcschichte d. Jhiere. Konigsberg,

(169) Barry. "Researches on Embryology." First Series. Philosophical Transactions, 1838, Part II. Second Series, Ibid. 1839, Part II. Third Series, Ibid. 1840.

(170) Ed. van Beneden. La maturation de Foeuf, la fecondation et les premieres phases du developpement embryonaire d. Mammiferes. Bruxelles, 1875.

(171) Ed. van Beneden. " Recherches sur 1'embryologie des Mammiferes. Archives de Biologic, Vol. I. 1880.

(172) Ed. v. Beneden and Ch. Julin. "Observations sur la maturation etc. de 1'oeuf chez les Cheiropteres." Archives de Biologie, Vol. I. 1880.

(173) Th. L. W. Bischoff. Entivicklungsgeschichte d. Siiugethiere 11. des Menschcn. Leipzig, 1842.

(174) Th. L. W. Bischoff. Entivicklungsgeschichte des Kanmcheneies. Braunschweig, 1842.

(175) Th. L. W. Bischoff. Entwicklungsgeschuhte des Hundeeies.

schweig, 1845.

(176) Th. L. W. Bischoff. Entivicklungsgesclnchte des Meerschivcinchens.

Giessen. 1852.


viii BIBLIOGRAPHY.


(177) Th. L. W. Bischoff. Entivicklungsgeschichte des Rehcs. Giesscn, 1854.

(178) Th. L. W. Bischoff. " Neue Beobachtungen z. Entwicklungsgesch. des Meerschweinchens." Abh. d. bayr. Akad., Cl. n. Vol. X. 1866.

(179) Th. L. W. Bischoff. Historisch-kritische B enter kungen z. d. naicstcn Alittheilungen iil>. d. erste Entwick. d. Siitigethiereier. Miinchen, 1877.

(180) M. Coste. Embryogenie comparee. Paris, 1837.

(181) E. Haeckel. Anthropogenie, Entwicklungsgeschichte des Menschen. Lci])zig, 1874.

(182) V. Hensen. "Beobachtungen lib. d. Befrucht. u. Entwick. d. Kaninchens u. Meerschweinchens." Zeit.f. Anat. u. Entwick., Vol. I. 1876.

(183) A. Kolliker. Entivicklungsgeschichte d. Menschen u. d. hb'hcren Thiere. Leipzig, 1879.

(184) A. Kolliker. "Die Entwick. d. Keimblatter des Kaninchens." Zoologist her Anseiger, Nos. 61, 62, Vol. in. 1880.

(185) N. Lieberkiihn. Ueber d. Keimblatter d. Siiugethiere. Doctor- Jubelfeier d. Herrn H. Nasse. Marburg, 1879.

(186) N. Lieberkiihn. "Z. Lehre von d. Keimblattern d. Saugethiere." Sitz. d. Gesell. z. Beford. d. gesam. Natunviss. Marburg, No. 3. 1880.

(187) Rauber. "Die erste Entwicklung d. Kaninchens." Sitzungsber. d. naturfor. Gesell. z. Leipzig. 1875.

(188) C. B. Reichert. " Entwicklung des Meerschweinchens." Abh. der. Berl. Akad. 1862.

(189) E. A. S chafer. " Description of a Mammalian ovum in an early condition of development." Proc. Roy. Soc., No. 168. 1876.

(190) E. A. Schafer. "A contribution to the history of development of the guinea-pig." Journal of Anal, and Phys. , Vol. x. and xi. 1876 and 1877.

Fcetal Membranes and Placenta of Mammalia.

(191) John Anderson. Anatomical and Zoological Researches in Western Yunnan. London, 1878.

(192) K. E. von Baer. Untersuchungen iiber die Gef&ssverbindung zwischen Mutter und Fruc/tf, 1828.

(193) C. G. Cams. Tabulae anatomiam comparali-vam illustrantes. 1831, 1840.

(194) H. C. Chapman. "The placenta and generative apparatus of the Elephant." Journ. Acad. Nat. Sc., Philadelphia. Vol. viii. 1880.

(195) C. Creighton. " On the formation of the placenta in the guinea-pig." Journal of Anat. and Phys., Vol. XII. 1878.

(196) Ecker. Icones Physiologicae. 1852-1859.

(197) G. B. Ercolani. 7'he utricular glands of the uterus, etc., translated from the Italian under the direction of H. O. Marcy. Boston, 1880. Contains translations of memoirs published in the Mem. deW Accad. d. Scienze d. Bologna, and additional matter written specially for the translation.

(198) G. B. Ercolani. Nuove ricerche sulla placenta nei pesci cartilaginosi e nei mammiferi. Bologna, 1 880.

(199) Eschricht. De organis quae respirationi et mttritioni fcetus Mammaliutn inservinnt. Hafniae, 1837.

(200) A. H. Gar rod and W. Turner. "The gravid uterus and placenta of Hyomoschus aquaticus." Proc. Zool. Soc., London, 1878.

(201) P. Hart ing. Het ei en de placenta van Halicore Dugong. Inaug. diss. Utrecht. " On the ovum and placenta of the Dugong." Abstract by Prof. Turner. Journal of Anat. and Phys., Vol. xin.

(202) Th. H. Huxley. The Elements of Comparative Anatomy. London, 1864.

(203) A. Kolliker. " Ueber die Placenta der Gattung Tragulus." Verh. der Wiirzb. phys.-med. Gesellschaft, Bd. x.

(204) C. D. Meigs. "On the reproduction of the Opossum (Didelphis Virginiana)." Amer. Phil. Soc. Trans., Vol. x. 1853.

(205) H.Milne-Edwards. " Sur la Classification Naturelle." Ann. Sciences Nat., Ser. 3, Vol. I. 1844.


BIBLIOGRAPHY.


IX


(206) Alf. Milne-Edwards. "Kecherches sur la famille dcs Chcvrutains.' 1 Ann. dcs Sciences Nat., Series V., Vol. II. 1864.

(207) Alf. Milne-Edwards. " Observations sur quelqucs points <le I'Kmbryologie des Lemuriens, etc." Ann. Sci. Nat., Ser. V., Vol. xv. 1872.

(208) Alf. Milne-Edwards. " Sur la conformation du placenta chcz le Tainandua." Ann. des Sci. Nat., xv. 1872.

(209) Alf. Milne-Edwards. " Kecherches s. 1. enveloppes fcetales du Tatou a neuf bandes." Ann. Sci. Nat., Ser. vi., Vol. vill. 1878.

(210) R. Owen. "On the generation of Marsupial animals, with a description of the impregnated uterus of the Kangaroo." Phil. Trans., 1834.

(211) R. Owen. "Description of the membranes of the uterine foetus of the Kangaroo." Mag. Nat. Hist., Vol. I. 1837.

(212) R. Owen. "On the existence of an Allantois in a foetal Kangaroo (Macropus major)." Zool. Soc. Proc., v. 1837.

(213) R. Owen. "Description of the foetal membranes and placenta of the Elephant." Phil. Trans., 1857.

(214) R.Owen. On the Anatomy of Vertebrates, Vol. III. London, 1868.

(215) G. Rolleston. " Placental structure of the Tenrec, etc." Transactions of the Zoological Society, Vol. V. 1866.

(216) W. Turner. "Observations on the structure of the human placenta." Journal of Anat. and Phys., Vol. vn. 1868.

(217) W. Turner. "On the placentation of the Cetacea." Trans. Roy. Soc. Edinb,, Vol. xxvi. 1872.

(218) W. Turner. "On the placentation of Sloths (Cholcepus Hoffrnanni)." Trans, of R. Society of Edinburgh, Vol. xxvn. 1875.

(219) W. Turner. "On the placentation of Seals (Halichcerus gryphus)." Trans, of R. Society of Edinburgh, Vol. xxvii. 1875.

(220) W.Turner. "On the placentation of the Cape Ant-eater (Orycteropus capensis)." Journal of Anat. and Phys., Vol. X. 1876.

(221) W. Turner. Lectures on the Anatomy of the Placenta. First Series. Edinburgh, 1876.

(222) W. Turner. "Some general observations on the placenta, with special reference to the theory of Evolution." Journal of Anat. and Phys., Vol. XI. 1877.

(223) W.Turner. " On the placentation of the Lemurs." Phil. Trans., Vol. 166, p. 2. 1877.

(224) W.Turner. " On the placentation of Apes." Phil. Trans., 1878.

(225) W. Turner. "The cotyledonary and diffused placenta of the Mexican deer (Cervus Americanus). " Journal of Anat. and Phys., Vol. xm. 1879.


Human Embryo.

(226) Fried. Ahlfeld. " Beschreibung eines sehr kleinen menschlichen Eies." Archiv f. Gynaekologie, Bd. xm. 1878.

(227) Herm. Beigel und Ludwig Loewe. "Beschreibung eines menschlichen Eichens aus der zweiten bis dritten Woche der Schwangerschaft." Archiv f. Gynaekologie, Bd. xn. 1877.

(228) K. Breus. " Ueber ein menschliches Ei aus der zweiten Woche der Graviditat." Wiener medicinische Wochenschrift, 1877.

(229) M. Coste. Histoire generale et particuliere du developpement des corps organises, 1847-59.

(230) A. Ecker. Icones Physiologicae. Leipzig, 1851-1859.

(231) V. Hensen. " Beitrag z. Morphologic d. Korperform u. d. Gehirns d. menschlichen Embryos." Archiv f. Anat. u. Phys., 1877.

(232) W. His. Anatomie menschlicher Etnbryonen, Part I. Embryonen d. ersten Monats. Leipzig, 1880.

(233) J. Kollmann. " Die menschlichen Eier von 6 MM. Grosse." Archiv f.


Anat. und Phys., 1879.

(234) W. Krause. Phys., 1875.

(235) W. Krause. /. wiss. Zool., Vol. xxxv.


Ueber d. Allantois d. Menschen." Archiv f. Anat. und


' Ueber zwei friihzeitige menschliche Embryonen." 1880.


Zeit.


X BIBLIOGRAPHY.


(236) L. Loewe. "Im Sachen cler Eihaute jiingster menschlicher Eicr. " Archiv fiir Gynaekologie, Bd. xiv. 1879.

(237) C. B. Reichert. " Beschreibung einer friihzeitigen menschlichcn Frucht im blaschenformigen Bildungszustande (sackformiger Keim von Baer) nebst vergleichenden Untersuchungen iiber die blaschenformigen Friichte der Saugethiere und des Menschen. " Abhandlungcn der konigl. Akad. d, Wiss, zu Berlin, 1873.

(238) Allen Thomson. "Contributions to the history of the structure of the human ovum and embryo before the third week after conception ; with a description of some early ova." Edinburgh Med. Siirg.Journal, Vol. LI I. 1839.

COMPARISON OF THE FORMATION OF THE GERMINAL LAYERS IN THE VERTEBRATA.

(239) F. M. Balfour. "A comparison of the early stages in the development of Vertebrates." Quart. J. of Micr. Science, Vol. xv. 1875.

(240) F. M. Balfour. "A monograph on the development of Elasmobranch Fishes." London, 1878.

(241) F. M. Balfour. " On the early development of the Lacertilia together with some observations, etc." Quart. J. of Micr. Science, Vol. xix. 1879.

(242) A. Gotte. Die Entwicklungsgeschichte d. Unke. Leipzig, 1875.

(243) W. His. "Ueb. d. Bildung d. Haifischembryonen." Zeit. f. Anal. it. Entwick., Vol. II. 1877. Cf. also His' papers on Teleostei, Nos. 65 and 66.

(244) A. Kowalevsky. " Entwick. d. Amphioxus lanceolatus." Mem. Acad. des Sciences St Petersbourg, Ser. vii. Tom. XI. 1867.

(245) A. Kowalevsky. " Weitere Studien lib. d. Entwick. d. Amphioxus lanceolatus." Archiv f. mikr. Anal., Vol. XIII. 1877.

(246) C. Kupffer. "Die Entstehung d. Allantois u. d. Gastrula d. Wirbelthiere." Zool. Anzeiger, Vol. II. 1879, PP- 5 2 ' 593' 61?.

(247) R. Remak. Untersuchungen iib. d. Entiuicklung d. Wirbelthiere, 1850 1858.

(248) A. Rauber. Primitivstreifen ti. Neurula d. Wirbelthiere, Leipzig, 1877.

PHYLOGENY OF THE CHORDATA.

(249) F. M. Balfour. A Monograph on the development of Elasmobranch Fishes, London, 1878.

(250) A. Dohrn. Der Ursprung d. Wirbelthiere und d. Princip. d. Functionswechsel. Leipzig, 1875.

(251) E. Haeckel. Schb'pfungsgeschichte. Leipzig. Vide also Translation. The History of Creation. King and Co. , London. 1876.

(252) E. Haeckel. Anthropogenie. Leipzig. Vide also Translation. Antliropogeny. Kegan Paul and Co., London, 1878.

(253) A. Kowalevsky. " Entwicklungsgeschichte d. Amphioxus lanceolatus." Mem. Acad. d. Scien. St Petersbourg, Ser. VII. Tom. xi. 1867, and Archiv f. ?nikr. Anat., Vol. XIII. 1877.

(254) A. Kowalevsky. "Weitere Stud. lib. d. Entwick. d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. VII. 1871.

(255) C. Semper. "Die Stammesverwandschaft d. Wirbelthiere u. Wirbellosen." Arbeit, a. d. zool.-zoot. Instit. Wiirzburg, Vol. u. 1875.

(256) C. Semper. "Die Verwandschaftbeziehungen d. gegliederten Thiere." Arbeit, a. d. zool.-zoot. Instit. Wiirzburg, Vol. in. 1876 1877.

GENERAL WORKS ON EMBRYOLOGY.

(257) Allen Thomson. British Association Address, 1877.

(258) A. Agassiz. "Embryology of the Ctenophoroe." Mem. Amcr. Acad. of Arts and Sciences, Vol. X. 1874.

(259) K. E. von Baer. Ueb. Entivicklnngsgeschichle d. Thiere. Konigsberg, 18281837.


BIBLIOGRAPHY.


XI


(260) F. M. Balfour. "A Comparison of the Early Stages in the Development of Vertebrates." Qttart. Journ. of Micr. Set., Vol. XV. 1875.


(261) 1874.


C. Glaus. Die Typenlehre u. E. HaeckeFs sg. Gastnca-theorie. Wieii,


(262) C. Claus. Grundziige d. Zoologie. Marburg und Leipzig, 1879.

(263) A. Dohrn. Der Ursprung d. Wirbdlhiere u. d. Princip des Functionswechsds. Leipzig, 1875.

(264) C. Gegenbaur. Grundriss d. vergleichenden Anatomic. Leipzig, 1878. Vide also Translation. Elements of Comparative Anatomy. Macmillan Co. 1878.

(265) A. Gotte. Ent^vicklungsgeschichte d. Unke. Leipzig, 1874.

(266) E. Haeckel. Studien z. Gastrcca-theorie, Jena, 1877; anc ' a ' so Jenaische Zeitschrift, Vols. vm. and IX. 1874-5.

(267) E. Haeckel. Schdpfungsgeschichte. Leipzig. Vide also Translation, The History of Creation. King & Co., London, 1878.

(268) E. Haeckel. Anthropogenic. Leipzig. Vide also Translation, Atithropogeny. Kegan Paul & Co., London, 1878.

(269) B. Hatschek. "Studien lib. Entwicklungsgeschichte d. Anneliden." Arbeit, a. d. zool. Instit. d. Univer. Wien. 1878.

(270) O. and R. Hertwig. " Die Actinien." Jenaische Zeitschrift, Vols. xiil. and XIV. 1879.

(271) O. and R. Hertwig. Die Cctlomtheorie. Jena, 1881.

(272) O. Hertwig. Die Chatognathen. Jena, 1880.

(273) R. Hertwig. Ueb. d. Ban d. Ctenophoren. Jena, 1880.

(274) T. H. Huxley. The Anatomy of Invertebrated Animals. Churchill, 1877.

(274*) T. H. Huxley. "On the Classification of the Animal Kingdom." Quart. J. of Micr. Science, Vol. XV. 1875.

(275) N. Kleinenberg. Hydra, eine anatomisch-entivicklungsgeschichte Untersnchung. Leipzig, 1872.

(276) A. Kolliker. Entwicklungsgeschichte d. Menschen u. d. hbh. Thiere. Leipzig, 1879.

(277) A. Kowalevsky. " Embryologische Studien an Wurmern u. Arthropoden." Mem. Acad. Petersbourg, Series vii. Vol. xvi. 1871.

(278) E. R. Lankester. "On the Germinal Layers of the Embryo as the Basis of the Genealogical Classification of Animals." Ann. and Mag. of Nat. Hist.

1873 (279) E. R. Lankester. " Notes on Embryology and Classification." Quart.

Jotirn. of Alter. Set., Vol. xvn. 1877.

(280) E. Metschnikoff. "Zur Entwicklungsgeschichte d. Kalkschwamme." Zeit. f. wiss. Zool., Vol. xxiv. 1874.

(281) E. Metschnikoff. " Spongiologische Studien." Zeit. f. wiss. Zool., Vol. xxxn. 1879.

(282) A. S. P. Packard. Life Histories of Animals, including Man, or Outlines of Comparative Embryology. Holt and Co., New York, 1876.

(283) C. Rabl. " Ueb. d. Entwick. d. Malermuschel. " Jenaische Zeitsch., Vol. x. 1876.

(284) C. Rabl. "Ueb. d. Entwicklung. d. Tellerschneke (Planorbis)." Morph. Jahrbuch, Vol. v. 1879.

(285) H. Rathke. Abhandhmgen z. Bildung und Enlwicklungsgesch.d. Menschen u. d. Thiere. Leipzig, 1833.

(286) H. Rathke. Ueber die Bildung u. Entwicklungs. d. Flusskrebses. Leipzig, 1829.

(287) R. Remak. Untersuch. ilb. d. Entwick. d. Wirbelthiere. Berlin, 1855.

(288) Salensky. " Bemerkungen lib. Haeckels Gastrsea-theorie." Archiv /. Naturgeschichte, 1874.

(289) E. Schafer. "Some Teachings of Development." Quart. Jotint. of Micr. Science, Vol. xx. 1880.

(290) C. Semper. " Die Verwandtschaftbeziehungen d. gegliederten Thiere." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. in. 1876-7.


Xll BIBLIOGRAPHY.


GENERAL WORKS DEALING WITH THE DEVELOPMENT OF THE ORGANS OF THE CHORDATA.

(291) K. E. von Baer. Ueber Enlwicklungsgeschichte d. Thiere. Konigsberg, ! 828 1837.

(292) F. M. Balfour. A Monograph on the development of Elasmobranch Fishes. London, 1878.

(293) Th. C. W. Bischoff. Entwicklungsgesch. d. Siiugdhiere u. d. Menschen. Leipzig, 1842.

(294) C. Gegenbaur. Grundriss d. vergleichenden Anatomic. Leipzig, 1878. Vide also English translation, Elements of Comp. Anatomy. London, 1878.

(295) M. Foster and F. M. Balfour. The Elements of Embryology. Part I. London, 1874.

(296) Alex. Gotte. Entwickhmgsgeschichte d. Unke. Leipzig, 1875.

(297) W. His. Untersuch. ilb. d. erste Anlage d. Wirbelthierleibes. Leipzig, 1868.

(298) A. K 6 Hiker. Entwickhmgsgeschichte d. Menschen u. der hoheren Thiere. Leipzig, 1879.

(299) H. Rathke. Abhandlungen u. Bildung und Entwickhingsgeschichle d. Menschen u. d. Thiere. Leipzig, 1838.

(300) H. Rathke. Entwicklungs. d. Natter. Konigsberg, 1839.

(301) H. Rathke. Entwicklungs. d. Wirbelthiere. Leipzig, 1861.

(302) R. Remak. Untersuchungen iib. d. Entwicklung d. Wirbelthiere. Berlin, 18501855.

(303) S. L. Schenk. Lehrbuch d. vergleich. Embryologie d. Wirbelthiere. Wien, 1874.

. EPIDERMIS AND ITS DERIVATIVES. General.

(304) T. H. Huxley. " Tegumentary organs." Todd's Cyclopedia of Anat. and Physiol.

(305) P. Z. Unna. "Histol. u. Entwick. d. Oberhaut." Archiv /. mikr. Anat. Vol. XV. 1876. Pft&also Kolliker (No. 298).

Scales of the Pisces.

(306) O. Hertwig. "Ueber Bau u. Entwicklung d. Placoidschuppen u. d. Zahne d. Selachier." Jenaische Zeitschrift, Vol. vill. 1874.

(307) O. Hertwig. " Ueber d. Hautskelet d. Fische." Morphol. Jahrbuch, Vol. u. 1876. (Siluroiden u. Acipenseridae.)

(308) O. Hertwig. "Ueber d. Hautskelet d. Fische (Lepidosteus u. Polypterus)." Morph. Jahrbuch, Vol. v. 1879.

Feathers.

(309) Th. Studer. Die Entwick. d. Federn. Inaug. Diss. Bern, 1873.

(310) Th. Studer. " Beitrage z. Entwick. d. Feder." Zeit.f. wiss. Zool., Vol. xxx. 1878.

Sweat-glands.

(311) M. S. Ranvier. " Sur la structure des glandes sudoripares." Comptes Rendus, Dec. 29, 1879.


BIBLIOGRAPHY. xiii


Mammary glands.

(312) C. Creighton. "On the development of the Mamma and the Mammary function." Jour, of Anat. and Phys. , Vol. xi. 1877.

(313) C. Gegenbaur. " Bemerkungen lib. d. Milchdriisen-Papillen d. Saugethiere." Jenaische Zeit.. Vol. VII. 1873.

(314) M. Huss. " Beitr. z. Entwick. d. Milchdriisen b. Menschen u. b. Wiederkauern." Jenaische Zeit., Vol. vil. 1873.

(315) C. Langer. " Ueber d. Bau u. d. Entwicklung d. Milchdriisen." Denk. d. k. Akad. Wiss. Wien, Vol. in. 1851.

THE NERVOUS SYSTEM. Evolution of the Nervous System.

(316) F. M. Balfour. " Address to the Department of Anat. and Physiol. of the British Association." 1880.

(317) C. Claus. "Studien lib. Polypen u. Quallen d. Adria. I. Acalephen, Discomedusen." Denk. d. math.-natiirwiss. Classe d. k. Akad. Wiss. Wien, Vol. xxxvin. 1877.

(318) Th. Eimer. Zoologische Studien a. Capri. I. Ueber Beroe ovatus. Ein Beitrag z. Anat. d. Rippenquallen. Leipzig, 1873.

(319) V. Hensen. " Zur Entwicklung d. Nervensystems. " Virchow's Archiv, Vol. xxx. 1864.

(320) O. and R. Hertwig. Das Nerven system u. d. Sinnesorgane d. Medusen. Leipzig, 1878.

(321) O. and R. Hertwig. "Die Actinien anat. u. histol. mit besond. Beriicksichtigung d. Nervenmuskelsystem untersucht." Jenaische Zeit., Vol. xiii. 1879.

(322) R. Hertwig. "Ueb. d. Bau d. Ctenophoren." Jenaische Zeitschrift, Vol. xiv. 1880.

(323) A. W. Hubrecht. "The Peripheral Nervous System in Palseo- and Schizonemertini, one of the layers of the body-wall." Quart, y. of Micr. Science, Vol. xx. 1880.

(324) N. Kleinenberg. Hydra, eine anatomisch-entwickhmgsgeschichthche Untersuchung. Leipzig, 1872.

(325) A. Kowalevsky. " Embryologische Studien an Wtirmern u. Arthropoden." Mem. Acad. Petersboiirg, Series vil., Vol. XVI. 1871.

(326) E. A. Schafer. "Observations on the nervous system of Aurelia aurita." Phil. Trans. 1878.

Nervous System of the Invertebrata.

(327) F. M. Balfour. "Notes on the development of the Araneina." Quart. J. of Micr. Science, Vol. xx. 1880.

(328) B. Hatschek. "Beitr. z. Entwicklung d. Lepidopteren.' Jenaische Zeitschrift, Vol. XI. 1877.

(329) N. Kleinenberg. "The development of the Earthworm, Lumbncus Trapezoides." Quart. J. of Micr. Science, Vol. xix. 1879.

(330) A. Kowalevsky. "Embryologische Studien an Wiirmern u. Arthropoden." Mem. Acad. Petersbourg, Series vin., Vol. xvi. 1871.

(331) H. Reichenbach. "Die Embryonalanlage u. erste Entwick. d. Flusskrebses." Zeit.f. wiss. Zool, Vol. xxix. 1877.

Central Nervous System of the Vertebrata.

(332) C. J. Carus. Versuch einer Darstellung d. Nervensystems, etc. Leipzig,

(333) J. L. Clark. " Researches on the development of the spinal cord in Man, Mammalia and Birds." Phil. Trans., 1862.


xiv BIBLIOGRAPHY.


(334) E. Dursy. " Beitrage zur Entwicklungsgeschichte des Hirnanhanges. " Centralblatt f. d. med. \Vissenschaften, 1 868. Nr. 8.

(335) E. Dursy. Zur Entwicklungsgeschichte des Kopfes des Menschen und der hb'heren Wirbelthiere. Tiibingen, 1869.

(336) A. Ecker. "Zur Entwicklungsgeschichte der Furchen und Windungen der Grosshirn-Hemispharen im Foetus des Menschen." Archiv f. Anthropologie, v. Ecker und Lindenschmidt. Vol. ill. 1868.

(337) E. Ehlers. " Die Epiphyse am Gehirn d. Plagiostomen." Zeit.f.wiss. Zool. Vol. xxx., suppl. 1878.

(338) P. Flechsig. Die Leitungsbahnen im Gehirn und Riickenmark des Menschen. Auf Grtind entwicklungsgeschichtlicher Untersuchungen. Leipzig, 1876.

(339) V. Hensen. "Zur Entwicklung des Nervensystems." Virchoisfs Archiv, Bd. xxx. 1864.

(340) L. Lowe. " Beitrage z. Anat. u. z. Entwick. d. Nervensystems d. Saugethiere u. d. Menschen." Berlin, 1880.

(341) L. Lowe. " Beitrage z. vergleich. Morphogenesis d. centralen Nervensystems d. Wirbelthiere." Mitthcil. a. d. embryol. Instit. Wien, Vol. u. 1880.

(342) A. M. Marshall. "The Morphology of the Vertebrate Olfactory organ." Quart. J. of Micr. Science, Vol. xix. 1879.

(343) V. v. Mihalkovics. Entwicklungsgeschichte d. Gehirns. Leipzig, 1877.

(344) W. Miiller. " Ueber Entwicklung und Bau der Hypophysis und des Processus infundibuli cerebri. " Jenaische Zeitschrift. Bd. vi. 1871.

(345) H. Rahl- Ruck hard. "Die gegenseitigen Verhaltnisse d. Chorda, Hypophysis etc. bei Haifischembryonen, nebst Bemerkungen lib. d. Deutung d. einzelnen Theile d. Fischgehirns." Morphol. Jahrbuch, Vol. vi. 1880.

(346) H. Rathke. " Ueber die Entstehung der glandula pituitaria. " Mullens Archiv f. Anat. und Physiol. , Bd. V. 1838.

(347) C. B. Reich ert. Der Bau des menschlichen Gehirns. Leipzig, 1859 u 1861.

(348) F. Schmidt. "Beitrage zur Entwicklungsgeschichte des Gehirns." Zcitschrift f. wiss. Zoologie, 1862. Bd. xi.

(349) G. Schwalbe. "Beitrag z. Entwick. d. Zwischenhirns." Sitz. d. Jenaischen Gesell.f. Med. u. Natttnviss. Jan. 23, 1880.

(350) Fried. Tiedemann. Anatomie und Bildungsgeschichte des Gehirns im Foetus des Menschen. Niirnberg, 1816.

Peripheral Nervous System of the Vertebrata.

(351) F. M. Balfour. "On the development of the spinal nerves in Elasmobranch Fishes." Philosophical Transactions, Vol. CLXVI. 1876; vide also, A monograph on the development of Elasmobranch Fishes. London, 1878, pp. 191216.

(352) W. His. " Ueb. d. Anfiinge d. peripherischen Nervensystems." Archiv f. Anat. u. Physiol., 1879.

(353) A. M. Marshall. " On the early stages of development of the nerves in Birds." Jottrnal of Anat. and Fkys.,Vo\. XI. 1877.

(354) A. M. Marshall. "The development of the cranial nerves in the Chick." Quart, y. of Micr. Science, Vol. xvni. 1878.

(355) A. M. Marshall. "The morphology of the vertebrate olfactory organ." Quart, y. of Micr. Science, Vol. xix. 1879.

(356) A. M. Marshall. " On the head-cavities and associated nerves in Elasmobranchs." Quart, y. of Micr. Science, Vol. xxi. 1881.

(357) C. Schwalbe. "Das Ganglion oculomotorii. " Jenaische Zeitschrift, Vol. xni. 1879.

Sympathetic Nervous System.

(360) F. M. Balfour. Monograph on the development of Elasmobranch Fishes. London, 1878, p. 173.

(361) S. L. Schenk and W. R. Birdsell. "Ueb. d. Lehre vond. Entwicklung d. Ganglien d. Sympatheticus." Mittheil. a. d. cmbryologischen Instit. Wien. Heft III. 1879.


BIBLIOGRAPHY. XV


THE EYE.

Eye of the Mollusca.

(362) N. Bobretzky. " Observations on the development of the Cephalopoda " (Russian). Nachrichtcn d. kaiserlichen Gesell. d. Frennde der Natuna iss. Anthropolog. Ethnogr. bei d. Universitdt Moskau.

(363) H. Grenacher. " Zur Entwicklungsgeschichte d. Cephalopoden." Zeit. f. wiss. Zool., Bd. xxiv. 1874.

(364) V. Hensen. "Ueber d. Auge einiger Cephalopoden." Zeit. f. wiss. Zool., Vol. xv. 1865.

(365) E. R. Lankester. " Observations on the development of the Cephalopoda." Quart. J. of Micr. Science, Vol. xv. 1875.

(366) C. Semper. Ueber Sehorganevon Typus d. Wirbelthicraugen. Wiesbaden, 1877.

Eye of the Arthropoda.

(367) N. Bobretzky. Development of Astacus and Palaemon. Kiew, 1873.

(368) A. Dohrn. " Untersuchungen lib. Bau u. Entwicklung d. Arthropoden. Palinurus und Scyllarus. " Zeit. f. wiss. Zool., Bd. xx. 1870, p. 264 et seq.

(369) E. Claparede. "Morphologic d. zusammengesetzten Auges bei den Arthropoden." Zeit. f. wiss. Zool., Bd. X. 1860.

(370) H. Grenacher. Untersuchungen iib. d. Sehorgane d. Arthropoden. Gottingen, 1879.

The Vertebrate Eye.

(371) J.Arnold. Beitrage zur Entwicklungsgeschichle des A uges. Heidelberg, 1874.

(372) Babuchin. "Beitrage zur Entwicklungsgeschichte des Auges." Wiirzliurger naturwissenschaftliche Zeitschrift, Bd. 8.

(373) L. Kessler. Zur Ent^vicklung d. Auges d. Wirbclthiere. Leipzig, 1877.

(374) N. Lieberkiihn. Ueber das Auge des Wirbelthierembryo. Cassel, 1872.

(375) N. Lieberkiihn. " Beitrage z. Anat. d. embryonalen Auges." Archiv f. Anat. und Phys., 1879.

(376) L. Lowe. "Beitrage zur Anatomic des Auges" and "Die Histogenese der Retina." Archiv f. mikr. Anat., Vol. xv. 1878.

(377) V. Mihalkowics. "Untersuchungen iiber den Kamm des Vogelauges." Archiv f. mikr. Anat., Vol. IX. 1873.

(378) W. Miiller. " Ueber die Stammesentwickelung des Sehorgans der Wirbelthiere." Festgabe Carl Ludwig. Leipzig, 1874.

(379) S. L. Schenk. "Zur Entwickelungsgeschichte des Auges der Fische." Wiener Sitzungsberichte, Bd. LV. 1867.

Accessory organs of the Vertebrate Eye.

(380) G. Born. "Die Nasenhohlen u. d. Thranennasengang d. Amphibien." Morphologisches Jahrbuch, Bd. II. 1876.

(381) G. Born. " Die Nasenhohlen u. d. Thranennasengang d. amnioten Wirbelthiere. I. Lacertilia. II. Aves." Morphologisches Jahrbuch, Bd. V. 1879.

Eye of the T2tnicata,

(382) A. Kowalevsky. "Weitere Studien iib. d. Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. VII. 1871.

(383) C. Kupffer. "Zur Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. VII. 1872.


xvi BIBLIOGRAPHY.


AUDITORY ORGANS. Auditory organs of tlie Invertebrata.

(384) V. Hensen. "Studien lib. d. Gehororgan d. Decapoden." Zeil.f. wiss. Zool., Vol. xui. 1863.

(385) O. and R. Her twig. Das Nervensystem u. d. Sinnesorgane d. Medusen. Leipzig, 1878.

Auditory organs of the Vertebrata.

(386) A. Boettcher. "Bau u. Entwicklung d. Schnecke." Denkschriften d. kaiserl. Leap. Carol. Akad. d. Wissenschaft., Vol. xxxv.

(387) C. Hasse. Dievergleich. Morphologieu. Histologied. hciutigen Gehororgane d. Wirbelthiere. Leipzig, 1873.

(388) V. Hensen. "Zur Morphologie d. Schnecke." Zeit. f, wiss. ZooI.,Vo\.

XIII. 1863.

(389) E. Huschke. "Ueb. d. erste Bildungsgeschichte d. Auges u. Ohres beim bebrliteten Kiichlein." Isis von Oken, 1831, and Meckel's Archiv, Vol. VI.

(390) Reissner. De Auris internee formatione. Inaug. Diss. Dorpat, 1851.

Accessory parts of Vertebrate Ear.

(391) David Hunt. "A comparative sketch of the development of the ear and eye in the Pig. " Transactions of the International Otological Congress, 1 876.

(392) W. Moldenhauer. "Zur Entwick. d. mittleren u. ausseren Ohres." Morphol. Jahrbiich, Vol. ill. 1877.

(393) V. Urbantschitsch. " Ueb. d. erste Anlage d. Mittelohres u. d. Trommelfelles." Mittheil. a. d. embryol. Instit. Wien, Heft I. 1877.

OLFACTORY ORGAN.

(394) G. Born. "Die Nasenhohlen u. d. Thranennasengang d. amnioten Wirbelthiere." Parts I. and II. Morphologisches Jahrbuch, Bd. V., 1879.

(395) A. Kolliker. " Ueber die Jacobson'schen Organe des Menschen." Festschrift f. Rienecker, 1877.

(396) A. M. Marshall. "Morphology of the Vertebrate Olfactory Organ." Quart. Journ. of Micr. Science, Vol. xix., 1879.

SENSE-ORGANS OF THE LATERAL LINE.

(397) F. M. Balfour. A Monograph on the development of Elasmobranch Fishes, pp. 141 146. London, 1878.

(398) H. Eisig. "Die Segmentalorgane d. Capitelliden." Mitlhcil. a. d. zool. Station zu Neapel, Vol. I. 1879.

(399) A. Gotte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.

(400) Fr. Ley dig. Lehrbuch d. Histologie des Menschen u. d. Thiere. Hamm.

T857 (401) Fr. Ley dig. Nene Beitrdge z. anat. Kenntniss d. Haiitdecke u. IJautsinnesorgane d. Fische. Halle, 1879.

(402) F. E. Schulze. "Ueb. d. Sinnesorgane d. Seitenlinie bei Fischen und Amphibien." Archiv f. mikr. Anat., Vol. vi. 1870.

(403) C. Semper. "Das Urogenitalsystem d. Selachier." Arbeit, a. d. zool.zoot. Instit. Wiirzburg, Vol. II.

(404) B. Solger. "Neue Untersuchungen zur Anat. d. Seitenorgane d. Fische." Archiv f. mikr. Anat., Vol. xvil. and xvni. 1879 and 1880.

ORIGIN OF THE SKELETON.

(405) C. Gegenbaur. "Ueb. primare u. secundare Knochenliildung mit besonderer Beziehung auf d. Lehre von dem Primordialcranium." Jciiaischc Zeitschrifl, Vol. in. 1867.


BIBLIOGRAPHY. xvii


(406) O. Hertwig. "Ueber Bau u. Entwicklung cl. Placoidschuppcn u. d. Ziihne d. Selachicr." Jetiaische Zeitschrift, Vol. vm. 1874.

(407) O. Hertwig. " Ueb. d. Zahnsystem d. Amphibien u. seine Bcdeutung f. d. Genese d. Skelets d. Mundhohle." Archiv f. mikr. Anat., Vol. xi. Supplementheft, 1874.

(408) O. Hertwig. " Ueber d. Hautskelet d. Fische." Morphol. Jahrlmch, Vol. u. 1876. (Siluroiden u. Acipenseriden.)

(409) O. Hertwig. "Ueber d. Hautskelet d. Fische (Lepidosteus u. I'olypterus)." Morph. Jahrbnch, Vol. v. 1879.

(410) A. Kolliker. "AllgemeineBetrachtungenub. die Entstehungd. knocliernen Schadels d. Wirbelthiere. " Berichle v. d. konigl. zoot. Anstalt z. \Viirzlwrg, 1849.

(411) Fr. Leydig. " Histologische Bemerkungen iib. d. Polypterus bichir." Zeit.f. wiss. Zool., Vol. V. 1858.

(412) H. Muller. "Ueber d. Entwick. d. Knochensubstanz nebst Bemerkungen, etc." Zeit. f. wiss. Zool., Vol. IX. 1859.

(413) Williamson. "On the structure and development of the Scales and Bones of Fishes." Phil. Trans., 1851.

(414) Vrolik. " Studien iib. d. Verknocherung u. die Knochen d. Schadels d. Teleostier." Niederldndisches Archiv f. Zoologie, Vol. i.


NOTOCHORD AND VERTEBRAL COLUMN.

(415) Cartier. " Beitrage zur Entwicklungsgeschichte der Wirbelsaule." Zeitschrift fur wiss. Zool., Bd. xxv. Suppl. 1875.

(416) C. Gegenbaur. Untersuchungen zur vergleichenden Anatomic der Wirbelsaule der Amphibien und Reptilien. Leipzig, 1862.

(417) C. Gegenbaur. "Ueber die Entwickelung der Wirbelsaule des Lepidosteus mit vergleichend anatomischen Bemerkungen." Jenaisckc Zeitschrift, Bd. ill. 1863.

(418) C. Gegenbaur. "Ueb. d. Skeletgewebe d. Cyclostomen." Jenaische Zeitschrift, Vol. v. 1870.

(419) Al. Gotte. "Beitrage zur vergleich. Morphol. des Skeletsystems d. Wirbelthiere." II. "Die Wirbelsaule u. ihre Anhange." Archiv f. mikr. Anat., Vol. xv. 1878 (Cyclostomen, Ganoiden, Plagiostomen, Chimaera), and Vol. xvi. 1879 (Teleostier).

(420) Hasse und Schwarck. "Studien zur vergleichenden Anatomic der Wirbelsaule u. s. w." Hasse, Anatomische Studiett, 1872.

(421) C. Hasse. Das natiirliche System d. Elasmobranchier auf Grundlage d. Bau. u. d. Entwick. ihrer Wirbelsaule. Jena, 1879.

(422) A. Kolliker. " Ueber die Beziehungen der Chorda dorsalis zur Bildung der Wirbel der Selachier und einiger anderen Fische." Verhandlungen der physical, medicin. Gesellschaft in Wiirzburg, Bd. X.

(423) A. Kolliker. " Weitere Beobachtungen iiber die Wirbel der Selachier insbesondere iiber die Wirbel der Lamnoidei." Abhandhmgen der senkenbergischen naturforschenden Gesellschaft in Frankfurt, Bd. V.

(424) H. Leboucq. " Recherches s. 1. mode de disparition de la corde dorsale chez les vertebres superieurs." Archives de Biologie, Vol. I. 1 880.

(425) Fr. Leydig. Anatomisch-histologische Untersuchungen iiber Fische und Reptilien. Berlin, 1853.

(426) Aug. Muller. "Beobachtungen zur vergleichenden Anatomic der Wirbelsaule." Miiller's Archiv. 1853.

(427) J. Muller. " Vergleichende Anatomic der Myxinoiden u. der Cyklostomen mit durchbohrtem Gaumen, I. Osteologie und Myologie." Abhandlungcn der koniglichen Akademie der Wissenschaften zu Berlin. 1834.

(428) W. Muller. "Beobachtungen des pathologischen Instituts zu Jena, I. Ueber den Bau der Chorda dorsalis." Jenaische Zeitschrift, Bd. VI. 1871.

(429) A. Schneider. Beitrage z. vergleich. Anat. u. Entwick. d. Wirbelthiere. Berlin, 1879.

B. III. *


xviii BIBLIOGRAPHY.


RIBS AND STERNUM.

(430) C. Claus. " Beitrage z. vergleich. Osteol. d. Vertcbraten. I. Rippen u. unteres Bogensystem." Sitz. d. kaiserl. Akad. Wiss. Wien, Vol. LXXIV. 1876.

(431) A. E. Fick. "Zur Entwicklungsgeschichte d. Rippen und Querfortsritze." Archiv f. Anat. und Physiol. 1879.

(432) C. Gegenbaur. "Zur Entwick. d. Wirbelsaule des Lepidosteus mil vergleich. anat. Bemerk." Jenaische Zeit., Vol. III. 1867.

(433) A. Gotte. "Beitrage z. vergleich. Morphol. d. Skeletsystems d. Wirbelthiere Brustbein u. Schultergiirtel." Archiv f. mikr. Anat., Vol. xiv. 1877.

(434) C. Hasse u. G. Born. " Bcmerkungen lib. d. Morphologic d. Rippen." Zoologischer Anzeiger, 1879.

(435) C.K.Hoffmann. " Beitrage z. vergl. Anat. d. Wirbelthiere." Niederliind. Archiv Zool., Vol. iv. 1878.

(436) W. K. Parker. " A monograph on the structure and development of the shoulder-girdle and sternum." Ray Soc. 1867.

(437) H. Rathke. Ueb. d. Ban u. d. Enlivicklung d. Brustbeins d. Sanricr.

1853 (438) G. Ruge. " Untersuch. lib. Entwick. am Brustbeine d. Menschen." Morphol. Jahrlmch., Vol. VI. 1880.

THE SKULL.

(439) A. Duges. "Recherches sur 1'Osteologie et la myologie des Batraciens a leur differents ages." Paris, Mem. savans tirang. 1835, and An. Sci. Nat. Vol. I. 1834.

(440) C. Gegenbaur. UntersucJmngen z. vergleich. Anat. d. Wirbelthiere, III. Heft. Das Kopfskelet d. Selachier. Leipzig, 1872.

(441) Giinther. Beob. iib. die Entwick. d. Gehbrorgans. Leipzig, 1842.

(442) O. Hertwig. " Ueb. d. Zahnsystem d. Amphibien u. seine Bedeutung f. d. Genese d. Skelets d. Mundhohle. " Archiv f. mikr, Anat., Vol. xi. 1874, suppl.

(443) T. H. Huxley. "On the theory of the vertebrate skull." Proc. Royal Soc., Vol. ix. 1858.

f444) T.H.Huxley. The Elements of Comparative Anatomy . London, 1869.


(445 (446 (447


T. H. Huxley. "On the Malleus and Incus." Proc. Zool. Soc.,

T. H. Huxley. "On Ceratodus Forsteri." Proc. Zool. Soc., 1876.

T. H. Huxley. " The nature of the craniofacial apparatus of Petromyzon."


Journ. of Anat. and Phys., Vol. X. 1876.

(448) T. H. Huxley. The Anatomy of Vertebrated Animals. London, 1871.

(449) W. K. Parker. "On the structure and development of the skull of the Common Fowl (Gallus Domesticus). " Phil. Trans., 1869.

(450) W. K. Parker. "On the structure and development of the skull of the Common Frog (Rana temporaria)." Phil. Trans., 1871.

(451) W. K. Parker. "On the structure and development of the skull in the Salmon (Salmo salar)." Bakerian Lecture, Phil. Trans., 1873.

(452) W. K. Parker. "On the structure and development of the skull in the Pig (Susscrofa)." Phil. Trans., 1874.

(453) W. K. Parker. "On the structure and development of the skull in the Batrachia." Part II. Phil. Trans., 1876.

(454) W. K. Parker. "On the structure and development of the skull in the Urodelous Amphibia." Part in. Phil. Trans., 1877.

(455) W. K. Parker. "On the structure and development of the skull in the Common Snake (Tropidonotus natrix)." Phil. Trans. , 1878.

(456) W. K. Parker. "On the structure and development of the skull in Sharks and Skates." Trans. Zoolog. Soc., 1878. Vol. x. pt. iv.

(1.17) W. K. Parker. "On the structure and development of the skull in the Lacertilia." Pt. I. Lacerta agilis, L. viridis and Zootoca vivipara. Phil. Trans., 1879.


BIBLIOGRAPHY,


(458) W. K. Parker. "The development of the Green Turtle." The Zoolo-v of the Voyage of H.M.S. Challenger. Vol. I. pt. v.

(459) W. K. Parker. "The structure and development of the skull in the Batrachia." 1't. in. Phil. Trans., 1880.

(460) W. K. Parker and G. T. Bettany. The Morphology of the Skull. London, 1877.

(460*) H. Rathke. Entwick. d. Natter. Konigsberg, 1830.

(461) C. B. Reichert. " Ueber die Visceralbogen d. Wirbelthiere." Mailer's Archiv, 1837.

(462) W. Salensky. " Beitrage z. Entwick. d. knorpeligen Gehorknochelchen." Morphol. Jahrbuch, Vol. VI. 1880.

Vide also Kolliker (No. 298), especially for the human and mammalian skull; Gotte (No. 296).

THE PECTORAL GIRDLE.

(463) Bruch. "Ueber die Entwicklung der Clavicula und die Farbe des Blutes." Zeit.f. wiss. Zool., IV. 1853.

(464) A. Duges. " Recherches sur 1'osteologie et la myologie des Batraciens a leurs differents ages." Memoires des savants etrang. Academic royale des sciences de Finstitut de France, Vol. VI. 1835.

(465) C. Gegenbaur. Unterstichungen zur vergleichenden Anatomic der Wirbelthiere, i Heft. Schultergilrtel der Wirbelthiere. Brustflosse der Fische. Leipzig, 1865.

(466) A. Gotte. "Beitrage z. vergleich. Morphol. d. Skeletsystems d. Wirbelthiere : Brustbien u. Schultergiirtel. " Archiv f. mikr. Anat. Vol. XIV. 1877.

(467) C. K. Hoffmann. "Beitrage z. vergleichenden Anatomic d. Wirbelthiere." Niederldndisches Archiv f. Zool. , Vol. V. 1879.

(468) W. K. Parker. " A Monograph on the Structure and Development of the Shoulder-girdle and Sternum in the Vertebrata." Ray Society, 1868.

(469) H. Rathke. Ueber die Entwicklung der Schildkroten. Braunschweig, 1848.

(470) H. Rathke. Ueber den Bau und die Entwicklung des Brustbeins der Satirier, 1853.

(471) A. Sab a tier. Comparaison des ceintures et des menibres anteneurs et posterieurs d. la Serie d. Vertebrcs. Montpellier, 1880.

(472) Georg 'Swirski. Untersuch. lib. d. Entwick. d. Schultergiirtels u. d. Skelets d. Brustflosse d. Hechts. Inaug. Diss. Dorpat, 1880.

THE PELVIC GIRDLE.

(473) A. Bunge. Untersuch. z. Entwick. d. Beckengilrtels d. Amphibien, Reptilien u. Vdgel. Inaug. Diss. Dorpat, 1880.

(474) C. Gegenbaur. " Ueber d. Ausschluss des Schambeins von d. Pfanne d. Hiiftgelenkes." Morph. Jahrbuch, Vol. II. 1876.

(475) Th. H. Huxley. "The characters of the Pelvis in Mammalia, etc." Proc. of Roy. Soc., Vol. xxvin. 1879.

(476) A. S aba tier. Comparaison des ceintures et des membres anterieurs ct postb-ieurs dans la Serie d. Vertebres. Montpellier, 1880.

SKELETON OF THE LIMBS.

(477) M. v. Davidoff. "Beitrage z. vergleich. Anat. d. hinteren Gliedmaassen d. Fische I." Morphol. Jahrbuch, Vol. v. 1879.

(478) C. Gegenbaur. Untersuchungen z. vergleich. Anat. d. Wirbelthiere. Leipzig, 18645. Erstes Heft. Carpus u. Tarsus. Zweites Heft. Brustflosse d. Fische.

(479) C. Gegenbaur. "Ueb. d. Skelet d. Gliedmaassen d. Wirbelthiere im Allgemeinen u. d. Hintergliedmaassen d. Selachier insbesondere." Jenaische Zeilschrift, Vol. V. 1870.


XX BIBLIOGRAPHY.


(480) C. Gegenbaur. " Ueb. d. Archipterygium." Jenaische Zeitschrift, Vol. vn. 1873.

(481) C. Gegenbaur. "Zur Morphologic d. Gliedmaassen d. Wirbelthiere." Morphologisches Jahrbuch, Vol. II. 1876.

(482) A. Gotte. Ueb. Entwick. u. Regeneration d. Gliedmaassenskelets d. Molche. Leipzig, 1879.

(483) T. H. Huxley. "On Ceratodus Forsteri, with some observations on the classification of Fishes." Proc. Zool. Soc. 1876.

(484) St George Mivart. "On the Fins of Elasmobranchii." Zoological Trans., Vol. x.

(485) A. Rosenberg. "Ueb. d. Entwick. d. Extremitaten-Skelets bei einigen d. Reduction ihrer Gliedmaassen charakterisirten Wirbelthiere." Zeit.f. wiss. Zool., Vol. xxin. 1873.

(486) E. Rosenberg. "Ueb. d. Entwick. d. Wirbelsaule u. d. centrale carpi d. Menschen." Morphologisches Jahrbuch, Vol. I. 1875.

(487) H. Strasser. "Z. Entwick. d. Extremitatenknorpel bei Salamandern u. Tritonen." Morphologisches Jahrbuch, Vol. V. 1879.

(488) G. 'S wirski. Unterstich. iib. d. Entwick. d. Schnltergiirtels u. d. Skelets d. Brustflosse d. Hechts. Inaug. Diss. Dorpat, 1880.

(489) J. K. Thacker. "Median and paired fins. A contribution to the history of the Vertebrate limbs." Trans, oftke Connecticut Acad., Vol. III. 1877.

(490) J. K. Thacker. "Ventral fins of Ganoids." Trans, of the Connecticut Acad., Vol. IV. 1877.

PLEURAL AND PERICARDIAL CAVITIES.

(491) M. Cadiat. " Du developpement de la partie cephalothoracique de 1'embryon, de la formation du diaphragme, des pleures, du pericarde, du pharynx et de 1'cesophage." Journal de FAnatomie et de la Physiologic, Vol. xiv. 1878.

VASCULAR SYSTEM. The Heart.

(492) A. C. Bernays. " Entwicklungsgeschichte d. Atrioventricularklappen." Morphol. Jahrbuch, Vol. 11. 1876.

(493) E. Gasser. " Ueber d. Entstehung d. Herzens beim Hiihn." Archiv f. mikr. Anat., Vol. xiv.

(494) A. Thomson. "On the development of the vascular system of the foetus of Vertebrated Animals." Edinb. New Phil. Journal, Vol. ix. 1830 and 1831.

(495) M. Tonge. "Observations on the development of the semilunar valves of the aorta and pulmonary artery of the heart of the Chick." Phil. Trans. CLIX. 1869.

Vide also Von Baer (291), Rathke (300), Hensen (182), Kolliker (298), Gotte (296), and Balfour (292).

The Arterial System.

(496) H. Rathke. "Ueb. d. Entwick. d. Arterien w. bei d. Saugethiere von d. Bogen d. Aorta ausgehen." Miiller's Archiv, 1843.

(41)7) PI. Rathke. " Untersuchungen iib. d. Aortenwurzeln d. Saurier." Denkschriften d. k. Akad. Wien, Vol. xiil. 1857.

Vide also His (No. 232) and general works on Vertebrate Embryology.

The Venous System.

(498) J.Marshall. "On the development of the great anterior veins." Phil. Trans., 1859.


BIHLIOGRAI'IIY. XXJ


(499) H. Rathke. " Ueb. d. Bildung d. Pfortader u. d. Lebervenen b. Sauge thieren." Meckel 's Archiv, 1830.

(500) H. Rathke. "Ueb. d. Bau u. d. Entwick. d. Venensystems d. Wirbclthiere." Bericht. iib. d. natttrh. Seminar, d. Univ. Konigsberg, 1838.

Vide also Von Baer (No. 291), Gotte (No. 296), Kolliker (No. 298), and Rathke (Nos. 299, 300, and 301).

THE SPLEEN.

(501) W. Miiller. "The Spleen." Strieker's Histology.

(502) Peremeschko. "Ueb. d. Entwick. d. Milz." Silz. d. Wien. Akad. Wiss., Vol. LVI. 1867.

THE SUPRARENAL BODIES.

(503) M. Braun. "Bau u. Entwick. d. Nebennieren bei Reptilian." Arbeit, a. d. zool.-zoot. Institut Wilrzburg, Vol. v. 1879.

(504) A. v. Brunn. "Ein Beitrag z. Kenntniss d. feinern Baues u. d. Entwick. d. Nebennieren." Archiv f. mikr. Anat., Vol. vni. 1872.

(505) Fr. Leydig. Untersuch. ilb. Fische u. Reptilien. Berlin, 1853.

(506) Fr. Leydig. Rochen u. Haie. Leipzig, 1852.

Vide also F. M. Balfour (No. 292), Kolliker (No. 298), Remak (No. 302), etc.

THE MUSCULAR SYSTEM OF THE VERTEBRATA.

(507) G.M.Humphry. " Muscles in Vertebrate Animals." J our n. of Anat. and Phys., Vol. vi. 1872.

(508) J. Miiller. "Vergleichende Anatomic d. Myxinoiden. Part I. Osteologie u. Myologie." Akad. Wiss., Berlin, 1834.

(509) A. M. Marshall. "On the head cavities and associated nerves of Elasmobranchs." Quart. J. of Micr. Science, Vol. XXI. 1881.

(510) A. Schneider. "Anat. u. Entwick. d. Muskelsystems d. Wirbelthiere." Sitz. d. Oberhessischen Gesellschaft, 1873.

(511) A. Schneider. Beitrdge z. vergleich. Anat. u. Entwick. d. Wirbelthiere. Berlin, 1879.

Vide also Gotte (No. 296), Kolliker (No. 298), Balfour (No. 292), Huxley, etc.

EXCRETORY ORGANS.

INVER TEBRA TA .

(512) H. Eisig. " Die Segmentalorgane d. Capitelliden." Mitth. a. d. zool. Slat. z. Neapel, Vol. I. 1879.

(513) J. Fraipont. " Recherches s. 1'appareil excreteur des Irematc Cestoides." Archives de Biologie, Vol. I. 1880.

(514) B. Hatschek. "Studien iib. Entwick. d. Annehden. Arbeit, a. d. zool. Instil. Wien, Vol. I. 1878. .

(515) B. Hatschek. "Ueber Entwick. von Echmrus, etc. Arbeit, a.

zool. Instit. Wien, Vol. ill. 1880.

VERTEBRATA.

General.

(516) F. M. Balfour. "On the origin and history of the urinogenital organs of Vertebrates." Journal of Anat. and Phys., Vol. X. 1876.


XXJi BIBLIOGRAPHY.


(517) Max. Fiirbringer 1 . "Zur vergleichenden Anat. u. Entwick. d. Excretionsorgane d. Vertebraten." Morphol. Jahrbuch, Vol. IV. 1878.

(518) H. Meckel. Zur Morphol. d. Harn- u. Geschlechtswerkz.d. Wirbelthiere, etc. Halle, 1848.

(519) Job. Mtiller. Bildungsgeschichte d. Genitalien, etc. Diisseldorf, 1830.

(520) H. Ratbke. "Beobachtungen u. Betrachtungen ii. d. Entwicklung d. Geschlechtswerkzeuge bei den Wirbelthieren." N. Schriften d. naturf. Gesell. in Dantzig, Bd. I. 1825.

(521) C. Semper 1 . "Das Urogenitalsystem d. Plagiostomen u. seine Bedeutung f. d. ubrigen Wirbelthiere." Arb. a. d. zool.-zoot. Insiit. Wiirzburg, Vol. u.

1875 (522) W. Waldeyer 1 . Eierstock u. Ei. Leipzig, 1870.

ElasmobrancJdi.

(523) A. Schultz. "Zur Entwick. d. Selachiereies." Archiv f. mikr. Anal., Vol. xi. 1875.

Vide also Semper (No. 521) and Balfour (No. 292).

Cyclostomata.

(524) J. M uller. " Untersuchungen ii. d. Eingeweide d. Fische. " Abh. d. k. Ak. Wiss. Berlin, 1845.

(525) W. Muller. "Ueber d. Persistenz d. Urniere b. Myxine glutinosa." Jenaische Zeitschrift, Vol. VII. 1873.

(526) W. Muller. "Ueber d. Urogenitalsystem d. Amphioxus u. d. Cyclostomen." Jenaische Zeitschrift, Vol. ix. 1875.

(527) A. Schneider. Beitrdge z. vergleich. Anat. u. Entwick. d. Wirbelthiere. Berlin, 1879.

(528) W. B. Scott. "Beitrage z. Entwick. d. Petromyzonten." Morphol. Jahrbuch, Vol. vn. 1881.

Teleostei.

(529) J. Hyrtl. "Das uropoetische System d. Knochenfische." Denkschr. d. k. k. Akad. Wiss. Wien, Vol. II. 1850.

(530) A. Rosenberg. Untersuchungen iib. die Enlwicklung d. Teleostierniere. Dorpat, 1867.

Vide also Oellacher (No. 72).

Amphibia.

(531) F. H. Bidder. Vergleichend-anatomische u. histologisclie Untcrsiiclniii^cn ii. die mdnnlichcn Geschlec/its- tmd Harmverkzeuge d. nackten Amphibien. Dorpat, 1846.

(532) C. L. Duvernoy. "Fragments s. les Organes genito-urinaires des Reptiles," etc. Mem. Acad. Sciences. Paris. Vol. xi. 1851, pp. 17 95.

(533) M. Fiirbringer. Zur Entwicklung d. Amphibienniere. Heidelberg, 1877.

(534) F. Ley dig. Analomie d. Amphibien u. Keptilien. Berlin, 1853.

(535) F. Leydig. Lehrbuch d. Histologie. Hamm, 1857.

(536) F. Meyer. "Anat. d. Urogenitalsystems d. Selachier u. Amphibien." Sitz. d. naturfor. Gesellsch. Leipzig, 1875.

(537) J. W. Spengel. "Das Urogenitalsystem d. Amphibien." Arb. a. d. zool.- zoot. Instil. Wiirzburg. Vol. in. 1876.

(538) Von Wittich. "Harn- u. Geschlechtswerkzeuge d. Amphibien." Zeit. f. wiss. Zool., Vol. iv.

Vide also Gotte (No. 296).

1 The papers of Fiirbringer, Semper and Waldeyer contain full references to the literature of the Vertebrate excretory organs.


BIBLIOGRAPHY. xxiii


Amniota.

(539) F. M. Balfour and A. Sedgwick. "On the existence of ahead-kidney in the embryo Chick," etc. Quart. J. of Micr. Science, Vol. XIX. 1878.

(540) Banks. On the Wolffian bodies of the foetus and their remains in the adult. Edinburgh, 1864.

(541) Th. Bornhaupt. UntersucJnmgen iib. die Entwicklung d. Urogenitalsystems beim Hiihnchen. Inaug. Diss. Riga, 1867.

(542) Max Braun. "Das Urogenitalsystem d. einheimischen Reptilien." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg. Vol. IV. 1877.

(543) J. Dansky u. J. Kostenitsch. " Ueb. d. Entwick. d. Keimblatter u. d. Wolffschen Ganges im Htihnerei." Me"m. Acad. Imp. Petersbourg, vn. Series, Vol. xxvn. 1880.

(544) Th. Egli. Beitrdge zur Anat. tmd Entiuick. d. Geschlechtsorgane. Inaug. Diss. Zurich, 1876.

(545) E. Gasser. Beitrdge zur Entwickhmgsgeschichte d. Allantois, der MiUler' schen Giinge u. des Afters. Frankfurt, 1874.

(546) E. Gasser. " Beob. iib. d. Entstehung d. WolfFschen Ganges bei Embryonen von Hiihnern u. Gansen." Arch, fiir mikr. Anat., Vol. xiv. 1877.

(547) E. Gasser. "Beitrage z. Entwicklung d. Urogenitalsystems d. Htihnerembryonen." Sitz. d. Cesell. zur Beforderung d. gesam. Naturwiss. Marburg, 1879.

(548) C. Kupffer. " Untersuchung liber die Entwicklung des Harn- und Geschlechtssystems." Archiv fiir mikr. Anat., Vol. II. 1866.

(549) A. Sedgwick. "Development of the kidney in its relation to the Wolffian body in the Chick." Quart. J. of Micros. Science, Vol. XX. 1880.

(550) A. Sedgwick. "On the development of the structure known as the glomerulus of the head -kidney in the Chick." Quart. J. of Micros. Science, Vol. XX. 1880.

(551) A. Sedgwick. "Early development of the Wolffian duct and anterior Wolffian tubules in the Chick ; with some remarks on the vertebrate excretory system." Quart. J. of Micros. Science, Vol. xxi. 1881.

(552) M. Watson. "The homology of the sexual organs, illustrated by comparative anatomy and pathology." Journal of Anat. and Phys., Vol. XIV. 1879.

(553) E. H. Weber. Zusdtze z, Lehre von Bane u. d. Verrichtungen d. Geschlechtsorgane. Leipzig, 1846.

Vide also Remak (No. 302), Foster and Balfour (No. 295), His (No. 297), Kolliker (No. 298).

GENERATIVE ORGANS.

(554) G. Balbiani. Lemons s. la generation des Vertebres. Paris, 1879.

(555) F. M. Balfour. "On the structure and development of the Vertebrate ovary." Quart. J. of Micr. Science, Vol. XVIII.

(556) E. van Beneden. "De la distinction originelledutecticuleet del'ovaire, etc." Bull. Ac. roy. belgique, Vol. xxxvn. 1874.

(557) N. Kleinenberg. "Ueb. d. Entstehung d. Eier b. Eudendrhim." Zeit. f. wiss. Zool., Vol. xxxv. 1 88 r.

(558) H. Ludwig. "Ueb. d. Eibildung im Theirreiche. " Arbeit, a. d. zool.zoot. Instit. Wiirzburg, Vol. I. 1874.

(559) C. Semper. "Das Urogenitalsystem d. Plagiostomen, etc." Arbeit, a. d. zool.-zoot. Instit. Wiirzburg, Vol. II. 1875.

(560) A. Weismann. "Zur Frage nach clem Ursprung d. Geschlechtszellen bei den Hydroiden." Zool. Anzeiger, No. 55, 1880.

Vide also O. and R. Hertwig (No. 271), Kolliker (No. 298), etc.

ALIMENTARY CANAL AND ITS APPENDAGES.

(561) B. Afanassiew. " Ueber Bau u. Entwicklung d. Thymus d. Saugeth." Archiv f. mikr. Anat. Bd. XIV. 1877.


XXIV BIBLIOGRAPHY.


(562) Fr. Boll. Das Princip d. Wachsthums. Berlin, 1876.

(563) E. Gasser. "Die Entstehung d. Cloakenoffhung hei Hiihneremhryonen." Archiv f. Anat. u. Physiol., Anat. Abth. 1880.

(564) A. Gotte. Beitrage zur Entwicklungsgeschichte 'd. Darmkanah im Hithnchcn. 1867.

(565) W. Miiller. " Ueber die Entwickelung der Schilddriise." ycnaische Zeitschrift, Vol. vi. 1871.

(566) W. Miiller. "Die Hypobranchialrinne d. Tunicaten." Jenaischc Zeitschrift, Vol. VII. 1872.

(567) S. L. Schenk. "Die Bauchspeicheldriise d. Embryo." Anatomischphysiologische UntersucJnmgcn. 1872.

(568) E. Selenka. " Beitrag zur Entwicklungsgeschichte d. Luftsacke d. Huhns." Zeit.f. wiss. Zool. 1866.

(569) L. Stieda. Untersuch. lib. d. Entivick. d. Glandula Thymus, Glandula thyroidea, u. Glandula carotica. Leipzig, 1881.

(570) C. Fr. Wolff. " De formatione intestinorum." Nov. Comment. Akad. Petrop. 1766.

(571) A. Wblfler. Ueb. d. Entwick. it. d. Ban d. Schilddriise. Berlin, 1880. Vide also Kolliker (298), Qotte (296), His (232 and 297), Foster and Balfour (2!)5),

Balfour (292), Remak (302), Schenk (303), etc.

Teeth.

(572) T. H. Huxley. "On the enamel and dentine of teeth." Quart. J. of Micros. Science, Vol. III. 1855.

(573) R. Owen. Odontography. London, 1840 1845.

(574) Ch. S. Tomes. Manual of dental anatomy, human and comparative. London, 1876.

(575) Ch. S. Tomes. " On the development of teeth." Quart. J. of Micros. Science, Vol. xvi. 1876.

(576) W. Waldeyer. " Structure and development of teeth." Strieker 's Histology. 1870.

Vide also Kolliker (298), Gegenbaur (294), Hertwig (306), etc.




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