THE GENERAL FEATURES OF THE ELASMOBRANCH EMBRYO AT SUCCESSIVE STAGES.
No complete series of figures, representing the various stages in
development of an Elasmobranch Embryo, has hitherto been published. With
the view of supplying this deficiency Plate 8 has been inserted. The
embryos represented in this Plate form a fairly complete series, but do not
all belong to a single species. Figs. A, B, C, D, E, F, H, I represent
embryos of Pristiurus; G being an embryo of Torpedo. The remaining figures,
excepting K, which is a Pristiurus embryo, are embryos of Scyllium
canicula. The embryos A-I were very accurately drawn from nature by my
sister, Miss A. B. Balfour. Unfortunately the exceptional beauty and
clearness of the originals is all but lost in the lithographs. To
facilitate future description, letters will be employed in the remainder of
these pages to signify that an embryo being described is of the same age as
the embryo on this Plate to which the letter used refers. Thus an embryo of
the same age as L will be spoken of hereafter as belonging to stage L.
A.
This figure represents a hardened blastoderm at a stage when the
embryo-swelling (_e.s._) has become obvious, but before the appearance of
the medullary groove. The position of the segmentation cavity is indicated
by a slight swelling of the blastoderm (_s.c_). The shape of the
blastoderm, in hardened specimens, is not to be relied upon, owing to the
traction which the blastoderm undergoes during the process of removing the
yolk from the egg-shell.
B.
B is the view of a fresh blastoderm. The projecting part of this, already
mentioned as the 'embryonic rim', is indicated by the shading. At the
middle of the embryonic rim is to be seen the rudiment of the embryo
(_m.g._). It consists of an area of the blastoderm, circumscribed on its
two sides and at one end, by a slight fold, and whose other end forms part
of the edge of the blastoderm. The end of the embryo which points towards
the _centre_ of the blastoderm is the head end, and that which forms part
of the _edge_ of the blastoderm is the tail end. To retain the nomenclature
usually adopted in treating of the development of the Bird, the fold at the
anterior end of the embryo may be called _the head fold_, and those at the
sides the _side folds_. There is in Elasmobranchii no tail fold, owing to
the position of the embryo at the periphery of the blastoderm, and it is by
the meeting of the three above-mentioned folds only, that the embryo
becomes pinched off from the remainder of the blastoderm. Along the median
line of the embryo is a shallow groove (_m.g._), the well-known medullary
groove of vertebrate embryology. It flattens out both anteriorly and
posteriorly, and is deepest in the middle part of its course.
C.
This embryo resembles in most of its features the embryo last described. It
is, however, considerably larger, and the head fold and side folds have
become more pronounced structures. The medullary groove is far deeper than
in the earlier stage, and widens out anteriorly. This anterior widening is
the first indication of a distinction between the brain and the remainder
of the central nervous system, a distinction which arises long before the
closure of the medullary canal.
D.
This embryo is far larger than the one last described, but the increase in
length does not cause it to project beyond the edge of the blastoderm, but
has been due to a growth inwards towards the centre of the blastoderm. The
head is now indicated by an anterior enlargement, and the embryo also
widens out posteriorly. The posterior widening (_t.s._) is formed by a pair
of rounded prominences, one on each side of the middle line. These are very
conspicuous organs during the earlier stages of development, and consist of
two large aggregations of mesoblast cells. In accordance with the
nomenclature adopted in my preliminary paper[177], they may be called
'tail-swellings'. Between the cephalic enlargements and the tail-swellings
is situated the rudimentary trunk of the embryo. It is more completely
pinched off from the blastoderm than in the last described embryo. The
medullary groove is of a fairly uniform size throughout the trunk of the
embryo, but flattens out and vanishes completely in the region of the head.
The blastoderm in Pristiurus and Scyllium grows very rapidly, and has by
this stage attained a very considerable size; but in Torpedo its growth is
very slow.
Footnote 177: _Quart. Journ. Micr. Science_, Oct. 1874. [This
Edition, No. V.]
E and F.
These two embryos may be considered together, for, although they differ in
appearance, yet they are of an almost identical age; and the differences
between the two are purely external. E appears to be a little abnormal in
not having the cephalic region so distinctly marked off from the trunk as
is usual. The head is proportionally larger than in the last stage, and the
tail-swellings remain as conspicuous as before. The folding off from the
blastoderm has progressed rapidly, and the head and tail are quite
separated from it. The medullary groove has become closed posteriorly in
both embryos, but the closing has extended further forwards in F than in E.
In F the medullary folds have not only united posteriorly, but have very
nearly effected a fresh junction in the region of the neck. At this point a
second junction of the two medullary folds is in fact actually effected
before the posterior closing has extended forwards so far. The later
junction in the region of the neck corresponds in position with the point,
where in the Bird the medullary folds first unite. No trace of a medullary
groove is to be met with in the head, which simply consists of a wide
flattened plate. Between the two tail-swellings surface views present the
appearance of a groove, but this appearance is deceptive, since in sections
no groove, or at most a very slight one, is perceptible.
G.
During the preceding stages growth in the embryo is very slow, and
considerable intervals of time elapse before any perceptible changes are
effected. This state of things now becomes altered, and the future changes
succeed each other with far greater rapidity. One of the most important of
these, and one which first presents itself during this stage, is the
disappearance of the yolk-spherules from the embryonic cells, and the
consequently increased transparency of the embryo. As a result of this, a
number of organs, which in the earlier stages were only to be investigated
by means of sections, now become visible in the living embryo.
The tail-swellings (_t.s._) are still conspicuous objects at the posterior
extremity of the embryo. The folding off of the embryo from the yolk has
progressed to such an extent that it is now quite possible to place the
embryo on its side and examine it from that point of view.
The embryo may be said to be attached to the yolk by a distinct stalk or
cord, which in the succeeding stages gradually narrows and elongates, and
is known as the umbilical cord (_so.s._). The medullary canal has now
become completely closed, even in the region of the brain, where during the
last stage no trace of a medullary groove had appeared. Slight
constrictions, not perceptible in views of the embryo as a transparent
object, mark off three vesicles in the brain. These vesicles are known as
the fore, mid, and hind brain. From the fore-brain there is an outgrowth on
each side, the first rudiment of the optic vesicle (_op._).
The mesoblast on each side of the body is divided into a series of
segments, known as protovertebræ or muscle-plates, the first of which lies
a little behind the head. The mesoblast of the tail has not as yet
undergone this segmentation. There are present in all seventeen segments.
These first appeared at a much earlier date, but were not visible owing to
the opacity of the embryo.
Another structure which became developed in even a younger embryo than C is
now for the first time visible in the living embryo. This is the notochord:
it extends from almost the extreme posterior to the anterior end of the
embryo. It lies between the ventral wall of the spinal canal and the dorsal
wall of the intestine; and round its posterior end these two walls become
continuous with each other (vide fig.). Anteriorly the termination of the
notochord cannot be seen, it can only be traced into a mass of mesoblast at
the base of the brain, which there separates the epiblast from the
hypoblast. The alimentary canal (_al._) is completely closed anteriorly and
posteriorly, though still widely open to the yolk-sac in the middle part of
its course. In the region of the head it exhibits on each side a slight
bulging outwards, the rudiment of the first visceral cleft. This is
represented in the figure by two lines (I _v.c._). The visceral clefts at
this stage consist of a pair of simple diverticula from the alimentary
canal, and there is no communication between the throat and the exterior.
H.
The present embryo is far larger than the last, but it has not been
possible to represent this increase in size in the drawings. Accompanying
this increase in size, the folding off of the embryo from the yolk has
considerably progressed, and the stalk which unites the embryo with the
yolk is proportionately narrower and longer than before.
The brain is now very distinctly divided into the three lobes, whose
rudiments appeared during the last stage. From the foremost of these, the
optic vesicles now present themselves as well-marked lateral outgrowths,
towards which there appears a growing in, or involution, from the external
skin (_op._) to form the lens. The opening of this involution is
represented by the dark spot in the centre.
A fresh organ of sense, the auditory sac, now for the first time becomes
visible as a shallow pit in the external skin on each side of the
hind-brain (_au.v._). The epiblast which is involuted to form this pit
becomes much thickened, and thereby the opacity, indicated in the figure,
is produced.
The muscle-plates have greatly increased in number by the formation of
fresh segments in the tail. Thirty-eight of them were present in the embryo
figured. The mesoblast at the base of the brain has increased in quantity,
and there is still a certain mass of unsegmented mesoblast which forms the
tail-swellings. The first rudiment of the heart becomes visible during this
stage as a cavity between the mesoblast of the splanchnopleure and the
hypoblast (_ht._).
The fore and hind guts are now longer than they were. A slight pushing in
from the exterior to form the mouth has appeared (_m._), and an indication
of the future position of the anus is afforded by a slight diverticulum of
the hind gut towards the exterior some little distance from the posterior
end of the embryo (_an._). The portion of the alimentary canal behind this
point, though at this stage large, and even dilated into a vesicle at its
posterior end (_al.v._), becomes eventually completely atrophied. In the
region of the throat the rudiment of a second visceral cleft has appeared
behind the first; neither of them are as yet open to the exterior. The
number of visceral clefts present in any given Pristiurus embryo affords a
very easy and simple way of determining its age.
I.
A great increase in size is again to be noticed in the embryo, but, as in
the case of the last embryo, it has not been possible to represent this in
the figure. The stalk connecting the embryo with the yolk has become
narrower and more elongated, and the tail region of the embryo
proportionately far longer than in the last stage. During this stage the
first spontaneous movements of the embryo take place, and consist in
somewhat rapid excursions of the embryo from side to side, produced by a
serpentine motion of the body.
The cranial flexure, which commenced in stage G, has now become very
evident, and the mid-brain[178] begins to project in the same manner as in
the embryo fowl on the third day, and will soon form the anterior
termination of the long axis of the embryo. The fore-brain has increased in
size and distinctness, and the anterior part of it may now be looked on as
the unpaired rudiment of the cerebral hemispheres.
Footnote 178: The part of the brain which I have here called
mid-brain, and which unquestionably corresponds to the part
called mid-brain in the embryos of higher vertebrates, becomes
in the adult what Miklucho-Maclay and Gegenbaur called the
vesicle of the third ventricle or thalamencephalon. I shall
always speak of it as the mid-brain.
Further growths have taken place in the organs of sense, especially in the
eye, in which the involution for the lens has made considerable progress.
The number of the muscle-plates has again increased, but there is still a
region of unsegmented mesoblast in the tail. The thickened portions of
mesoblast which caused the tail-swellings are still to be seen and would
seem to act as the reserve from which is drawn the matter for the rapid
growth of the tail, which occurs soon after this. The mass of the mesoblast
at the base of the brain has again increased. No fresh features of interest
are to be seen in the notochord. The heart is now much more conspicuous
than before, and its commencing flexure is very apparent. It now beats
actively. The hind gut especially is much longer than in the last specimen;
and the point where the anus will appear is very easily detected by the
bulging out of the gut towards the external skin at that point (_an._). The
alimentary vesicle, first observable during the last stage, is now a more
conspicuous organ (_al.v._). Three visceral clefts, none of which are as
yet open to the exterior, may now be seen.
K.
The figures G, H, I are representations of living and transparent embryos,
but the remainder of the figures are drawings of opaque embryos which were
hardened in chromic acid.
The stalk connecting the embryo with the yolk is now, comparatively
speaking, quite narrow, and is of sufficient length to permit the embryo to
execute considerable movements.
The tail has grown immensely, but is still dilated terminally. This
terminal dilatation is mainly due to the alimentary vesicle, but the tract
of gut connecting this with the gut in front of the anus is now a solid rod
of cells and very soon becomes completely atrophied.
The two pairs of limbs have appeared as elongated ridges of epiblast. The
anterior pair is situated just at the front end of the umbilical stalk; and
the posterior pair, which is the more conspicuous of the two, is situated
some little distance behind the stalk.
The cranial flexure has greatly increased, and the angle between the long
axis of the front part of the head and of the body is less than a right
angle. The conspicuous mid-brain forms the anterior termination of the long
axis of the body. The thin roof of the fourth ventricle may in the figure
be noticed behind the mid-brain. The auditory sac is nearly closed and its
opening is not shewn in the figure. In the eye the lens is completely
formed.
Owing to the opacity of the embryo, the muscle-plates are only indistinctly
indicated, and no other features of the mesoblast are to be seen.
The mouth is now a deep pit, whose borders are almost completely formed by
the thickening in front of the first visceral cleft, which may be called
the first visceral arch or mandibular arch.
Four visceral clefts are now visible, all of which are open to the
exterior, but in a transparent embryo one more, not open to the exterior,
would have been visible behind the last of these.
L.
This embryo is considerably older than the one last described, but growth
is not quite so rapid as might be gathered from the fact that L is nearly
twice as long as K, since the two embryos belong to different genera; and
the Scyllium embryos, of which L is an example, are larger than Pristiurus
embryos. The umbilical stalk is now quite a narrow elongated structure,
whose subsequent external changes are very unimportant, and consist for the
most part merely in an increase in its length.
The tail has again grown greatly in length, and its terminal dilatation
together with the alimentary vesicle contained in it, have both completely
vanished. A dorsal and ventral fin are now clearly visible; they are
continuous throughout their whole length. The limbs have grown and are more
easily seen than in the previous stage.
Great changes have been effected in the head, resulting in a diminution of
the cranial flexure. This diminution is nevertheless apparent rather than
real, and is chiefly due to the rapid growth of the rudiment of the
cerebral hemispheres. The three main divisions of the brain may still be
clearly seen from the surface. Posteriorly is situated the hind-brain, now
consisting of the medulla oblongata and cerebellum. At the anterior part of
the medulla is to be seen the thin roof of the fourth ventricle, and
anteriorly to this again the roof becomes thickened to form the rudiment of
the cerebellum. In front of the hind-brain lies the mid-brain, the roof of
which is formed by the optic lobes, which are still situated at the front
end of the long axis of the embryo.
Beyond the mid-brain is placed the fore-brain, whose growth is rapidly
rendering the cranial flexure imperceptible.
The rudiments of the nasal sacs are now clearly visible as a pair of small
pits. The pits are widely open to the exterior, and are situated one on
each side, near the front end of the cerebral hemispheres. Five visceral
clefts are open to the exterior, and in them the external gills have
commenced to appear (L´).
The first cleft is no longer similar to the rest, but has commenced to be
metamorphosed into the spiracle.
Accompanying the change in position of the first cleft, the mandibular arch
has begun to bend round and enclose the front as well as the side of the
mouth. By this change in the mandibular arch the mouth becomes narrowed in
an antero-posterior direction.
M.
Of this embryo the head alone has been represented. Two views of it are
given, one (M) from the side and the other (M´) from the under surface. The
growth of the front part of the head has considerably diminished the
prominence of the cranial flexure. The full complement of visceral clefts
is now present--six in all. But the first has already atrophied
considerably, and may easily be recognized as the spiracle. In Scyllium,
there are present at no period more than six visceral clefts. The first
visceral arch on each side has become bent still further round, to form the
front border of the mouth. The opening of the mouth has in consequence
become still more narrowed in an antero-posterior direction. The width of
the mouth in this direction, serves for the present and for some of the
subsequent stages as a very convenient indication of age.
N.
The limbs, or paired fins, have now acquired the general features and form
which they possess in the adult.
The unpaired fins have now also become divided in a manner not only
characteristic of the Elasmobranchii but even of the genus Scyllium.
There is a tail fin, an anal fin and two dorsal fins, both the latter being
situated behind the posterior paired fins.
In the head may be noticed a continuation of the rapid growth of the
anterior part.
The mouth has become far more narrow and slit-like; and with many other of
the organs of the period commences to approach the form of the adult.
The present and the three preceding stages shew the gradual changes by
which the first visceral arch becomes converted into the rudiments of the
upper and of the lower jaw. The fact of the conversion was first made known
through the investigations of Messrs Parker and Gegenbaur.
O.
In this stage the embryo is very rapidly approaching the form of the adult.
This is especially noticeable in the fins, which project in a manner quite
characteristic of the adult fish. The mouth is slit-like, and the openings
of the nasal sacs no longer retain their primitive circular outline. The
external gills project from all the gill-slits including the spiracle.
P.
The head is rapidly elongating by the growth of the snout, and the
divisions of the brain can no longer be seen with distinctness from the
exterior, and, with the exception of the head and of the external gills,
the embryo almost completely resembles the adult.
Q.
The snout has grown to such an extent, that the head has nearly acquired
its adult shape. In the form of its mouth the embryo now quite resembles
the adult fish.
* * * * *
This part of the subject may be conveniently supplemented by a short
description of the manner in which the blastoderm encloses the yolk. It has
been already mentioned that the growth of the blastoderm is not uniform.
The part of it in the immediate neighbourhood of the embryo remains
comparatively stationary, while the growth elsewhere is very rapid. From
this it results that that part of the edge of the blastoderm where the
embryo is attached forms a bay in the otherwise regular outline of the edge
of the blastoderm. By the time that one-half of the yolk is enclosed the
bay is a very conspicuous feature (Pl. 9, fig. 1). In this figure _bl._
points to the blastoderm, and _yk._ to the part of the yolk not yet
enclosed by the blastoderm.
Shortly subsequent to this the bay becomes obliterated by its two sides
coming together and coalescing, and the embryo ceases to lie at the edge of
the yolk.
This stage is represented on Pl. 9, fig. 2. In this figure there is only a
small patch of yolk not yet enclosed (_yk_), which is situated at some
little distance behind the embryo. Throughout all this period the edge of
the blastoderm has remained thickened, a feature which persists till the
complete investment of the yolk, which takes place shortly after the stage
last figured. In this thickened edge a circular vein arises, which brings
back the blood from the yolk-sac to the embryo. The opening in the
blastoderm (Pl. 9, fig. 2, _yk._), exposing the portion of the yolk not yet
enclosed, may be conveniently called the blastopore, according to Professor
Lankester's nomenclature.
The interesting feature which characterizes the blastopore in
Elasmobranchii is the fact of its not corresponding in position with the
opening of the anus of Rusconi. We thus have in Elasmobranchii two
structures, each of which corresponds in part with the single structure in
Amphioxus which may be called either blastopore or anus of Rusconi, which
yet do not in Elasmobranchii coincide in position. It is the blastopore of
Elasmobranchii which has undergone a change of position, owing to the
unequal growth of the blastoderm; while the anus of Rusconi retains its
normal situation. In Osseous Fishes the blastopore undergoes a similar
change of position. The possibility of a change in position of this
structure is peculiarly interesting, in that it possibly serves to explain
how the blastopore of different animals corresponds in different cases with
the anus or the mouth, and has not always a fixed situation[179].
Footnote 179: For a fuller discussion of this question vide
Self, "A comparison of the early stages of development in
vertebrates." _Quart. Journ. of Micr. Science_, July, 1875.
[This Edition, No. VI.]
EXPLANATION OF PLATES 8 and 9.
COMPLETE LIST OF REFERENCE LETTERS.
_a._ Arteries of yolk sac (red). _al._ Alimentary cavity. _alv._ Alimentary
vesicle at the posterior end of the alimentary canal. _an._ Point where
anus will appear. _auv._ Auditory vesicle. _bl._ Blastoderm. _ch._
Notochord. _es._ Embryo-swelling. _h._ Head. _ht._ Heart. _m._ Mouth. _mg._
Medullary groove. _mp._ Muscle-plate or protovertebra. _op._ Eye. _sc._
Segmentation cavity. _sos._ Somatic stalk. _ts._ Tail-swelling. _v._ Veins
of yolk sac (blue). _vc._ Visceral cleft. I. _vc._ 1st visceral cleft. _x._
Portion of blastoderm outside the arterial circle in which no blood-vessels
are present. _yk._ Yolk.
PLATE 8.
Fig. A. Surface view of blastoderm of Pristiurus hardened in chromic acid.
Fig. B. Surface view of fresh blastoderm of Pristiurus.
Figs. C, D, E, and F. Pristiurus embryos hardened in chromic acid.
Fig. G. Torpedo embryo viewed as a transparent object.
Figs. H, I. Pristiurus embryos viewed as transparent objects.
Fig. K. Pristiurus embryo hardened in chromic acid.
The remainder of the figures are representations of embryos of Scyllium
canicula hardened in chromic acid. In every case, with the exception of the
figures marked P and Q, two representations of the same embryo are given;
one from the side and one from the under surface.
PLATE 9.
Fig. 1. Yolk of a Pristiurus egg with blastoderm and embryo. About
two-thirds of the yolk have been enveloped by the blastoderm. The embryo is
still situated at the edge of the blastoderm, but at the end of a bay in
the outline of this. The thickened edge of the blastoderm is indicated by a
darker shading. Two arteries have appeared.
Fig. 2. Yolk of an older Pristiurus egg. The yolk has become all but
enveloped by the blastoderm, and the embryo ceases to lie at the edge of
the blastoderm, owing to the coalescence of the two sides of the bay which
existed in the earlier stage. The circulation is now largely developed. It
consists of an external arterial ring, and an internal venous ring, the
latter having been developed in the thickened edge of the blastoderm.
Outside the arterial ring no vessels are developed.
Fig. 3. The yolk has now become completely enveloped by the blastoderm. The
arterial ring has increased in size. The venous ring has vanished, owing to
the complete enclosure of the yolk by the blastoderm. The point where it
existed is still indicated (_y_) by the brush-like termination of the main
venous trunk in a number of small branches.
Fig. 4. Diagrammatic projection of the vascular system of the yolk sac of a
somewhat older embryo.
The arterial ring has grown much larger and the portion of the yolk where
no vessels exist is very small (_x_). The brush-like termination of the
venous trunk is still to be noticed.
The two main trunks (arterial and venous) in reality are in close contact
as in fig. 5, and enter the somatic stalk close together.
The letter _a_ which points to the venous (blue) trunk should be _v_ and
not _a_.
Fig. 5. Circulation of the yolk sac of a still older embryo, in which the
arterial circle has ceased to exist, owing to the space outside it having
become smaller and smaller and finally vanished.