subject, as is clear from the following passage in this memoir
(pp. 369-370):--"Each vertebra of _Lepidosteus_ thus consists
of a section of the notochord, and of the cartilaginous tissue
surrounding its sheath, which gives origin to the upper arches
for the whole length of the vertebral column, and in the caudal
region to that of the lower arches also. _The latter do not
however complete the enclosure of a lower canal, but this is
effected by special independent elements_, which are to be
interpreted as homologues of the ribs." (The italics are ours.)
While we fully accept the homology between the ribs and the
lower elements of the hæmal arches of the tail, the view
expressed in the italicised section, to the effect that the
lower parts of the caudal arches are not true hæmal arches but
are independently formed elements, is entirely opposed to our
observations, and has we believe only arisen from the fact that
Gegenbaur had not the young larvæ to work with by which alone
this question could be settled.
The changes which have taken place by this stage with reference to the
hæmal arches of the tail are not very considerable.
In the case of a few more vertebræ the hæmal processes have united into an
arch, and the spinous processes of the arches in the region of the caudal
fin have grown considerably in length. A more important change is perhaps
the commencement of a segmentation of the distal parts of the hæmal arches
from the proximal. This process has not, however, as yet resulted in a
complete separation of the two, such as we find in the adult.
If the hæmal processes are traced forwards (Plate 42, figs. 75 and 76) from
the anterior segment where they meet ventrally, it will be found that each
hæmal process consists of a basal portion, adjoining the notochord, and a
peripheral portion. These two parts are completely continuous, but the line
of a future separation is indicated by the structure of the cartilage,
though not shewn in our figures. As the true body-cavity of the trunk
replaces the obliterated body-cavity of the caudal region, no break of
continuity will be found in the structure of the hæmal processes (Plates 41
and 42, figs. 73 and 74), but while the basal portions grow somewhat
larger, the peripheral portions gradually elongate and take the form of
delicate rods of cartilage extending ventralwards, on each side of the
body-cavity, immediately outside the peritoneal membrane, and along the
lines of insertion of the intermuscular septa. These rods obviously become
the ribs of the adult.
As one travels forwards the ribs become continually longer and more
important, and though they are at this stage united with the hæmal
processes in every part of the trunk, yet they are much more completely
separated from these processes in front than behind (Plate 41, fig. 72).
In front (Plate 41, fig. 72), each rib (_rb._), after continuing its
ventral course for some distance, immediately outside the peritoneal
membrane, turns outwards, and passes along one of the intermuscular septa
till it reaches the epidermis. This feature in the position of the ribs is,
as has been already pointed out in the anatomical part of this section,
characteristic of all the ribs of the adult.
It is unfortunate that we have had no specimens shewing the ribs at an
earlier stage of development; but it appears hardly open to doubt that _the
ribs are originally continuous with the hæmal processes_, and that the
indications of a separation between those two parts at this stage are not
due to a secondary fusion, but to a commencing segmentation.
It further appears, as Müller, Gegenbaur and others have stated, that the
ribs and hæmal processes of the tail are serially homologous structures;
but that the view maintained by Götte in his very valuable memoirs on the
Vertebrate skeleton is also correct to the effect that _the hæmal arches of
the tail are homologous throughout the series of Fishes_.
To this subject we shall return again at the end of the section.
Before leaving the hæmal arches it may be mentioned that behind the region
of the ventral caudal fin the two hæmal processes merge into one, and form
an unpaired knob resting on the ventral side of the notochord, and not
perforated by a canal.
There are now present well-developed intervertebral rings of cartilage,
each of which eventually becomes divided into two parts, and converted into
the adjacent faces of the contiguous vertebræ. These rings are united with
the neural and hæmal arches of the vertebræ in front and behind.
Each ring, as shewn by the transverse section (Plate 41, fig. 71), is not
uniformly thick, but exhibits four projections, two dorsal and two ventral.
These four projections are continuous with the bases of the neural and
hæmal arches of the adjacent vertebræ, and afford presumptive evidence of
the derivation of the intervertebral rings from the neural and hæmal
arches; in that had they so originated, it would be natural to anticipate
the presence of four thickenings indicating the four points from which the
cartilage had spread, while if the rings had originated independently, it
would not be easy to give any explanation of the presence of such
thickenings. Gegenbaur (No. 6), from the investigation of a much older
larva than that we are now describing, also arrived at the conclusion that
the intervertebral cartilages were derived from the neural and hæmal
arches; but as doubts have been thrown upon this conclusion by Götte, and
as it obviously required further confirmation, we have considered it
important to attempt to settle this point. From the description given
above, it is clear that we have not, however, been able absolutely to trace
the origin of this cartilage, but at the same time we think that we have
adduced weighty evidence in corroboration of Gegenbaur's view.
As shewn in longitudinal section (Plate 41, fig. 69, _iv.r._), the
intervertebral rings are thicker in the middle than at the two ends. In
this thickened middle part the division of the cartilage into two parts to
form the ends of two contiguous vertebræ is subsequently effected. The
curved line which this segmentation will follow is, however, already marked
out, and from surface views it might be supposed that this division had
actually occurred.
The histological structure of the intervertebral cartilage is very distinct
from that of the cartilage of the bases of the arches, the nuclei being
much more closely packed. In parts, indeed, the intervertebral cartilage
has almost the character of fibro-cartilage. On each side of the line of
division separating two vertebræ it is invested by a superficial osseous
deposit.
The next oldest larva we have had was 11 centims. in length. The
filamentous dorsal lobe of the caudal fin still projected far beyond the
permanent caudal fin (Plate 34, fig. 16).
The vertebral column was considerably less advanced in development than
that dissected by Gegenbaur, though it shews a great advance on the
previous stage. Its features are illustrated by two transverse sections,
one through the median plane of a vertebral region (Plate 42, fig. 78) and
the other through that of an intervertebral region (Plate 42, fig. 79), and
by a horizontal section (Plate 42, fig. 77).
In the last stage the notochord was only constricted vertebrally. Now,
however, by the great growth of intervertebral cartilage there have
appeared (Plate 42, fig. 77) very well-marked _intervertebral_
constrictions, by the completion of which the vertebræ of _Lepidosteus_
acquire their unique character amongst Fishes.
These constrictions still, however, coexist with the earlier, though at
this stage relatively less conspicuous, vertebral constrictions.
The gelatinous body of the notochord retains its earlier condition. The
sheath has, however, undergone some changes. In the vertebral regions there
is present in any section of the sheath--(1) externally, the membrana
elastica externa (_m.el._); then (2) the external layer of the sheath
(_sh._), which is, however, less thick than before, and exhibits a very
faint form of radial striation; and (3) internally, a fairly thick and
concentrically striated layer. The whole thickness is, on an average, 0.18
millim.
In the intervertebral regions the membrana elastica externa is still
present in most parts, but has become absorbed at the posterior border of
each vertebra, as shewn in longitudinal section in Plate 42, fig. 77. It is
considerably puckered transversely. The sheath of the notochord within the
membrana elastica externa is formed of a concentrically striated layer,
continuous with the innermost layer of the sheath in the vertebral regions.
It is puckered longitudinally. Thus, curiously enough, the membrana
elastica externa and the sheath of the notochord in the intervertebral
regions are folded in different directions, the folds of the one being only
visible in transverse sections (Plate 42, fig. 79), and those of the other
in longitudinal sections (Plate 42, fig. 77).
The osseous and cartilaginous structures investing the notochord may
conveniently be dealt with in the same order as before, viz.: the neural
arches, the hæmal arches, and the intervertebral cartilages.
The cartilaginous portions of the neural arches are still unossified, and
form (Plate 42, fig. 78, _n.a._) small wedge-shaped masses resting on the
sheath of the notochord. They are invested by a thick layer of bone
prolonged upwards to meet the dorsal processes (_n.a´._), which are still
formed of cartilage invested by bone.
It will be remembered that in the last stage there was no key-stone closing
in the neural arch above. This deficiency is now however supplied, and
consists of (1) two bars of cartilage repeated for each vertebra, but
intervertebrally placed, which are directly differentiated from the
ligamentum longitudinale superius, into which they merge above; and (2) two
osseous plates placed on the outer sides of these cartilages, which are
continuous with the lateral osseous bars of the neural arch. The former of
these elements gives rise to the cartilaginous elements above the osseous
bridge of the neural arch in the adult. The two osseous plates supporting
these cartilages clearly form what we have called in our description of the
adult the osseous roof of the spinal canal.
A comparison of the neural arch at this stage with the arch in the adult,
and in the stage last described, shews that the greater part of the neural
arch of the adult is formed of membrane-bone, there being preformed in
cartilage only a small basal part, a dorsal process, and paired key-stones
below the ligamentum longitudinale superius.
The hæmal arches (Plate 42, fig. 78) are still largely cartilaginous, and
rest upon the sheath of the notochord. They are invested by a thick layer
of bone. The bony layer investing the neural and hæmal arches is prolonged
to form a continuous investment round the vertebral portions of the
notochord (Plate 42, fig. 78). This investment is at the sides prolonged
outwards into irregular processes (Plate 42, fig. 78), which form the
commencement of the outer part of the thick but cellular osseous cylinder
forming the middle part of the vertebral body.
The intervertebral cartilages are much larger than in the earlier stage
(Plate 42, figs. 77 and 79), and it is by their growth that the
intervertebral constrictions of the notochord are produced. They have
ceased to be continuous with the cartilage of the arches, the intervening
portion of the vertebral body between the two being only formed of bone.
They are not yet divided into two masses to form the contiguous ends of
adjacent vertebræ.
Externally, the part of each cartilage which will form the hinder end of a
vertebral body is covered by a tube of bone, having the form of a truncated
funnel, shewn in longitudinal section in Plate 42, fig. 77, and in
transverse section in Plate 42, fig. 79.
At each end, the intervertebral cartilages are becoming penetrated and
replaced by beautiful branched processes from the homogeneous bone which
was first of all formed in the perichondrium (Plate 42, fig. 77).
This constitutes the latest stage which we have had.
Gegenbaur (No. 6) has described the vertebral column in a somewhat older
larva of 18 centims.
The chief points in which the vertebral column of this larva differed from
ours are: (1) the disappearance of all trace of the primitive vertebral
constriction of the notochord; (2) the nearly completed constriction of the
notochord in the intervertebral regions; (3) the complete ossification of
the vertebral portions of the bodies of the vertebræ, the terminal
so-called intervertebral portions alone remaining cartilaginous; (4) the
complete ossification of the basal portions of the hæmal and neural
processes included within the bodies of the vertebræ, so that in the case
of the neural arch all trace of the fact that the greater part was
originally not formed in cartilage had become lost. The cartilage of the
dorsal spinous processes was, however, still persistent.
The only points which remain obscure in the later history of the vertebral
column are the history of the notochord and of its sheath. We do not know
how far these are either simply absorbed or partially or wholly ossified.
Götte in his memoir on the formation of the vertebral bodies of the
Teleostei attempts to prove (1) that the so-called membrana elastica
externa of the Teleostei is not a homogeneous elastica, but is formed of
cells, and (2) that in the vertebral regions ossification first occurs in
it.
In _Lepidosteus_ we have met with no indication that the membrana elastica
externa is composed of cells; though it is fair to Götte to state that we
have not examined such isolated portions of it as he states are necessary
in order to make out its structure. But further than this we have satisfied
ourselves that during the earlier stage of ossification this membrane is
not ossified, and indeed in part becomes absorbed in proximity to the
intervertebral cartilages; and Gegenbaur met with no ossification of this
membrane in the later stage described by him.
_Summary of the development of the vertebral column and ribs._
A mesoblastic investment is early formed round the notochord, which is
produced into two dorsal and two ventral ridges, the former uniting above
the neural canal. Around the cuticular sheath of the notochord an elastic
membrane, the membrana elastica externa, is next developed. The neural
ridges become enlarged at each inter-muscular septum, and these
enlargements soon become converted into cartilage, thus forming a series of
neural processes riding on the membrana elastica externa, and extending
about two-thirds of the way up the sides of the neural canal. The hæmal
processes arise simultaneously with, and in the same manner as, the neural.
They are small in the trunk, but at the front end of the anal fin they
suddenly enlarge and extend ventralwards. Each succeeding pair of hæmal
arches becomes larger than the one in front, each arch finally meeting its
fellow below the caudal vein, thus forming a completely closed hæmal canal.
These arches are moreover produced into long spines supporting the fin-rays
of the caudal fin, which thus differs from the other unpaired fins in being
supported by parts of the vertebral column, and not by separately formed
skeletal elements.
In the next stage which we have had the opportunity of studying (larva of
5-1/2 centims.), a series of very well-marked _vertebral_ constrictions are
to be seen in the notochord. The sheath is now much thicker in the
vertebral than in the intervertebral regions: this is due to a special
differentiation of a superficial part of the sheath, which appears more
granular than the remainder. This granular part of the sheath thus forms a
cylinder in each vertebral region. Between it and the gelatinous tissue of
the notochord there remains a thin unmodified portion of the sheath, which
is continuous with the intervertebral parts of the sheath. The neural and
hæmal arches are seen to be continuous with a cartilaginous tube embracing
the intervertebral regions of the notochord, and continuous from one
vertebra to the next. A delicate layer of bone, developed in the
perichondrium, invests the cartilaginous neural arches, and this bone grows
upwards so as to unite above with the osseous investment of separately
developed bars of cartilage, which are directed obliquely backwards. These
bars, or dorsal processes, may be reckoned as parts of the neural arches.
Between the dorsal processes of the two sides is placed a median rod of
cartilage, which is developed separately from the true neural arches, and
which constitutes the median spinous element of the adult. Immediately
below this rod is placed the ligamentum longitudinale superius. There is
now a commencement of separation between the dorsal and ventral parts of
the hæmal arches, not only in the tail, but also in the trunk, where they
pass ventralwards on each side of the body-cavity, immediately outside the
peritoneal membrane, along the lines of insertion of the intermuscular
septa. These are obviously the ribs of the adult, and there is no break of
continuity of structure between the hæmal processes of the tail and the
ribs. In the anterior part of the trunk the ribs pass outwards along the
intermuscular septa till they reach the epidermis. Thus the ribs are
originally continuous with the hæmal processes. Behind the region of the
ventral caudal fin the two hæmal processes merge into one, which is not
perforated by a canal.
Each of the intervertebral rings of cartilage becomes eventually divided
into two parts, and converted into the adjacent faces of contiguous
vertebræ, the curved line where this will be effected being plainly marked
out. These rings are united with the neural and hæmal arches of the
vertebræ next in front and behind. As these rings are formed originally by
the spreading of the cartilage from the primitive neural and hæmal
processes, the intervertebral cartilages are clearly derived from the
neural and hæmal arches. The intervertebral cartilages are thicker in the
middle than at their two ends.
In our latest stage (11 centims.), the vertebral constrictions of the
notochord are rendered much less conspicuous by the growth of the
intervertebral cartilages giving rise to marked intervertebral
constrictions. In the intervertebral regions the membrana elastica externa
has become aborted at the posterior border of each vertebra, and the
remaining part is considerably puckered transversely. The inner sheath of
the notochord is puckered longitudinally in the intervertebral regions. The
granular external layer of the sheath in the vertebral regions is less
thick than in the last stage, and exhibits faint radial striations.
Two closely approximated cartilaginous elements now form a key-stone to the
neural arch above: these are directly differentiated from the ligamentum
longitudinale superius, into which they merge above. An osseous plate is
formed on the outer side of each of these cartilages. These plates are
continuous with the lateral osseous bars of the neural arches, and also
give rise to the osseous roof of the spinal canal of the adult.
Thus the greater part of the neural arches is formed of membrane bone. The
hæmal arches are invested by a thick layer of bone, and there is also a
continuous osseous investment round the vertebral portions of the
notochord. The intervertebral cartilages become penetrated by branched
processes of bone.
_Comparison of the vertebral column of Lepidosteus with that of
other forms._
The peculiar form of the articulatory faces of the vertebræ of
_Lepidosteus_ caused L. Agassiz (No. 2) to compare them with the vertebræ
of Reptiles, and subsequent anatomists have suggested that they more nearly
resemble the vertebræ of some Urodelous Amphibia than those of any other
form.
If, however, Götte's account of the formation of the amphibian vertebræ is
correct, there are serious objections to a comparison between the vertebræ
of _Lepidosteus_ and Amphibia on developmental grounds. The essential point
of similarity supposed to exist between them consists in the fact that in
both there is a great development of intervertebral cartilage which
constricts the notochord intervertebrally, and forms the articular faces of
contiguous vertebræ.
In _Lepidosteus_ this cartilage is, as we have seen, derived from the bases
of the arches; but in Amphibia it is held by Götte to be formed by a
special thickening of a cellular sheath round the notochord which is
probably homologous with the cartilaginous sheath of the notochord of
Elasmobranchii, and therefore with part of the notochordal sheath placed
within the membrana elastica externa.
If the above statements with reference to the origin of the intervertebral
cartilage in the two types are true, it is clear that no homology can exist
between structures so differently developed. Provisionally, therefore, we
must look elsewhere than in _Lepidosteus_ for the origin of the amphibian
type of vertebræ.
The researches which we have recorded demonstrate, however, in a very
conclusive manner that the vertebræ of _Lepidosteus_ have very close
affinities with those of Teleostei.
In support of this statement we may point: (1) To the structure of the
sheath of the notochord; (2) to the formation of the greater part of the
bodies of the vertebræ from ossification in membrane around the notochord;
(3) to the early biconcave form of the vertebræ, only masked at a later
period by the development of intervertebral cartilages; (4) to the
character of the neural arches.
This latter feature will be made very clear if the reader will compare our
figures of the sections of later vertebræ (Plate 42, fig. 78) with
Götte's[523] figure of the section of the vertebra of a Pike (Plate 7,
fig. 1). In Götte's figure there are shewn similar intercalated pieces of
cartilage to those which we have found, and similar cartilaginous dorsal
processes of the vertebræ. Thus we are justified in holding that whether or
no the opisthocoelous form of the vertebræ of _Lepidosteus_ is a
commencement of a type of vertebræ inherited by the higher forms, yet in
any case the vertebræ are essentially built on the type which has become
inherited by the Teleostei from the bony Ganoids.
Footnote 523: "Beiträge zur vergl. Morphol. d. Skeletsystems
d. Wirbelthiere." _Archiv f. Mikr. Anat._ Vol. XVI. 1879.
PART III.--_The ribs of Fishes._
The nature and homologies of the ribs of Fishes have long been a matter of
controversy; but the subject has recently been brought forward in the
important memoirs of Götte[524] on the Vertebrate skeleton. The
alternatives usually adopted are, roughly speaking, these:--Either the
hæmal arches of the tail are homologous throughout the piscine series,
while the ribs of Ganoids and Teleostei are not homologous with those of
Elasmobranchii; or the ribs are homologous in all the piscine groups, and
the hæmal arches in the tail are differently formed in the different types.
Götte has brought forward a great body of evidence in favour of the first
view; while Gegenbaur[525] may be regarded as more especially the champion
of the second view.
Footnote 524: "Beiträge z. vergl. Morph. d. Skeletsystems d.
Wirbelthiere. II. Die Wirbelsäule u. ihre Anhänge." _Archiv f.
Mikr. Anat._, Vol. XV., 1878, and Vol. XVI., 1879.
Footnote 525: "Ueb. d. Entwick. d. Wirbelsäule d. Lepidosteus,
mit. vergl. Anat. Bemerkungen." _Jenaische Zeitschrift_,
Bd. III., 1863.
One of us held in a recent publication[526] that the question was not yet
settled, though the view that the ribs are homologous throughout the series
was provisionally accepted.
Footnote 526: _Comparative Embryology_, Vol. II., pp. 462, 463
[the original edition].
It is admitted by both Gegenbaur and Götte that in _Lepidosteus_ the ribs,
in the transition from the trunk to the tail, bend inwards, and finally
unite in the region of the tail to form the ventral parts of the hæmal
arches, and our researches have abundantly confirmed this conclusion.
Are the hæmal arches, the ventral parts of which are thus formed by the
coalescence of the ribs, homologous with the hæmal arches in
Elasmobranchii? The researches recorded in the preceding pages appear to us
to demonstrate in a conclusive manner that they are so.
The development of the hæmal arches in the tail in these two groups is
practically identical; they are formed in both as simple elongations of the
primitive hæmal processes, which meet below the caudal vein. In the adult
there is an apparent difference between them, arising from the fact that in
_Lepidosteus_ the peripheral parts of the hæmal processes are only
articulated with the basal portions, and not, as in Elasmobranchii,
continuous with them. This difference does not, however, exist in the early
larva, since in the larval _Lepidosteus_ the hæmal arches of the tail are
unsegmented cartilaginous arches, as they permanently are in
Elasmobranchii. If, however, the homology between the hæmal arches of the
two types should still be doubted, the fact that in both types the hæmal
arches are similarly modified to support the fin-rays of the ventral lobe
of the caudal fin, while in neither type are they modified to support the
anal fin, may be pointed out as a very strong argument in confirmation of
their homology.
The demonstration of the homology of the hæmal arches of the tail in
_Lepidosteus_ and Elasmobranchii might at first sight be taken as a
conclusive argument in favour of Götte's view, that the ribs of
Elasmobranchii are not homologous with those of Ganoidei. This view is
mainly supported by two facts:--
(1) In the first place, the ribs in Elasmobranchii do not at first sight
appear to be serially homologous with the ventral parts of the hæmal arches
of the tail, but would rather seem to be lateral offshoots of the hæmal
processes, while the hæmal arches of the tail appear to be completed by the
coalescence of independent ventral prolongations of the hæmal processes.
(2) In the second place, the position of the ribs is different in the two
groups. In Elasmobranchii they are situated between the dorso-lateral and
ventro-lateral muscles (woodcut, fig. 1, _rb._), while in _Lepidosteus_ and
other Ganoids they immediately girth the body-cavity.
[Illustration: FIG. 1.
Diagrammatic section through the trunk of an advanced embryo of _Scyllium_,
to shew the position of the ribs.
_ao._, aorta; _c.sh._, cartilaginous notochordal sheath; _cv._, cardinal
vein; _hp._, hæmal process; _k._, kidney; _l.s._, ligamentum longitudinale
superius; _m.el._, membrana elastica externa; _na._, neural arch; _no._,
notochord; _ll._, lateral line; _rb._, rib; _sp.c._, spinal cord.]
There is much, therefore, to be said in favour of Götte's view. At the same
time, there is another possible interpretation of the facts which would
admit the homology of the ribs as well as of the hæmal arches throughout
the Pisces.
Let us suppose, to start with, that the primitive arrangement of the parts
is more or less nearly that found in _Lepidosteus_, where we have
well-developed ribs in the region of the trunk, girthing the body-cavity,
and uniting in the caudal region to form the ventral parts of the hæmal
arches. It is easy to conceive that the ribs in the trunk might somewhat
alter their position by passing into the muscles, along the inter-muscular
septa, till they come to lie between the dorso-lateral and ventro-lateral
muscles, as in Elasmobranchii. _Lepidosteus_ itself affords a proof that
such a change in the position of the ribs is not impossible, in that it
differs from other Ganoids and from Teleostei in the fact that the free
ends of the ribs leave the neighbourhood of the body-cavity and penetrate
into the muscles.
If it be granted that the mere difference in position between the ribs of
Ganoids and Elasmobranchii is not of itself sufficient to disprove their
homology, let us attempt to picture what would take place at the junction
of the trunk and tail in a type in which the ribs had undergone the above
change in position. On nearing the tail it may be supposed that the ribs
would gradually become shorter, and at the same time alter their position,
till finally they shaded off into ordinary hæmal processes. If, however,
the hæmal canal became prolonged forwards by the formation of some
additional complete or nearly complete hæmal arches, an alteration in the
relation of the parts would necessarily take place. Owing to the position
of the ribs, these structures could hardly assist in the new formation of
the anterior part of the hæmal canal, but the continuation forwards of the
canal would be effected by prolongations of the hæmal processes supporting
the ribs. The new arches so formed would naturally be held to be homologous
with the hæmal arches of the tail, though really not so, while the true
nature of the ribs would also be liable to be misinterpreted, in that the
ribs would appear to be lateral outgrowths of the hæmal processes of a
wholly different nature to the ventral parts of the hæmal arches of the
tail.
In some Elasmobranchii, as shewn in the accompanying woodcut (fig. 2), in
the transitional vertebræ between the trunk and the tail, the ribs are
supported by lateral outgrowths of the hæmal processes, while the wholly
independent prolongations of the hæmal processes appear to be about to give
rise to the hæmal arches of the tail.
This peculiar state of things led Götte, and subsequently one of us, to
deny for Elasmobranchii all homology between the ribs and any part of the
hæmal arches of the tail; but in view of the explanation just suggested,
this denial was perhaps too hasty.
[Illustration: FIG. 2.
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._, hæmal process; _r.p._,
process to which the rib is articulated; _m.el._, membrana elastica
externa; _ch._, notochord; _ao._, aorta; _V.cau._, caudal vein.]
We are the more inclined to take this view because the researches of Götte
appear to shew that an occurrence, in many respects analogous, has taken
place in some Teleostei.
In Teleostei, Johannes Müller, and following him Gegenbaur, do not admit
that the hæmal arches of the tail are in any part formed by the ribs.
Gegenbaur (_Elements of Comp. Anat._, translation, p. 431) says, "In the
Teleostei, the costiferous transverse processes" (what we have called the
hæmal processes) "gradually converge in the caudal region, and form
inferior arches, which are not homologous with those of Selachii and
Ganoidei, although they also form spinous processes."
The opposite view, that the hæmal arches of the tail in Teleostei contain
parts serially homologous with the basal parts of the hæmal processes as
well as with the ribs, has been also maintained by many anatomists, _e.g._,
Meckel, Aug. Müller, &c., and has recently found a powerful ally in Götte.
In many cases, the relations of the parts appear to be fundamentally those
found in _Lepidosteus_ and _Amia_, and Götte has shewn by his careful
embryological investigations on _Esox_ and _Anguilla_, that in these two
forms there is practically conclusive evidence that the ribs as well as the
hæmal costiferous processes of Gegenbaur, which support them, enter into
the formation of the hæmal arches of the tail.
In a great number of Teleostei, _e.g._, the Salmon and most Cyprinoids,
&c., the hæmal arches in the region of transition from the trunk to the
tail have a structure which at first sight appears to support Johannes
Müller's and Gegenbaur's view. The hæmal processes grow larger and meet
each other ventrally; while the ribs articulated to them gradually grow
smaller and disappear.
The Salmon is typical in this respect, and has been carefully studied by
Götte, who attempts to shew (with, in our opinion, complete success) that
the anterior hæmal arches are really not entirely homologous with the true
hæmal arches behind, but that in the latter, the closure of the arch below
is effected by the hæmal spine, which is serially homologous with a pair of
coalesced ribs, while in the anterior hæmal arches, _i.e._, those of the
trunk, the closure of the arch is effected by a bridge of bone uniting the
hæmal processes.
The arrangement of the parts just described, as well as the view of Götte
with reference to them, will be best understood from the accompanying
woodcut (fig. 3), copied from Götte's memoir.
Götte sums up his own results on this point in the following words (p.
138): "It follows from this, that the half rings, forming the hæmal canal
in the hindermost trunk vertebræ of the Salmon, are not (with the exception
of the last) completely homologous with those of the tail, but are formed
by a connecting piece between the basal stumps (hæmal processes), which
originates as a paired median process of these stumps."
The incomplete homology between the anterior hæmal arches and the true
caudal hæmal arches which follow them is exactly what we suggest may be the
case in Elasmobranchii, and if it be admitted in the one case, we see no
reason why it should not also be admitted in the other.
[Illustration: FIG. 3.
Semi-diagrammatic transverse sections through the first caudal vertebra
(A), the last trunk vertebra (B), and the two trunk vertebræ in front (C
and D), of a Salmon embryo of 2-3 centims. (From Götte.)
_ub._, hæmal arch; _ub´._, hæmal process; _ub´´._, rib; _c._, notochord;
_a._, aorta; _v._, vein; _h._, connecting pieces between hæmal processes;
_u._, kidney; _d._, intestine; _sp´._, hæmal spine; _m´._, muscles.]
If this admission is made, the only ground for not regarding the ribs of
Elasmobranchii as homologous with those of Ganoids is their different
position, and we have already attempted to prove that this is not a
fundamental point.
The results of our researches appear to us, then, to leave two alternatives
as to the ribs of Fishes. One of these, which may be called Götte's view,
may be thus stated:--The hæmal arches are homologous throughout the Pisces:
in Teleostei, Ganoidei, and Dipnoi[527], the ribs, placed on the inner face
of the body-wall, are serially homologous with the ventral parts of the
hæmal arches of the tail; in Elasmobranchii, on the other hand, the ribs
are neither serially homologous with the hæmal arches of the tail nor
homologous with the ribs of Teleostei and Ganoidei, but are outgrowths of
the hæmal processes into the space between the dorso-lateral and
ventro-lateral muscles, which may perhaps have their homologues in
Teleostei and Ganoids in certain accessory processes of the vertebræ.
Footnote 527: We find the serial homology of the ribs and
ventral parts of the hæmal arches to be very clear in
_Ceratodus_. Wiedersheim states that it is not clear in
_Protopterus_, although he holds that the facts are in favour
of this view.
The other view, which we are inclined to adopt, and the arguments for which
have been stated in the preceding pages, is as follows:--The Teleostei,
Ganoidei, Dipnoi, and Elasmobranchii are provided with homologous hæmal
arches, which are formed by the coalescence below the caudal vein of simple
prolongations of the primitive hæmal processes of the embryo. The canal
enclosed by the hæmal arches can be demonstrated embryologically to be the
aborted body-cavity.
In the region of the trunk the hæmal processes and their prolongations
behave somewhat differently in the different types.
In Ganoids and Dipnoi, in which the most primitive arrangement is probably
retained, the ribs are attached to the hæmal processes, and are placed
immediately without the peritoneal membrane at the insertions of the
intermuscular septa. These ribs are in many instances (_Lepidosteus_,
_Acipenser_), and very probably in all, developed continuously with the
hæmal processes, and become subsequently segmented from them. They are
serially homologous with the ventral parts of the hæmal arches of the tail,
which, like them, are in many instances (_Ceratodus_, _Lepidosteus_,
_Polypterus_, and to some extent in _Amia_) segmented off from the basal
parts of the hæmal arches.
In Teleostei the ribs have the same position and relations as those in
Ganoids and Dipnoi, but their serial homology with the ventral parts of the
hæmal processes of the tail, is often (_e.g._, the Salmon) obscured by some
of the anterior hæmal arches in the posterior part of the trunk being
completed, not by the ribs, but by independent outgrowths of the basal
parts of the hæmal processes.
In Elasmobranchii a still further divergence from the primitive arrangement
is present. The ribs appear to have passed outwards along the intermuscular
septa into the muscles, and are placed between the dorso-lateral and
ventro-lateral muscles (a change of position of the ribs of the same
nature, but affecting only their ends, is observable in _Lepidosteus_).
This change of position, combined probably with the secondary formation of
a certain number of anterior hæmal arches similar to those in the Salmon,
renders their serial homology with the ventral parts of the hæmal processes
of the tail far less clear than in other types, and further proof is
required before such homology can be considered as definitely established.
This is not the place to enter into the obscure question as to how far the
ribs of the Amphibia and Amniota are homologous with those of Fishes. It is
to be remarked, however, that the ribs of the Urodela (1) occupy the same
position in relation to the muscles as the Elasmobranch ribs, (2) that they
are connected with the neural arches, and (3) that they coexist in the tail
with the hæmal arches, and seem, therefore, to be as different as possible
from the ribs of the Dipnoi.
PART IV.--_The skeleton of the ventral lobe of the tail fin, and its
bearing on the nature of the tail fin of the various types of Pisces._
In the embryos or larvæ of all the Elasmobranchii, Ganoidei, and Teleostei
which have up to this time been studied, the unpaired fins arise as median
longitudinal folds of the integument on the dorsal and ventral sides of the
body, which meet at the apex of the tail. The tail at first is symmetrical,
having a form which has been called diphycercal or protocercal. At a later
stage, usually, though not always, parts of these fins atrophy, while other
parts undergo a special development and constitute the permanent unpaired
fins.
Since the majority of existing as well as extinct Fishes are provided with
discontinuous fins, those forms, such as the Eel (_Anguilla_), in which the
fins are continuous, have probably reverted to an embryonic condition: an
evolutional process which is of more frequent occurrence than has usually
been admitted.
In the caudal region there is almost always developed in the larvæ of the
above groups a special ventral lobe of the embryonic fin a short distance
from the end of the tail. In Elasmobranchii and Chondrostean Ganoids the
portion of the embryonic tail behind this lobe persists through life, and a
special type of caudal fin, which is usually called heterocercal, is thus
produced. This type of caudal fin appears to have been the most usual in
the earlier geological periods.
Simultaneously with the formation of the ventral lobe of the heterocercal
caudal fin, the notochord with the vertebral tissues surrounding it,
becomes bent somewhat dorsalwards, and thus the primitive caudal fin forms
a dorsally directed lobe of the heterocercal tail. We shall call this part
the dorsal lobe of the tail-fin, and the secondarily formed lobe the
ventral lobe.
_Lepidosteus_ and _Amia_ (Wilder, No. 15) amongst the bony Ganoids, and, as
has recently been shewn by A. Agassiz[528], most Teleostei acquire at an
early stage of their development heterocercal caudal fins, like those of
Elasmobranchii and the Chondrostean Ganoids; but in the course of their
further growth the dorsal lobe partly atrophies, and partly disappears as
such, owing to the great prominence acquired by the ventral lobe. A portion
of the dorsally flexed notochord and of the cartilage or bone replacing or
investing it remains, however, as an indication of the original dorsal
lobe, though it does not project backwards beyond the level of the end of
the ventral lobe, which in these types forms the terminal caudal fin.
Footnote 528: "On the Young Stages of some Osseous Fishes.--I.
The Development of the Tail," _Proc. of the American Academy of
Arts and Sciences_, Vol. XIII., 1877.
The true significance of the dorsally flexed portion of the vertebral axis
was first clearly stated by Huxley[529], but as A. Agassiz has fairly
pointed out in the paper already quoted, this fact does not in any way
militate against the view put forward by L. Agassiz that there is a
complete parallelism between the embryonic development of the tail in these
Fishes and the palæontological development of this organ. We think that it
is moreover convenient to retain the term homocercal for those types of
caudal fin in which the dorsal lobe has atrophied so far as not to project
beyond the ventral lobe.
Footnote 529: "Observations on the Development of some Parts
of the Skeleton of Fishes," _Quart. Journ. of Micr. Science_,
Vol. VII., 1859.
We have stated these now well-known facts to enable the reader to follow us
in dealing with the comparison between the skeleton supporting the fin-rays
of the ventral lobe of the caudal fin, and that supporting the fin-rays of
the remaining unpaired fins.
It has been shewn that in _Lepidosteus_ the unpaired fins fall into two
categories, according to the nature of the skeletal parts supporting them.
The fin-rays of the true ventral lobe of the caudal fin are supported by
the spinous processes of certain of the hæmal arches. The remaining
unpaired fins, including the anal fin, are supported by the so-called
interspinous bones, which are developed independently of the vertebral
column and its arches.
The question which first presents itself is, how far does this distinction
hold good for other Fishes? This question, though interesting, does not
appear to have been greatly discussed by anatomists. Not unfrequently the
skeletal supports of the ventral lobe of the caudal fin are assumed to be
the same as those of the other fins.
Davidoff[530], for instance, in speaking of the unpaired fins of
Elasmobranch embryos, says (p. 514): "The cartilaginous rays of the dorsal
fins agreed not only in number with the spinous processes (as indeed is
also found in the caudal fin of the full-grown Dog-fish)," &c.
Footnote 530: "Beiträge z. vergl. Anat. d. hinteren
Gliedmassen d. Fische," _Morph. Jahrbuch_, Vol. V., 1879.
Thacker[531], again, in his memoir on the Median and Paired Fins, states at
p. 284: "We shall here consider the skeleton of the dorsal and anal fins
alone. That of the caudal fin has undergone peculiar modifications by the
union of fin-rays with hæmal spines."
Footnote 531: _Trans. of the Connecticut Acad._, Vol. III.,
1877.
Mivart[532] goes into the question more fully. He points out (p. 471) that
there is an essential difference between the dorsal and ventral parts of
the caudal fin in Elasmobranchii, in that in the former the radials are
more numerous than the vertebræ and unconformable to them, while in the
latter they are equal in number to the vertebræ and continuous with them.
"This," he goes on to say, "seems to point to a difference in nature
between the dorsal and ventral portions of the caudal fin, in at least most
Elasmobranchii." He further points out that _Polyodon_ resembles
Elasmobranchii. As to Teleostei, he does not express himself decidedly
except in the case of _Muræna_, to which we shall return.
Footnote 532: St George Mivart, "Fins of Elasmobranchii,"
_Zool. Trans._, Vol. X.
Mivart expresses himself as very doubtful as to the nature of the supports
of the caudal fin, and thinks "that the caudal fin of different kinds of
Fishes may have arisen in different ways in different cases."
An examination of the ventral part of the caudal fin in various Ganoids,
Teleostei, and Elasmobranchii appears to us to shew that there can be but
little doubt that, in the majority of the members of these groups at any
rate, and we believe in all, the same distinction between the ventral lobe
of the caudal fin and the remaining unpaired fins is found as in
_Lepidosteus_.
In the case of most Elasmobranchii, a simple inspection of the caudal fin
suffices to prove this, and the anatomical features involved in this fact
have usually been recognized; though, in the absence of embryological
evidence, the legitimate conclusion has not always been drawn from them.
The difference between the ventral lobe of the caudal fin and the other
fins in the mode in which the fin-rays are supported is as obvious in
Chondrostean Ganoids as it is in Elasmobranchii; it would appear also to
hold good for _Amia_. _Polypterus_ we have had no opportunity of examining,
but if, as there is no reason to doubt, the figure of its skeleton given by
Agassiz (_Poissons Fossiles_) is correct, there can be no question that the
ventral lobe of the caudal fin is supported by the hæmal arches, and not by
interspinous bones. In _Calamoicthys_, the tail of which we have had an
opportunity of dissecting through the kindness of Professor Parker, the
fin-rays of the ventral lobe of the true caudal fin are undoubtedly
supported by true hæmal arches.
There is no unanimity of opinion as to the nature of the elements
supporting the fin-rays of the caudal fin of Teleostei.
Huxley[533] in his paper on the development of the caudal fin of the
Stickleback, holds that these elements are of the nature of interhæmal
bones. He says (p. 39): "The last of these rings lay just where the
notochord began to bend up. It was slightly longer than the bony ring which
preceded it, and instead of having its posterior margin parallel with the
anterior, it sloped from above downwards and backwards. Two short osseous
plates, attached to the anterior part of the inferior surface of the
penultimate ring, or rudimentary vertebral centrum, passed downwards and a
little backwards, and abutted against a slender elongated mass of
cartilage. Similar cartilaginous bodies occupy the same relation to
corresponding plates of bone in the anterior vertebræ in the region of the
anal fin; and it is here seen, that while the bony plates coalesce and form
the inferior arches of the caudal vertebræ, the cartilaginous elements at
their extremities become the interhæmal bones. The cartilage connected with
the inferior arch of the penultimate centrum is therefore an "interhæmal"
cartilage. The anterior part of the inferior surface of the terminal
ossification likewise has its osseous inferior arch, but the direction of
this is nearly vertical, and though it is connected below with an element
which corresponds in position with the interhæmal cartilage, this cartilage
is five or six times as large, and constitutes a broad vertical plate,
longer than it is deep, and having its longest axis inclined downwards and
backwards....
"Immediately behind and above this anterior hypural apophysis (as it
may be termed) is another very much smaller vertical cartilaginous
plate, which may be called the posterior hypural apophysis."
Footnote 533: "Observations on the Development of some parts
of the Skeleton of Fishes," _Quart. Journ. Micr. Science_,
Vol. VII., 1859.
We have seen that Mivart expresses himself doubtful on the subject.
Gegenbaur[534] appears to regard them as hæmal arches.
Footnote 534: _Elements of Comparative Anatomy._
(Translation), p. 431.
The latter view appears to us without doubt the correct one. An examination
of the tail of normal Teleostei shews that the fin-rays of that part of the
caudal fin which is derived from the ventral lobe of the larva are
supported by elements serially homologous with the hæmal arches, but in no
way homologous with the interspinous bones of the anal fin. The elements in
question formed of cartilage in the larva, become ossified in the adult,
and are known as the hypural bones. They may appear in the form of a series
of separate hæmal arches, corresponding in number with the primitive
somites of this region, which usually, however, atrophy in the adult, or
more often are from the first imperfectly segmented, and have in the adult
the form of two or three or even of a single broad bony plate. The
transitional forms between this state of things and that, for instance, in
_Lepidosteus_ are so numerous, that there can be no doubt that even the
most peculiar forms of the hypural bones of Teleostei are simply modified
hæmal arches.
This view of the hypural bones is, moreover, supported by embryological
evidence, since Aug. Müller[535] (p. 205) describes their development in a
manner which, if his statements are to be trusted, leaves no doubt on this
point.
Footnote 535: "Beobachtungen zur vergl. Anat. d. Wirbelsäule,"
Müller's _Archiv_, 1853.
There are a considerable number of Fishes which are not provided with an
obvious caudal fin as distinct from the remaining unpaired fins, _i.e._
Chimæra, Eels, and various Eel-like forms amongst Teleostei, and the
Dipnoi. Gegenbaur appears to hold that these Fishes ought to be classed
together in relation to the structure of the caudal portion of their
vertebral column, as he says on p. 431 of his _Comparative Anatomy_
(English Translation): "In the Chimæræ, Dipnoi, and many Teleostei, the
caudal portion of the vertebral column ends by gradually diminishing in
size, but in most Fishes, &c."
For our purpose it will, however, be advisable to treat them separately.
The tail of Chimæra appears to us to be simply a peculiar modification of
the typical Elasmobranch heterocercal tail, in which the true ventral lobe
of the caudal fin may be recognized in the fin-fold immediately in front of
the filamentous portion of the tail. In the allied genus _Callorhynchus_
this feature is more distinct. The filamentous portion of the tail of
Chimæra constitutes, according to the nomenclature adopted above, the true
dorsal lobe, and may be partially paralleled in the filamentous dorsal lobe
of the tail of the larval _Lepidosteus_ (Plate 34, fig. 16).
The tail of the eel-like Teleostei is again undoubtedly a modification of
the normal form of tail characteristic of the Teleostei, in which, however,
the caudal fin has become very much reduced and merged into the
prolongations of the anal and dorsal fins.
This can be very clearly seen in Siluroid forms with an Eel-like tail, such
as _Cnidoglanis_. Although the dorsal and ventral fins appear to be
continuous round the end of the tail, and there is superficially no
distinct caudal fin, yet an examination of the skeleton of _Cnidoglanis_
shews that the end of the vertebral column is modified in the usual
Teleostean fashion, and that the hæmal arches of the modified portion of
the vertebral column support a small number of fin-rays; the adjoining
ventral fin-rays being supported by independent osseous fin-supports
(interspinous bones).
In the case of the Eel (_Anguilla anguilla_) Huxley (_loc. cit._) long ago
pointed out that the terminal portion of the vertebral column was modified
in an analogous fashion to that of other Teleostei, and we have found that
the modified hæmal arches of this part support a few fin-rays, though a
still smaller number than in _Cnidoglanis_. The fin-rays so supported
clearly constitute an aborted ventral lobe of the caudal fin.
Under these circumstances we think that the following statement by Mivart
(_Zool. Trans._ Vol. X., p. 471) is somewhat misleading:--
"As to the condition of this part (_i.e._ the ventral lobe of the
tail-fin) in Teleosteans generally, I will not venture as yet to say
anything generally, _except that it is plain that in such forms as
Muræna, the dorsal and ventral parts of the caudal fin are similar in
nature and homotypal with ordinary dorsal and anal fins_[536]."
Footnote 536: The italics are ours.
The italicized portion of this sentence is only true in respect to that
part of the fringe of fin surrounding the end of the body, which is not
only homotypal with, but actually part of, the dorsal and anal fins.
Having settled, then, that the tails of Chimæra and of Eel-like Teleostei
are simply special modifications of the typical form of tail of the group
of Fishes to which they respectively belong, we come to the consideration
of the Dipnoi, in which the tail-fin presents problems of more interest and
greater difficulty than those we have so far had to deal with.
The undoubtedly very ancient and primitive character of the Dipnoi has led
to the view, implicitly if not definitely stated in most text-books, that
their tail-fin retains the character of the piscine tail prior to the
formation of the ventral caudal lobe, a stage which is repeated
embryologically in the pre-heterocercal condition of the tail in ordinary
Fishes.
Through the want of embryological data, and in the absence of really
careful histological examination of the tail of any of the Dipnoi, we are
not willing to speak with very great confidence as to its nature; we are
nevertheless of the opinion that the facts we can bring forward on this
head are sufficient to shew that the tail of the existing Dipnoi is largely
aborted, so that it is more or less comparable with that of the Eel.
We have had opportunities of examining the structure of the tail of
_Ceratodus_ and _Protopterus_ in dissected specimens in the Cambridge
Museum. The vertebral axis runs to the ends of the tail without shewing any
signs of becoming dorsally flexed. At some distance from the end of the
tail the fin-rays are supported by what are apparently segmented spinous
prolongations of the neural and hæmal arches. The dorsal elements are
placed above the longitudinal dorsal cord, and occupy therefore the same
position as the independent elements of the neural arches of _Lepidosteus_.
They are therefore to be regarded as homologous with the dorsal
fin-supports or interspinous bones of other types. The corresponding
ventral elements are therefore also to be regarded as interspinous bones.
In view of the fact that the fin-supports, whenever their development has
been observed, are found to be formed independently of the neural and hæmal
arches, we may fairly assume that this is also true for what we have
identified as the interspinous elements in the Dipnoi.
The interspinous elements become gradually shorter as the end of the tail
is approached, and it is very difficult from a simple examination of
dissected specimens to make out how far any of the posterior fin-rays are
supported by the hæmal arches only. To this question we shall return, but
we may remark that, although there is a prolongation backwards of the
vertebral axis beyond the last interspinous elements, composed it would
seem of the coalesced neural and hæmal arches but without the notochord,
yet by far the majority of the fin-rays which constitute the apparent
caudal fin are supported by interspinous elements.
The grounds on which we hold that the tail of the Dipnoi is to be regarded
as a degenerate rather than primitive type of tail are the following:--
(1) If it be granted that a diphycercal or protocercal form of tail must
have preceded a heterocercal form, it is also clear that the ventral
fin-rays of such a tail must have been supported, as in _Polypterus_ and
_Calamoicthys_, by hæmal arches, and not by interspinous elements;
otherwise, a special ventral lobe, giving a heterocercal character to the
tail, and provided with fin-rays supported only by hæmal arches, could
never have become evolved from the protocercal tail-fin. Since the ventral
fin-rays of the tail of the Dipnoi are supported by interspinous elements
and not by hæmal arches, this tail-fin cannot claim to have the character
of _that_ primitive type of diphycercal or protocercal tail from which the
heterocercal tail must be supposed to have been evolved.
(2) Since the nearest allies of the Dipnoi are to be found in _Polypterus_
and the Crossopterygidæ of Huxley, and since in these forms (as evinced by
the structure of the tail-fin of _Polypterus_, and the transitional type
between a heterocercal and diphycercal form of fin observable in fossil
Crossopterygidæ) the ventral fin-rays of the caudal fin were clearly
supported by hæmal arches and not by interspinous elements, it is rendered
highly probable that the absence of fin-rays so supported in the Dipnoi is
a result of degeneration of the posterior part of the tail.
[We use this argument without offering any opinion as to whether the
diphycercal character of the tail of many Crossopterygidæ is primary or
secondary.]
(3) The argument just used is supported by the degenerate and variable
state of the end of the vertebral axis in the Dipnoi--a condition most
easily explained by assuming that the terminal part of the tail has become
aborted.
(4) We believe that in _Ceratodus_ we have been able to trace a small
number of the ventral fin-rays supported by hæmal arches only, but these
rays are so short as not to extend so far back as some of the rays attached
to the interspinous elements in front. These rays may probably be
interpreted, like the more or less corresponding rays in the tail of the
Eel, as the last remnant of a true caudal fin.
The above considerations appear to us to shew with very considerable
probability that the true caudal fin of the Dipnoi has become all but
aborted like that of various Teleostei; and that the apparent caudal fin is
formed by the anal and dorsal fins meeting round the end of the stump of
the tail.
From the adult forms of Dipnoi we are, however, of opinion that no
conclusion can be drawn as to whether their ancestors were provided with a
diphycercal or a heterocercal form of caudal fin.
The general conclusions with reference to the tail-fin at which we have
arrived are the following:--
(1) The ventral lobe of the tail-fin of Pisces differs from the other
unpaired fins in the fact that its fin-rays are directly supported by
spinous processes of certain of the hæmal arches instead of independently
developed interspinous bones.
(2) The presence or absence of fin-rays in the tail-fin supported by hæmal
arches may be used in deciding whether apparently diphycercal tail-fins are
aborted or primitive.
EXCRETORY AND GENERATIVE ORGANS.
I.--_Anatomy._
The excretory organs of _Lepidosteus_ have been described by Müller (No.
13) and Hyrtl (No. 11). These anatomists have given a fairly adequate
account of the generative ducts in the female, and Hyrtl has also described
the male generative ducts and the kidney and its duct, but his description
is contradicted by our observations in some of the most fundamental points.
In the female example of 100.5 centims. which we dissected, the kidney
forms a paired gland, consisting of a narrow strip of glandular matter
placed on each side of the vertebral column, on the dorsal aspect of the
body-cavity. It is covered on its ventral aspect by the oviduct and by its
own duct, but is separated from both of these by a layer of the tough
peritoneal membrane, through which the collecting tubes pass. It extends
forwards from the anus for about three-fifths of the length of the
body-cavity, and in our example had a total length of about 28 centims.
(Plate 39, fig. 60, _k_). Anteriorly the two kidneys are separated by a
short interval in the median line, but posteriorly they come into contact,
and are so intimately united as almost to constitute a single gland.
A superficial examination might lead to the supposition that the kidney
extended forwards for the whole length of the body-cavity up to the region
of the branchial arches, and Hyrtl appears to have fallen into this error;
but what appears to be its anterior continuation is really a form of
lymphatic tissue, something like that of the spleen, filled with numerous
cells. This matter (Plate 39, fig. 60, _ly._) continues from the kidney
forwards without any break, and has a colour so similar to that of the
kidney as to be hardly distinguishable from it with the naked eye. The true
anterior end of the kidney is placed about 3 centims. in front on the left
side, and on the same level on the right side as the wide anterior end of
the generative duct (Plate 39, fig. 60, _od._). It is not obviously divided
into segments, and is richly supplied with malpighian bodies.
It is clear from the above description that there is no trace of
head-kidney or pronephros visible in the adult. To this subject we shall,
however, again return.
As will appear from the embryological section, the ducts of the kidneys are
probably simply the archinephric ducts, but to avoid the use of terms
involving a theory, we propose in the anatomical part of our work to call
them kidney ducts. They are thin-walled widish tubes coextensive with the
kidneys. If cut open there may be seen on their inner aspect the numerous
openings of the collecting tubes of the kidneys. They are placed ventrally
to and on the outer border of the kidneys (Plate 39, fig. 60, _s.g._).
Posteriorly they gradually enlarge, and approaching each other in the
median line, coalesce, forming an unpaired vesicle or bladder
(_bl._)--about 6 centims. long in our example--opening by a median pore on
a more or less prominent papilla (_u.g._) behind the anus. The dilated
portions of the two ducts are called by Hyrtl the horns of the bladder.
The sides of the bladder and its so-called horns are provided with lateral
pockets into which the collecting tubes of the kidney open. These pockets,
which we have found in two female examples, are much larger in the horns of
the bladder than in the bladder itself. Similar pockets, but larger than
those we have found, have been described by Hyrtl in the male, but are
stated by him to be absent in the female. It is clear from our examples
that this is by no means always the case.
Hyrtl states that the wide kidney ducts, of which his description differs
in no material point from our own, suddenly narrow in front, and,
perforating the peritoneal lining, are continued forwards to supply the
anterior part of the kidney. We have already shewn that the anterior part
of the kidney has no existence, and the kidney ducts supplying it are,
according to our investigations, equally imaginary.
It was first shewn by Müller, whose observations on this point have been
confirmed by Hyrtl, &c., that the ovaries of _Lepidosteus_ are continuous
with their ducts, forming in this respect an exception to other Ganoids.
In our example of _Lepidosteus_ the ovaries (Plate 39, fig. 60, _ov._) were
about 18 centims. in length. They have the form of simple sacks, filled
with ova, and attached about their middle to their generative duct, and
continued both backwards and forwards from their attachment into a blind
process.
With reference to these sacks Müller has pointed out--and the importance of
this observation will become apparent when we deal with the
development--that the ova are formed in the thickness of the inner wall of
the sack. We hope to shew that the inner wall of the sack is alone
equivalent to the genital ridge of, for instance, the ovary of _Scyllium_.
The outer aspect of this wall--_i.e._, that turned towards the interior of
the sack--is equivalent to the outer aspect of the Elasmobranch genital
ridge, on which alone the ova are developed[537]. The sack into which the
ova fall is, as we shall shew in the embryological section, a special
section of the body-cavity shut off from the remainder, and the dehiscence
of the ova into this cavity is equivalent to their discharge into the
body-cavity in other forms.
Footnote 537: _Treatise on Comparative Embryology_, Vol. I.,
p. 43 [the original edition].
The oviduct (Plate 39, fig. 60, _od._) is a thin-walled duct of about 21
centims. in length in the example we are describing, continuous in front
with the ovarian sack, and gradually tapering behind, till it ends (_od´._)
by opening into the dilated terminal section of the kidney duct on the
inner side, a short distance before the latter unites with its fellow. It
is throughout closely attached to the ureter and placed on its inner, and
to some extent on its ventral, aspect. The hindermost part of the oviduct
which runs beside the enlarged portion of the kidney duct--that portion
called by Hyrtl the horn of the urinary bladder--is so completely enveloped
by the wall of the horn of the urinary bladder as to appear like a
projection into the lumen of the latter structure, and the somewhat
peculiar appearance which it presents in Hyrtl's figure is due to this
fact. In our examples the oviduct was provided with a simple opening into
the kidney duct, on a slight papilla; the peculiar dilatations and
processes of the terminal parts of the oviduct, which have been described
by Hyrtl, not being present.
The results we have arrived at with reference to the male organs are very
different indeed from those of our predecessor, in that we find _the
testicular products to be carried off by a series of vasa efferentia, which
traverse the mesorchium, and are continuous with the uriniferous tubuli; so
that the semen passes through the uriniferous tubuli into the kidney duct
and so to the exterior. We have moreover been unable to find in the male a
duct homologous with the oviduct of the female._
This mode of transportation outwards of the semen has not hitherto been
known to occur in Ganoids, though found in all Elasmobranchii, Amphibia,
and Amniota. It is not, however, impossible that it exists in other
Ganoids, but has hitherto been overlooked.
Our male example of Lepidosteus was about 60 centims. in length, and was no
doubt mature. It was smaller than any of our female examples, but this
according to Garman (vide, p. 361) is usual. The testes (Plate 39,
fig. 58A., _t._) occupied a similar position to the ovaries, and were about
21 centims. long. They were, as is frequently the case with piscine testes,
divided into a series of lobes (10-12), and were suspended by a delicate
mesentery (mesorchium) from the dorsal wall of the abdomen on each side of
the dorsal aorta. Hyrtl (No. 11) states that air or quicksilver injected
between the limbs of the mesentery, passed into a vas deferens homologous
with the oviduct which joins the ureter. We have been unable to find such a
vas deferens; but we have found in the mesorchium a number of tubes of a
yellow colour, the colour being due to a granular substance quite unlike
coagulated blood, but which appeared to us from microscopic examination to
be the remains of spermatozoa[538]. These tubes to the number of 40-50
constitute, we believe, the vasa efferentia. Along the line of suspension
of the testis on its inner border these tubes unite to form an elaborate
network of tubes placed on the inner face of the testis--an arrangement
very similar to that often found in Elasmobranchii (vide F. M. Balfour,
_Monograph on the Development of Elasmobranch Fishes_, plate 20, figs. 4
and 8).
Footnote 538: The females we examined, which were no doubt
procured at the same time as the male, had their oviducts
filled with ova: and it is therefore not surprising that the
vasa efferentia should be naturally injected with sperm.
We have figured this network on the posterior lobe of the testi
(fig. 58B), and have represented a section through it (fig. 59A, _n.v.e._),
and through one of the vasa efferentia (_v.e._) in the mesorchium. Such a
section conclusively demonstrates the real nature of these passages: they
are filled with sperm like that in the body of the testis, and are, as may
be seen from the section figured, continuous with the seminal tubes of the
testis itself.
At the attached base of the mesorchium the vasa efferentia unite into a
longitudinal canal, placed on the inner side of the kidney duct (Plate 39,
fig. 58A, _l.c._, also shewn in section in Plate 39, fig. 59B, _l.c._).
From this canal tubules pass off which are continuous with the tubuli
uriniferi, as may be seen from fig. 59B, but the exact course of these
tubuli through the kidney could not be made out in the preparations we were
able to make of the badly conserved kidney. Hyrtl describes the arrangement
of the vascular trunks in the mesorchium in the following way (No. 11, p.
6): "The mesorchium contains vascular trunks, viz., veins, which through
their numerous anastomoses form a plexus at the hilus of the testis, whose
efferent trunks, 13 in number, again unite into a plexus on the vertebral
column, which is continuous with the cardinal veins." The arrangement
(though not the number) of Hyrtl's vessels is very similar to that of our
vasa efferentia, and we cannot help thinking that a confusion of the two
may have taken place; which, in badly conserved specimens, not injected
with semen, would be very easy.
We have, as already stated, been unable to find in our dissections any
trace of a duct homologous with the oviduct of the female, and our sections
through the kidney and its ducts equally fail to bring to light such a
duct. The kidney ducts are about 19 centims. in length, measured from the
genital aperture to their front end. These ducts are generally similar to
those in the female; they unite about 2 centims. from the genital pore to
form an unpaired vesicle. Their posterior parts are considerably enlarged,
forming what Hyrtl calls the horns of the urinary bladder. In these
enlarged portions, and in the wall of the unpaired urinary bladder,
numerous transverse partitions are present, as correctly described by
Hyrtl, which are similar to those in the female, but more numerous. They
give rise to a series of pits, at the blind ends of which are placed the
openings of the kidney tubules. The kidney duct without doubt serves as vas
deferens, and we have found in it masses of yellowish colour similar to the
substance in the vasa efferentia identified by us as remains of
spermatozoa.
II.--_Development._
In the general account of the development we have already called attention
to the earliest stages of the excretory system.
We may remind the reader that the first part of the system to be formed is
the segmental or archinephric duct (Plate 36, figs. 28 and 29, _sg._). This
duct arises, as in Teleostei and Amphibia, by the constriction of a hollow
ridge of the somatic mesoblast into a canal, which is placed in contiguity
with the epiblast, along the line of junction between the mesoblastic
somites and the lateral plates of mesoblast. Anteriorly the duct does not
become shut off from the body-cavity, and also bends inwards towards the
middle line. The inflected part of the duct is the first rudiment of the
pronephros, and very soon becomes considerably dilated relatively to the
posterior part of the duct.
The posterior part of each segmental duct acquires an opening into the
cloacal section of the alimentary tract. Apart from this change, the whole
of the ducts, except their pronephric sections, remain for a long time
unaltered, and the next changes we have to speak of concern the definite
establishment of the pronephros.
The dilated incurved portion of each segmental duct soon becomes
convoluted, and by the time the embryo is about 10 millims. in length, but
before the period of hatching, an important change is effected in the
relations of their peritoneal openings[539].
Footnote 539: The change is probably effected somewhat earlier
than would appear from our description, but our specimens were
not sufficiently well preserved to enable us to speak
definitely as to the exact period.
Instead of leading into the body-cavity, they open into an isolated chamber
on each side (Plate 38, fig. 51, _pr.c._), which we will call the
_pronephric chamber_. The pronephric chamber is not, however, so far as we
can judge, completely isolated from the body-cavity. We have not, it is
true, detected with certainty at this stage a communication between the
two; but in later stages, in larvæ of from 11 to 26 millims., we have found
a richly ciliated passage leading from the body-cavity into the pronephros
on each side (Plate 38, fig. 52, _p.f.p._). We have not succeeded in
determining with absolute certainty the exact relations between this
passage and the tube of the pronephros, but we are inclined to believe that
it opens directly into the pronephric chamber just spoken of.
As we hope to shew, this chamber soon becomes largely filled by a vascular
glomerulus. On the accomplishment of these changes, the pronephros is
essentially provided with all the parts typically present in a segment of
the mesonephros (woodcut, fig. 4). There is a peritoneal tube (_f_)[540],
opening into a vesicle (_v_); from near the neck of the peritoneal tube
there comes off a convoluted tube (_pr.n._), forming the main mass of the
pronephros, and ending in the segmental duct (_sd._).
Footnote 540: We feel fairly confident that there is only one
pronephric opening on each side, though we have no single
series of sections sufficiently complete to demonstrate this
fact with absolute certainty.
[Illustration: FIG. 4.
Diagrammatic views of the pronephros of _Lepidosteus_.
A, pronephros supposed to be isolated and seen from the side; B, section
through the vesicle of the pronephros and the ciliated peritoneal funnel
leading into it; _pr.n._, coiled tube of pronephros; _sd._, segmental or
archinephric duct; _f._, peritoneal funnel; _v._, vesicle of pronephros;
_bv._, blood vessel of glomerulus; _gl._, glomerulus.]
The different parts do not, however, appear to have the same morphological
significance as those in the mesonephros.
Judging from the analogy of Teleostei, the embryonic structure of whose
pronephros is strikingly similar to that of _Lepidosteus_, the two
pronephric chambers into which the segmental ducts open are constricted off
sections of the body-cavity.
With the formation of the convoluted duct opening into the isolated section
of the body-cavity we may speak of a definite pronephros as having become
established. The pronephros is placed, as can be made out in later stages,
on the level of the opening of the air-bladder into the throat.
The pronephros increases in size, so far as could be determined, by the
further convolution of the duct of which it is mainly formed; and the next
change of importance which we have noticed is the formation of a vascular
projection into the pronephric chamber, forming the glomerulus already
spoken of (vide woodcut, fig. 4, _gl._), which is similar to that of the
pronephros of Teleostei. We first detected these glomeruli in an embryo of
about 15 millims., some days after hatching (Plate 38, fig. 52, _gl._), but
it is quite possible that they may be formed considerably earlier.
In the same embryo in which the glomeruli were found we also detected for
the first time a _mesonephros_ consisting of a series of isolated segmental
or nephridial tubes, placed posteriorly to the pronephros along the dorsal
wall of the abdomen.
These were so far advanced at this stage that we are not in a position to
give any account of their mode of origin. They are, however, formed
independently of the segmental ducts, and in the establishment of the
junction between the two structures, there is no outgrowth from the
segmental duct to meet the segmental tubes. We could not at this stage find
peritoneal funnels of the segmental tubes, though we have met with them at
a later stage (Plate 38, fig. 53, _p.f._), and our failure to find them at
this stage is not to be regarded as conclusive against their existence.
A very considerable space exists between the pronephros and the foremost
segmental tube of the mesonephros. The anterior mesonephric tubes are,
moreover, formed earlier than the posterior.
In the course of further development, the mesonephric tubules increase in
size, so that there ceases to be an interval between them, the mesonephros
thus becoming a continuous gland. In an embryo of 26 millims. there was no
indication of the formation of segmental tubes to fill up the space between
the pronephros and mesonephros.
The two segmental ducts have united behind into an unpaired structure in an
embryo of 11 millims. This structure is no doubt the future unpaired
urinogenital chamber (Plate 39, figs. 58A, and 60, _bl._). Somewhat later,
the hypoblastic cloaca becomes split into two sections, the hinder one
receiving the coalesced segmental ducts, and the anterior remaining
continuous with the alimentary tract. The opening of the hinder one forms
the urinogenital opening, and that of the anterior the anus.
In an older larva of about 5.5 centims. the pronephros did not exhibit any
marked signs of atrophy, though the duct between it and the mesonephros was
somewhat reduced and surrounded by the trabecular tissue spoken of in
connection with the adult. In the region between the pronephros and the
front end of the fully developed part of the mesonephros very rudimentary
tubules had become established.
The latest stage of the excretory system which we have studied is in a
young Fish of about 11 centims. in length. The special interest of this
stage depends upon the fact that the ovary is already developed, and not
only so, but the formation of the oviducts has commenced, and their
condition at this stage throws considerable light on the obscure problem of
their nature in the Ganoids.
Unfortunately, the head of the young Fish had been removed before it was
put into our hands, so that it was impossible for us to determine whether
the pronephros was still present; but as we shall subsequently shew, the
section of the segmental duct, originally present between the pronephros
and the front end of the permanent kidney or mesonephros, has in any case
disappeared.
In addition to an examination of the excretory organs _in situ_, which
shewed little except the presence of the generative ridges, we made a
complete series of sections through the excretory organs for their whole
length (Plate 39, figs. 54-57).
Posteriorly these sections shewed nothing worthy of note, the excretory
organs and their ducts differing in no important particular from these
organs as we have described them in the adult, except in the fact that the
segmental ducts are not joined by the oviducts.
Some little way in front of the point where the two segmental ducts
coalesce to form the urinary bladder, the genital ridge comes into view.
For its whole extent, except near its anterior part (of which more
hereafter) this ridge projects freely into the body-cavity, and in this
respect the young Fish differs entirely from the adult. As shewn in Plate
39, figs. 56 and 57 (_g.r._), it is attached to the abdominal wall on the
ventral side of, and near the inner border of each kidney. The genital
ridge itself has a structure very similar to that which is characteristic
of young Elasmobranchii, and it may be presumed of young Fishes generally.
The free edge of the ridge is swollen, and this part constitutes the true
generative region of the ridge, while its dorsal portion forms the
supporting mesentery. The ridge itself is formed of a central stroma and a
germinal epithelium covering it. The epithelium is thin on the whole of the
inner aspect of the ridge, but, just as in Elasmobranchii, it becomes
greatly thickened for a band-like strip on the outer aspect. Here, the
epithelium is several layers deep, and contains numerous primitive germinal
cells (_p.o._).
Though the generative organs were not sufficiently advanced for us to
decide the point with certainty, the structure of the organ is in favour of
the view that this specimen was a female, and, as will be shewn directly,
there can on other grounds be no doubt that this is so. The large size of
the primitive germinal cells (primitive ova) reminded us of these bodies in
Elasmobranchii.
In the region between the insertion of the genital ridge (or ovary, as we
may more conveniently call it) and the segmental duct we detected the
openings of a series of peritoneal funnels of the excretory tubes (Plate
39, fig. 57, _p.f._), which clearly therefore persist till the young Fish
has reached a very considerable size.
As we have already said, the ovary projects freely into the body-cavity for
the greater part of its length. Anteriorly, however, we found that a lamina
extended from the free ventral edge of the ovary to the dorsal wall of the
body-cavity, to which it was attached on the level of the outer side of the
segmental duct. A somewhat triangular channel was thus constituted, the
inner wall of which was formed by the ovary, the outer by the lamina just
spoken of, and the roof by the strip of the peritoneum of the abdominal
wall covering that part of the ventral surface of the kidney in which the
openings of the peritoneal funnels of the excretory tubes are placed. The
structure of this canal will be at once understood by the section of it
shewn in Plate 39, fig. 55.
There can be no doubt that this canal is the commencing ovarian sack. On
tracing it backwards we found that the lamina forming its outer wall arises
as a fold growing upwards from the free edge of the genital ridge meeting a
downward growth of the peritoneal membrane from the dorsal wall of the
abdomen; and in Plate 39, fig. 56, these two laminæ may be seen before they
have met. Anteriorly the canal becomes gradually smaller and smaller in
correlation with the reduced size of the ovarian ridge, and ends blindly
nearly on a level with the front end of the excretory organs.
It should be noted that, owing to the mode of formation of the ovarian
sack, the outer side of the ovary with the band of thickened germinal
epithelium is turned towards the lumen of the sack; and thus the fact of
the ova being formed on the inner wall of the genital sack in the adult is
explained, and the comparison which we instituted in our description of the
adult between the inner wall of the genital sack and the free genital ridge
of Elasmobranchii receives its justification.
It is further to be noticed that, from the mode of formation of the ovarian
sack, the openings of the peritoneal funnels of the excretory organs ought
to open into its lumen; and if these openings persist in the adult, they
will no doubt be found in this situation.
Before entering on further theoretical considerations with reference to the
oviduct, it will be convenient to complete our description of the excretory
organs at this stage.
When we dissected the excretory organs out, and removed them from the body
of the young Fish, we were under the impression that they extended for the
whole length of the body-cavity. Great was our astonishment to find that
slightly in front of the end of the ovary both excretory organs and
segmental ducts grew rapidly smaller and finally vanished, and that what we
had taken to be the front part of the kidney was nothing else but a linear
streak of tissue formed of cells with peculiar granular contents supported
in a trabecular work (Plate 39, fig. 54). This discovery first led us to
investigate histologically what we, in common with previous observers, had
supposed to be the anterior end of the kidneys in the adult, and to shew
that they were nothing else but trabecular tissue with cells like that of
lymphatic glands. The interruption of the segmental duct at the
commencement of this tissue demonstrates that if any rudiment of the
pronephros still persists, it is quite functionless, in that it is not
provided with a duct.
III.--_Theoretical considerations._
There are three points in our observations on the urinogenital system which
appear to call for special remark. The first of these concerns the
structure and fate of the pronephros, the second the nature of the oviduct,
and the third the presence of vasa efferentia in the male.
Although the history we have been able to give of the pronephros is not
complete, we have nevertheless shewn that in most points it is essentially
similar to the pronephros of Teleostei. In an early stage we find the
pronephros provided with a peritoneal funnel opening into the body-cavity.
At a later stage we find that there is connected with the pronephros on
each side, a cavity--the pronephric cavity--into which a glomerulus
projects. This cavity is in communication on the one hand with the lumen of
the coiled tube which forms the main mass of the pronephros, and on the
other hand with the body-cavity by means of a richly ciliated canal
(woodcut, fig. 4, p. 817).
In Teleostei the pronephros has precisely the same characters, except that
the cavity in which the glomerulus is placed is without a peritoneal canal.
The questions which naturally arise in connection with the pronephros are:
(1) what is the origin of the above cavity with its glomerulus; and (2)
what is the meaning of the ciliated canal connecting this cavity with the
peritoneal cavity?
We have not from our researches been able to answer the first of these
questions. In Teleostei, however, the origin of this cavity has been
studied by Rosenberg[541] and Götte[542]. According to the account of the
latter, which we have not ourselves confirmed but which has usually been
accepted, the front end of the segmental duct, instead of becoming folded
off from the body-cavity, becomes included in a kind of diverticulum of the
body-cavity, which only communicates with the remainder of the body-cavity
by a narrow opening. On the inner wall of this diverticulum a projection is
formed which becomes a glomerulus. At this stage in the development of the
pronephros we have essentially the same parts as in the fully formed
pronephros of _Lepidosteus_, the only difference being that the passage
connecting the diverticulum containing the glomerulus with the remainder of
the body-cavity is short in Teleostei, and in _Lepidosteus_ forms a longish
ciliated canal. In Teleostei the opening into the body-cavity becomes soon
closed. If the above comparison is justified, and if the development of
these parts in _Lepidosteus_ takes place as it is described as doing in
Teleostei, there can, we think, be no doubt that the ciliated canal of
_Lepidosteus_, which connects the pronephric cavity with the body-cavity,
is a persisting communication between this cavity and the body-cavity; and
that _Lepidosteus_ presents in this respect a more primitive type of
pronephros than Teleostei.
Footnote 541: Rosenberg, _Untersuch. ueb. d. Entwick. d.
Teleostierniere_, Dorpat, 1867.
Footnote 542: Götte, _Entwick. d. Unke_, p. 826.
It may be noted that in _Lepidosteus_ the whole pronephros has exactly the
character of a single segmental tube of the mesonephros. The pronephric
cavity with its glomerulus is identical in structure with a malpighian
body. The ciliated canal is similar in its relations to the peritoneal
canal of such a segmental tube, and the coiled portion of the pronephros
resembles the secreting part of the ordinary segmental tube. This
comparison is no doubt an indication that the pronephros is physiologically
very similar to the mesonephros, and so far justifies Sedgwick's[543]
comparison between the two, but it does not appear to us to justify the
morphological conclusions at which he has arrived, or to necessitate any
modification in the views on this subject expressed by one of us[544].
Footnote 543: Sedgwick, "Early Development of the Wolffian
Duct and anterior Wolffian Tubules in the Chick; with some
Remarks on the Vertebrate Excretory System," _Quart. Journ. of
Micros. Science_, Vol. XXI., 1881.
Footnote 544: F. M. Balfour, _Comparative Embryology_,
Vol. II., pp. 600-603 [the original edition].
The genital ducts of Ganoids and Teleostei have for some time been a source
of great difficulty to morphologists; and any contributions with reference
to the ontogeny of these structures are of interest.
The essential point which we have made out is that the anterior part of the
oviduct of _Lepidosteus_ arises by a fold of the peritoneum attaching
itself to the free edge of the genital ridge. We have not, unfortunately,
had specimens old enough to decide how the posterior part of the oviduct is
formed; and although in the absence of such stages it would be rash in the
extreme to speak with confidence as to the nature of this part of the duct,
it may be well to consider the possibilities of the case in relation to
other Ganoids and Teleostei.
The simplest supposition would be that the posterior part of the genital
duct had the same origin as the anterior, _i.e._, that it was formed for
its whole length by the concrescence of a peritoneal fold with the genital
ridge, and that the duct so formed opened into the segmental duct.
The other possible supposition is that a true Müllerian duct--_i.e._, a
product of the splitting of the segmental duct--is subsequently developed,
and that the open end of this duct coalesces with the duct which has
already begun to be formed in our oldest larva.
In attempting to estimate the relative probability of these two views, one
important element is the relation of the oviducts of _Lepidosteus_ to those
of other Ganoids.
In all other Ganoids (vide Hyrtl, No. II) there are stated to be genital
ducts in both sexes which are provided at their anterior extremities with a
funnel-shaped mouth open to the abdominal cavity. At first sight,
therefore, it might be supposed that they had no morphological relationship
with the oviducts of _Lepidosteus_, but, apart from the presence of a
funnel-shaped mouth, the oviducts of _Lepidosteus_ are very similar to
those of Chondrostean Ganoids, being thin-walled tubes opening on a
projecting papilla into the dilated kidney ducts (horns of the urinary
bladder, Hyrtl). These relations seem to prove beyond a doubt that the
oviduct of _Lepidosteus_ is for its major part homologous with the genital
ducts of other Ganoids.
The relationship of the genital ducts to the kidney ducts in _Amia_ and
_Polypterus_ is somewhat different from that in the Chondrostei and
_Lepidosteus_. In _Amia_ the ureters are so small that they may be
described rather as joining the coalesced genital ducts than _vice versâ_,
although the apparent coalesced portion of the genital ducts is shewn to be
really part of the kidney ducts by receiving the secretion of a number of
mesonephric tubuli. In _Polypterus_ the two ureters are stated to unite,
and open by a common orifice into a sinus formed by the junction of the two
genital ducts, which has not been described as receiving directly the
secretion of any part of the mesonephros.
It has been usual to assume that the genital ducts of Ganoids are true
Müllerian ducts in the sense above defined, on the ground that they are
provided with a peritoneal opening and that they are united behind with the
kidney ducts. In the absence of ontological evidence this identification is
necessarily provisional. On the assumption that it is correct we should
have to accept the second of the two alternatives above suggested as to the
development of the posterior parts of the oviduct in _Lepidosteus_.
There appear to us, however, to be sufficiently serious objections to this
view to render it necessary for us to suspend our judgment with reference
to this point. In the first place, if the view that the genital ducts are
Müllerian ducts is correct, the true genital ducts of _Lepidosteus_ must
necessarily be developed at a later period than the secondary attachment
between their open mouths and the genital folds, which would, to say the
least of it, be a remarkable inversion of the natural order of development.
Secondly, the condition of our oldest larva shews that the Müllerian duct,
if developed later, is only split off from quite the posterior part of the
segmental duct; yet in all types in which the development of the Müllerian
duct has been followed, its anterior extremity, with the abdominal opening,
is split off from either the foremost or nearly the foremost part of the
segmental duct.
Judging from the structure of the adult genital ducts of other Ganoids they
must also be developed only from the posterior part of the segmental duct,
and this peculiarity so struck one of us that in a previous paper[545] the
suggestion was put forward that the true Ganoid genital ducts were perhaps
not Müllerian ducts, but enlarged segmental tubes with persisting abdominal
funnels belonging to the mesonephros.
Footnote 545: F. M. Balfour, "On the Origin and History of the
Urinogenital Organs of Vertebrates," _Journ. of Anat. and
Phys._, Vol. X., 1876 [This edition, No. VII].
If the possibility of the oviduct of _Lepidosteus_ not being a Müllerian
duct is admitted, a similar doubt must also exist as to the genital ducts
of other Ganoids, and we must be prepared to shew that there is a
reasonable ground for scepticism on this point. We would in this connexion
point out that the second of the two arguments urged against the view that
the genital duct of _Lepidosteus_ is not a Müllerian duct applies with
equal force to the case of all other Ganoids.
The short funnel-shaped genital duct of the Chondrostei is also very unlike
undoubted Müllerian ducts, and could moreover easily be conceived as
originating by a fold of the peritoneum, a slight extension of which would
give rise to a genital duct like that of _Lepidosteus_.
The main difficulty of the view that the genital ducts of Ganoids are not
Müllerian ducts lies in the fact that they open into the segmental duct.
While it is easy to understand the genesis of a duct from a folding of the
peritoneum, and also easy to understand how such a duct might lead to the
exterior by coalescing, for instance, with an abdominal pore, it is not
easy to see how such a duct could acquire a communication with the
segmental duct.
We do not under these circumstances wish to speak dogmatically, either in
favour of or against the view that the genital ducts of Ganoids are
Müllerian ducts. Their ontogeny would be conclusive on this matter, and we
trust that some of the anatomists who have the opportunity of studying the
development of the Sturgeon will soon let us know the facts of the case. If
there are persisting funnels of the mesonephric segmental tubes in adult
Sturgeons, some of them ought to be situated within the genital ducts, if
the latter are not Müllerian ducts; and naturalists who have the
opportunity ought also to look out for such openings.
The mode of origin of the anterior part of the genital duct of
_Lepidosteus_ appears to us to tell strongly in favour of the view, already
regarded as probable by one of us[546], that the Teleostean genital ducts
are derived from those of Ganoids; and if, as appears to us indubitable,
the most primitive type of Ganoid genital ducts is found in the
Chondrostei, it is interesting to notice that the remaining Ganoids present
in various ways approximations to the arrangement typically found in
Teleostei. _Lepidosteus_ obviously approaches Teleostei in the fact of the
ovarian ridge forming part of the wall of the oviduct, but differs from the
Teleostei in the fact of the oviduct opening into the kidney ducts, instead
of each pair of ducts having an independent opening in the cloaca, and in
the fact that the male genital products are not carried to the exterior by
a duct homologous with the oviduct. _Amia_ is closer to the Teleostei in
the arrangement of the posterior part of the genital ducts, in that the two
genital ducts coalesce posteriorly; while _Polypterus_ approaches still
nearer to the Teleostei in the fact that the two genital ducts and the two
kidney ducts unite with each other before they join; and in order to
convert this arrangement into that characteristic of the Teleostei we have
only to conceive the coalesced ducts of the kidneys acquiring an
independent opening into the cloaca behind the genital opening.
Footnote 546: F. M. Balfour, _Comparative Embryology_,
Vol. II., p. 605 [the original edition].
_The male genital ducts._--The discovery of the vasa efferentia in
_Lepidosteus_, carrying off the semen from the testis, and transporting it
to the mesonephros, and thence through the mesonephric tubes to the
segmental duct, must be regarded as the most important of our results on
the excretory system.
It proves in the first place that the transportation outwards of the
genital products of both sexes by homologous ducts, which has been hitherto
held to be universal in Ganoids, and which, in the absence of evidence to
the contrary, must still be assumed to be true for all Ganoids except
_Lepidosteus_, is a secondary arrangement. This conclusion follows from the
fact that in Elasmobranchii, &c., which are not descendants of the Ganoids,
the same arrangement of seminal ducts is found as in _Lepidosteus_, and it
must therefore have been inherited from an ancestor common to the two
groups.
If, therefore, the current statements about the generative ducts of Ganoids
are true, the males must have lost their vasa efferentia, and the function
of vas deferens must have been taken by the homologue of the oviduct,
presumably present in the male. The Teleostei must, moreover, have sprung
from Ganoidei in which the vasa efferentia had become aborted.
Considerable phylogenetic difficulties as to the relationships of Ganoidei
and Elasmobranchii are removed by the discovery that Ganoids were
originally provided with a system of vasa efferentia like that of
Elasmobranchii.
THE ALIMENTARY CANAL AND ITS APPENDAGES.
I.--_Anatomy._
Agassiz (No. 2) gives a short description with a figure of the viscera of
_Lepidosteus_ as a whole. Van der Hoeven has also given a figure of them in
his memoir on the air-bladder of this form (No. 8), and Johannes Müller
first detected the spiral valve and gave a short account of it in his
memoir (No. 13). Stannius, again, makes several references to the viscera
of _Lepidosteus_ in his anatomy of the Vertebrata, and throws some doubt on
Müller's determination of the spiral valve.
The following description refers to a female _Lepidosteus_ of 100.5
centims. (Plate 40, fig. 66).
With reference to the mouth and pharynx, we have nothing special to remark.
Immediately behind the pharynx there comes an elongated tube, which is not
divisible into stomach and oesophagus, and may be called the stomach
(_st._). It is about 44.6 centims. long, and gradually narrows from the
middle towards the hinder or pyloric extremity. It runs straight backwards
for the greater part of its length, the last 3.8 centims., however, taking
a sudden bend forwards. For about half its length the walls are thin, and
the mucous membrane is smooth; in the posterior half the walls are thick,
and the mucous membrane is raised into numerous longitudinal ridges. The
peculiar glandular structure of the epithelium of this part in the embryo
is shewn in Plate 40, fig. 62 (_st._). Its opening into the duodenum is
provided with a very distinct pyloric valve (_py._). This valve projects
into a kind of chamber, freely communicating with the duodenum, and
containing four large pits (_c´_), into each of which a group of pyloric
cæca opens. These cæca form a fairly compact gland (_c._) about 6.5
centims. long, which overlaps the stomach anteriorly, and the duodenum
posteriorly.
Close to the pyloric valve, on its right side, is a small papilla, on the
apex of which the bile duct opens (_b.d´_).
A small, apparently glandular, mass closely connected with the bile duct,
in the position in which we have seen the pancreas in the larva (Plate 40,
figs. 62 and 63, _p._), is almost certainly a rudimentary pancreas, like
that of many Teleostei; but its preservation was too bad for histological
examination. We believe that the pancreas of _Lepidosteus_ has hitherto
been overlooked.
The small intestine passes straight backwards for about 8 centims., and
then presents three compact coils. From the end of these a section, about 5
centims. long, the walls of which are much thicker, runs forwards. The
intestine then again turns backwards, making one spiral coil. This spiral
part passes directly, without any sharp line of demarcation, into a short
and straight tube, which tapers slightly from before backwards, and ends at
the anus. The mucous membrane of the intestine for about the first 3.5
centims. is smooth, and the muscular walls thin: the rest of the small
intestine has thick walls, and the mucous membrane is reticulated.
A short spiral valve (_sp.v._), with a very rudimentary epithelial fold,
making nearly two turns, begins in about the posterior half of the spiral
coil of the intestine, extending backwards for slightly less than half the
straight terminal portion of the intestine, and ending 4 centims. in front
of the anus. Its total length in one example was about 4.5 centims.
The termination of the spiral valve is marked by a slight constriction, and
we may call the straight portion of the intestine behind it the rectum
(_rc._).
The posterior part of the intestine, from the beginning of the spiral valve
to the anus, _is connected with the ventral wall of the abdomen by a
mesentery_.
The air-bladder (_a.b._) is 45 centims. long, and opens into the alimentary
canal by a slit-like aperture (_a.b´._) on the median dorsal line,
immediately behind the epipharyngeal teeth. Each lip of this aperture is
largely formed by a muscular cushion, thickest at its posterior end, and
extending about 6 millims. behind the aperture itself. A narrow passage is
bounded by these muscular walls, which opens dorsally into the air-bladder.
The air-bladder is provided with two short anterior cornua, and tapers to a
point behind: it shews no indication of any separation into two parts. A
strong band of connective tissue runs along the inner aspect of its whole
dorsal region, from which there are given off on each side--at intervals of
about 12 millims. anteriorly, gradually increasing to 18 millims.
posteriorly--bands of muscle, which pass outwards towards its side walls,
and then spread out into the numerous reticulations with which the
air-bladder is lined throughout. By the contraction of these muscles the
cavity of the air-bladder can doubtless be very much diminished.
The main muscular bands circumscribe a series of more or less complete
chambers, which were about twenty-seven in number on each side in our
example. The chambers are confined to the sides, so that there is a
continuous cavity running through the central part of the organ. The whole
organ has the characteristic structure of a simple lung.
The liver (_lr._) consists of a single elongated lobe, about 32 centims.
long, tapering anteriorly and posteriorly, the anterior half being on the
average twice as thick as the posterior half. The gall-bladder (_g.b._)
lies at its posterior end, and is of considerable size, tapering gradually
so as to pass insensibly into the bile duct. The hepatic duct (_hp.d._)
opens into the gall-bladder at its anterior end.
The spleen (_s._) is a large, compact, double gland, one lobe lying in the
turn of the intestine immediately above the spiral valve, and the other on
the opposite side of the intestine, so that the intestine is nearly
embraced between the two lobes.
II.--_Development._
We have already described in detail the first formation of the alimentary
tract so far as we have been able to work it out, and we need only say here
that the anterior and posterior ends of the canal become first formed, and
that these two parts gradually elongate, so as to approach each other; the
growth of the posterior part is, however, the most rapid. The junction of
the two parts takes place a very short distance behind the opening of the
bile duct into the intestine.
For some time after the two parts of the alimentary tract have nearly met,
the ventral wall of the canal at this point is not closed; so that there is
left a passage between the alimentary canal and the yolk-sack, which forms
a vitelline duct.
After the yolk-sack has ceased to be visible as an external appendage it
still persists within the abdominal cavity. It has, however, by this stage
ceased to communicate with the gut, so that the eventual absorption of the
yolk is no doubt entirely effected by the vitelline vessels. At these later
stages of development we have noticed that numerous yolk nuclei, like those
met with in Teleostei and Elasmobranchii[547], are still to be found in the
yolk.
Footnote 547: For a history of similar nuclei, vide _Comp.
Embryol._, Vol. II., chapters III. and IV.
It will be convenient to treat the history of sections of the alimentary
tract in front of and behind the vitelline duct separately. The former
gives rise to the pharyngeal region, the oesophagus, the stomach, and the
duodenum.
The pharyngeal region, immediately after it has become established, gives
rise to a series of paired pouches. These may be called the branchial
pouches, and are placed between the successive branchial arches. The first
or hyomandibular pouch, placed between the mandibular and hyoid arches, has
rather the character of a double layer of hypoblast than of a true pouch,
though in parts a slight space is developed between its two walls. It is
shewn in section in Plate 37, fig. 43 (_h.m._), from an embryo of about 10
millims., shortly before hatching. It does not appear to undergo any
further development, and, so far as we can make out, disappears shortly
after the embryo is hatched, without acquiring an opening to the exterior.
It is important to notice that this cleft, which in the cartilaginous
Ganoids and _Polypterus_ remains permanently open as the spiracle, is
rudimentary even in the embryo of _Lepidosteus_.
The second pouch is the hyobranchial pouch: its outer end meets the
epiblast before the larva is hatched, and a perforation is effected at the
junction of the two layers, converting the pouch into a visceral cleft.
Behind the hyobranchial pouch there are four branchial pouches, which
become perforated and converted into branchial clefts shortly after
hatching.
The region of the oesophagus following the pharynx is not separated from
the stomach, unless a glandular posterior region (vide description of
adult) be regarded as the stomach, a non-glandular anterior region forming
the oesophagus. The lumen of this part appears to be all but obliterated in
the stages immediately before hatching, giving rise for a short period to a
solid oesophagus like that of Elasmobranchii and Teleostei[548].
Footnote 548: Vide _Comp. Embryol._, Vol. II., pp. 50-63 [the
original edition].
From the anterior part of the region immediately behind the pharynx the
air-bladder arises as a dorsal unpaired diverticulum. From the very first
it has an elongated slit-like mouth (Plate 40, fig. 64, _a.b´._), and is
placed in the mesenteric attachment of the part of the throat from which it
springs.
We have first noticed it in the stages immediately after hatching. At first
very short and narrow, it grows in succeeding stages longer and wider,
making its way backwards in the mesentery of the alimentary tract (Plate
40, fig. 65, _a.b._). In the larva of a month and a half old (26 millims.)
it has still a perfectly simple form, and is without traces of its adult
lung-like structure; but in the larva of 11 centims. it has the typical
adult structure.
The stomach is at first quite straight, but shortly after the larva is
hatched its posterior end becomes bent ventralwards and forwards, so that
the flexure of its posterior end (present in the adult) is very early
established. The stomach is continuous behind with the duodenum, the
commencement of which is indicated by the opening of the bile duct.
The liver is the first-formed alimentary gland, and is already a compact
body before the larva is hatched. We have nothing to say with reference to
its development, except that it exhibits the same simple structure in the
embryo that it does in the adult.
A more interesting glandular body is the pancreas. It has already been
stated that in the adult we have recognized a small body which we believe
to be the pancreas, but that we were unable to study its histological
characters.
In the embryo there is a well-developed pancreas which arises in the same
position and the same manner as in those Vertebrata in which the pancreas
is an important gland in the adult.
We have first noticed the pancreas in a stage shortly after hatching (Plate
40, fig. 61, _p._). It then has the form of a funnel-shaped diverticulum of
the _dorsal_ wall of the duodenum, immediately behind the level of the
opening of the bile duct. From the apex of this funnel numerous small
glandular tubuli soon sprout out.
The similarity in the development of the pancreas in _Lepidosteus_ to that
of the same gland in Elasmobranchii is very striking[549].
Footnote 549: Vide F. M. Balfour, "Monograph on Development of
Elasmobranch Fishes," p. 226 [This edition, No. X., p. 454].
The pancreas at a later stage is placed immediately behind the end of the
liver in a loop formed by the pyloric section of the stomach (Plate 40,
fig. 62, _p._). During larval life it constitutes a considerable gland, the
anterior end of which partly envelopes the bile duct (Plate 40, fig. 63,
_p._).
Considering the undoubted affinities between _Lepidosteus_ and the
Teleostei, the facts just recorded with reference to the pancreas appear to
us to demonstrate that the small size and occasional absence (?) of this
gland in Teleostei is a result of the degeneration of this gland; and it
seems probable that the pancreas will be found in the larvæ of most
Teleostei. These conclusions render intelligible, moreover, the great
development of the pancreas in the Elasmobranchii.
We have first noticed the pyloric cæca arising as outgrowths of the
duodenum in larvæ of about three weeks old, and they become rapidly longer
and more prominent (Plate 40, fig. 62, _c._).
The portion of the intestine behind the vitelline duct is, as in all the
Vertebrata, at first straight. In Elasmobranchii the lumen of the part of
the intestine in which a spiral valve is present in the adult, very early
acquires a more or less semilunar form by the appearance of a fold which
winds in a long spiral. In _Lepidosteus_ there is a fold similar in every
respect (Plate 38, fig. 53, _sp.v._), forming an open spiral round the
intestine. This fold is the first indication of the spiral valve, but it is
relatively very much later in its appearance than in Elasmobranchii, not
being formed till about three weeks after hatching. It is, moreover, in
correlation with the small extent of the spiral valve of the adult,
confined to a much smaller portion of the intestine than in Elasmobranchii,
although owing to the relative straightness of the anterior part of the
intestine it is proportionately longer in the embryo than in the adult.
The similarity of the embryonic spiral valve of _Lepidosteus_ to that of
Elasmobranchii shews that Stannius' hesitation in accepting Müller's
discovery of the spiral valve in _Lepidosteus_ is not justified.