Views of the pronephros of LepidosteusDiagrammatic views of the pronephros ofLepidosteus.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.
Diagrammatic views of the pronephros ofLepidosteus.
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 ofLepidosteus, 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 (videwoodcut, fig. 4,gl.), which is similar to that of the pronephros of Teleostei. We first detected these glomeruli in an embryo of about 15millims., 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 amesonephrosconsisting 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 26millims.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 11millims.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 5.5centims.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 11centims.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 organsin 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 segmentalducts 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 peritoneumof 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 withpeculiar 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 thiscavity 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 ofLepidosteus, 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 inLepidosteusforms 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 inLepidosteustakes place as it is described as doing in Teleostei, there can, we think, be no doubt that the ciliated canal ofLepidosteus, which connects the pronephric cavity with the body-cavity, is a persisting communication between this cavity and the body-cavity; and thatLepidosteuspresents in this respect a more primitive type of pronephros than Teleostei.
It may be noted that inLepidosteusthe 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 atwhich he has arrived, or to necessitate any modification in the views on this subject expressed by one of us[544].
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 ofLepidosteusarises 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 ofLepidosteusto those of other Ganoids.
In all other Ganoids (videHyrtl,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 ofLepidosteus, but, apart from the presence of a funnel-shaped mouth, the oviducts ofLepidosteusare very similar to those of Chondrostean Ganoids, being thin-walled tubes opening on a projecting papilla into the dilated kidney ducts (horns of theurinary bladder, Hyrtl). These relations seem to prove beyond a doubt that the oviduct ofLepidosteusis for its major part homologous with the genital ducts of other Ganoids.
The relationship of the genital ducts to the kidney ducts inAmiaandPolypterusis somewhat different from that in the Chondrostei andLepidosteus. InAmiathe ureters are so small that they may be described rather as joining the coalesced genital ducts thanvice 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. InPolypterusthe 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 inLepidosteus.
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 ofLepidosteusmust 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.
If the possibility of the oviduct ofLepidosteusnot 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 ofLepidosteusis 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 ofLepidosteus.
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 ofLepidosteusappears 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.Lepidosteusobviously 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.Amiais closer to the Teleostei in the arrangement of the posterior part of the genital ducts, in that the two genital ducts coalesce posteriorly; whilePolypterusapproaches 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.
The male genital ducts.—The discovery of the vasa efferentia inLepidosteus, 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 exceptLepidosteus, is a secondary arrangement. This conclusion follows from the fact that in Elasmobranchii,&c., which are not descendants ofthe Ganoids, the same arrangement of seminal ducts is found as inLepidosteus, 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.
[537]Treatise on Comparative Embryology,Vol.I., p. 43 [the original edition].
[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.
[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.
[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.
[541]Rosenberg,Untersuch. ueb. d. Entwick. d. Teleostierniere, Dorpat, 1867.
[542]Götte,Entwick. d. Unke, p. 826.
[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.
[544]F. M. Balfour,Comparative Embryology,Vol.II.,pp.600-603 [the original edition].
[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].
[546]F. M. Balfour,Comparative Embryology,Vol.II., p. 605 [the original edition].
I.—Anatomy.
Agassiz (No.2) gives a short description with a figure of the viscera ofLepidosteusas a whole. Van der Hœven 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 ofLepidosteusin his anatomy of the Vertebrata, and throws some doubt on Müller's determination of the spiral valve.
The following description refers to a femaleLepidosteusof 100.5centims.(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 œsophagus, and may be called the stomach (st.). It is about 44.6centims.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 3.8centims., 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 6.5centims.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 ofLepidosteushas hitherto been overlooked.
The small intestine passes straight backwards for about 8centims., and then presents three compact coils. From the end of these a section, about 5centims.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 3.5centims.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 4centims.in front of the anus. Its total length in one example was about 4.5centims.
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 45centims.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 6millims.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 12millims.anteriorly, gradually increasing to 18millims.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 32centims.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.
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 œsophagus, 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 10millims., shortly before hatching. Itdoes 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 andPolypterusremains permanently open as the spiracle, is rudimentary even in the embryo ofLepidosteus.
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 œsophagus following the pharynx is not separated from the stomach, unless a glandular posterior region (videdescription of adult) be regarded as the stomach, a non-glandular anterior region forming the œsophagus. 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 œsophagus like that of Elasmobranchii and Teleostei[548].
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 (26millims.) it has still a perfectly simple form, and is without traces of its adult lung-like structure; but in the larva of 11centims.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 behindwith 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 thedorsalwall 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 inLepidosteusto that of the same gland in Elasmobranchii is very striking[549].
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 betweenLepidosteusand 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. InLepidosteusthere 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 ofLepidosteusto that of Elasmobranchii shews that Stannius' hesitation in accepting Müller's discovery of the spiral valve inLepidosteusis not justified.
J. Müller (Bau u. Entwick. d. Myxinoiden) holds that the so-called bursa entiana of Elasmobranchii (i.e., the chamber placed between the part of the intestine with the spiral valve and the end of the pylorus) is the homologue of the more elongated portion of the small intestine which occupies a similar position in the Sturgeon. This portion of the small intestine is no doubt homologous with the still more elongated and coiled portion of the small intestine inLepidosteusplaced between the chamber into which the pyloric cæca,&c., open and the region of the spiral valve. The fact that the vitelline duct in the embryoLepidosteusis placed close to the pyloric end of the stomach, and that the greater portion of the small intestine is derived from part of the alimentary canal behind this, shews that Müller is mistaken in attempting to homologise the bursa entiana of Elasmobranchii, which is placed in front of the vitelline duct, with the coiled part of the small intestine of the above forms. The latter is either derived from an elongation of the very shortportion of the intestine between the vitelline duct and the primitive spiral valve, or more probably by the conversion of the anterior part of the intestine, originally provided with a spiral valve into a coiled small intestine not so provided.
We have already called attention to the peculiar mesentery present in the adult attaching the posterior straight part of the intestine to the ventral wall of the body. This mesentery, which together with the dorsal mesentery divides the hinder section of the body-cavity into two lateral compartments is, we believe, a persisting portion of the ventral mesentery which, as pointed out by one of us[550], is primitively present for the whole length of the body-cavity. The persistence of such a large section of it as that found in the adultLepidosteusis, so far as we know, quite exceptional. This mesentery is shewn in section in the embryo in Plate 38, fig. 53 (v.mt.). The small vessel in it appears to be the remnant of the subintestinal vein.
[547]For a history of similar nuclei,videComp. Embryol.,Vol.II., chaptersIII.andIV.
[548]VideComp. Embryol.,Vol.II.,pp.50-63 [the original edition].
[549]VideF. M. Balfour,“Monograph on Development of Elasmobranch Fishes,”p. 226 [This edition,No.X., p.454].
[550]Comparative Embryology,Vol.II.p. 514 [the original edition].
It is well known thatLepidosteusis provided with a gill on the hyoid arch, divided on each side into two parts. An excellent figure of this gill is given by Müller (No.13, plate 5, fig. 6), who holds from a consideration of the vascular supply that the two parts of this gill represent respectively the hyoid gill and the mandibular gill (called by Müller pseudobranch). Müller's views on this subject have not usually been accepted, but it is the fashion to regard the whole of the gill as the hyoid gill divided into two parts. It appeared to us not improbable that embryology might throw some light on the history of this gill, and accordingly we kept a look out in our embryos for traces of gills on the hyoid and mandibular arches. The results we have arrived at are purely negative, but are not the less surprising for this fact. The hyomandibular cleft as shewn above, is never fully developed, and early undergoes a complete atrophy—a fact which is, on the whole, against Müller's view; but what astonished us most in connection with the gill in question is that we have beenunable to find any trace of it even in the oldest larva whose head we have had (26millims.), and at a period when the gills on the hinder arches have reached their full development.
We imagined the gill in question to be the remnant of a gill fully formed in extinct Ganoid types, and therefore expected to find it better developed in the larva than in the adult. That the contrary is the fact appears to us fairly certain, although we cannot at present offer any explanation of it.
A. Agassiz concludes his memoir on the development ofLepidosteusby pointing out that in spite of certain affinities in other directions this form is“not so far removed from the bony Fishes as has been supposed.”Our own observations go far to confirm Agassiz' opinion.
Apart from the complete segmentation, the general development ofLepidosteusis strikingly Teleostean. In addition to the general Teleostean features of the embryo and larva, which can only be appreciated by those who have had an opportunity of practically working at the subject, we may point to the following developmental features[551]as indicative of Teleostean affinities:—
(1) The formation of the nervous system as a solid keel of the epiblast.
(2) The division of the epiblast into a nervous and epidermic stratum.
(3) The mode of development of the gut (videpp.752-754).
(4) The mode of development of the pronephros; though, as shewn on p.822, the pronephros ofLepidosteushas primitive characters not retained by Teleostei.
(5) The early stages in the development of the vertebral column (videp.779).
In addition to these, so to speak, purely embryonic characters there are not a few important adult characters:—
(1) The continuity of the oviducts with the genital glands.
(2) The small size of the pancreas, and the presence of numerous so-called pancreatic cæca.
(3) The somewhat coiled small intestine.
(4) Certain characters of the brain,e.g., the large size of the cerebellum; the presence of the so-called lobi inferiores on the infundibulum; and of tori semicirculares in the mid-brain.
In spite of the undoubtedly important list of features to which we have just called attention, a list containing not less important characters, both embryological and adult, separatingLepidosteusfrom the Teleostei, can be drawn up:—
(1) The character of the truncus arteriosus.
(2) The fact of the genital ducts joining the ureters.
(3) The presence of vasa efferentia in the male carrying the semen from the testes to the kidney, and through the tubules of the latter into the kidney duct.
(4) The presence of a well-developed opercular gill.
(5) The presence of a spiral valve; though this character may possibly break down with the extension of our knowledge.
(6) The typical Ganoid characters of the thalamencephalon and the cerebral hemispheres (videpp.769and770).
(7) The chiasma of the optic nerves.
(8) The absence of a pecten, and presence of a vascular membrane between the vitreous humour and the retina.
(9) The opisthocœlous form of the vertebræ.
(10) The articulation of the ventral parts of the hæmal arches of the tail with processes of the vertebral column.
(11) The absence of a division of the muscles into dorso-lateral and ventro-lateral divisions.
(12) The complete segmentation of the ovum.
The list just given appears to us sufficient to demonstrate thatLepidosteuscannot be classed with the Teleostei; and we hold that Müller's view is correct, according to whichLepidosteusis a true Ganoid.
The existence of the Ganoids as a distinct group has, however, recently been challenged by so distinguished an Ichthyologist as Günther, and it may therefore be well to consider how far the group as defined by Müller is a natural one for livingforms[552], and how far recent researches enable us to improve upon Müller's definitions. In his classical memoir (No.13) the characters of the Ganoids are thus shortly stated:—
"These Fishes are either provided with plate-like angular or rounded cement-covered scales, or they bear osseous plates, or are quite naked. The fins are often, but not always, beset with a double or single row of spinous plates or splints. The caudal fin occasionally embraces in its upper lobe the end of the vertebral column, which may be prolonged to the end of the upper lobe. Their double nasal openings resemble those of Teleostei. The gills are free, and lie in a branchial cavity under an operculum, like those of Teleostei. Many of them have an accessory organ of respiration, in the form of an opercular gill, which is distinct from the pseudobranch, and can be present together with the latter; many also have spiracles like Elasmobranchii. They have many valves in the stem of the aorta like the latter, also a muscular coat in the stem of the aorta. Their ova are transported from the abdominal cavity by oviducts. Their optic nerves do not cross each other. The intestine is often provided with a spiral valve, like Elasmobranchii. They have a swimming-bladder with a duct, like many Teleostei. Their pelvic fins are abdominal.
“If we include in a definition only those characters which are invariable, the Ganoids may be shortly defined as being those Fish with numerous valves to the stem of the aorta, which is also provided with a muscular coat; with free gills and an operculum, and with abdominal pelvic fins.”
To these distinctive characters, he adds in an appendix to his paper, the presence of the spiral valve, and the absence of a processus falciformis and a choroid gland.
To the distinctive set of characters given by Müller we may probably add the following:—
(1) Oviducts and urinary ducts always unite, and open by a common urinogenital aperture behind the anus.
(2) Skull hyostylic.
(3) Segmentation complete in the types so far investigated, though perhapsAmiamay be found to resemble the Teleostei in this particular.
(4) A pronephros of the Teleostean type present in the larva.
(5) Thalamencephalon very large and well developed.
(6) The ventricle in the posterior part of the cerebrum is not divided behind into lateral halves, the roof of the undivided part being extremely thin.
(7) Abdominal pores always present.
The great number of characters just given are amply sufficient to differentiate the Ganoids as a group; but, curiously enough, the only characters amongst the whole series which have been given, which can be regarded as peculiar to the Ganoids, are (1) the characters of the brain, and (2) the fact of the oviducts and kidney ducts uniting together and opening by a common pore to the exterior.
This absence of characters peculiar to the Ganoids is an indication of how widely separated in organization are the different members of this great group.
At the same time, the only group with which existing Ganoids have close affinities is the Teleostei. The points they have in common with the Elasmobranchii are merely such as are due to the fact that both retain numerous primitive Vertebrate characters[553], and the gulf which really separates them is very wide.
There is again no indication of any close affinity between the Dipnoi and, at any rate, existing Ganoids.
Like the Ganoids, the Dipnoi are no doubt remnants of a very primitive stock; but in the conversion of the air-bladder into a true lung, the highly specialized character of their limbs[554], their peculiar autostylic skulls, the fact of their ventral nasal openings leading directly into the mouth, their multisegmented bars (interspinous bars), directly prolonged from the neural and hæmal arches and supporting the fin-rays of the unpaired dorsal and ventral fins, and their well-developed cerebral hemispheres,very unlike those of Ganoids and approaching the Amphibian type, they form a very well-defined group, and one very distinctly separated from the Ganoids.
No doubt the Chondrostean Ganoids are nearly as far removed from the Teleostei as from the Dipnoi, but the links uniting these Ganoids with the Teleostei have been so fully preserved in the existing fauna of the globe, that the two groups almost run into each other. If, in fact, we were anxious to make any radical change in the ordinary classification of Fishes, it would be by uniting the Teleostei and Ganoids, or rather constituting the Teleostei into one of the sub-groups of the Ganoids, equivalent to the Chondrostei. We do not recommend such an arrangement, which in view of the great preponderance of the Teleostei amongst living Fishes would be highly inconvenient, but the step fromAmiato the Teleostei is certainly not so great as that from the Chondrostei toAmia, and is undoubtedly less than that from the Selachii to the Holocephali.
[551]The features enumerated above are not in all cases confined toLepidosteusand Teleostei, but are always eminently characteristic of the latter.
[552]We do not profess to be able to discuss this question for extinct forms of Fish, though of course it is a necessary consequence of the theory of descent that the various groups should merge into each other as we go back in geological time.
[553]As instances of this we may cite (1) the spiral valve; (2) the frequent presence of a spiracle; (3) the frequent presence of a communication between the pericardium and the body-cavity; (4) the heterocercal tail.
[554]VideF. M. Balfour,“On the Development of the Skeleton of the Paired Fins of Elasmobranchii,”Proc. Zool. Soc., 1881 [This edition,No.XX.].
1.Agassiz, A.“The Development ofLepidosteus.”Part 1.,Proc. Amer. Acad.Arts and Sciences,Vol.XIV.1879.
2.Agassiz, L.Recherches s. l. Poissons Fossiles.Neuchatel. 1833-45.
3.Boas, J. E.“Ueber Herz u. Arterienbogen beiCeradotusu.Protopterus,”Morphol. Jahrbuch,Vol.VI.1880.
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6.Gegenbaur, C.“Zur Entwick. d. Wirbelsäule d.Lepidosteus,&c.”Jenaische Zeitschrift,Vol.III.1867.
7.Hertwig, O.“Ueber d. Hautskelet d. Fische (Lepidosteusu.Polypterus),”Morphol. Jahrbuch,Vol.V.1879.
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a.Anus.ab.Air-bladder.ab´.Aperture of air-bladder into throat.ac.Anterior commissure.af.Anal fin.al.Alimentary canal.ao.Aorta.ar.Artery.au.Auditory pit.b.Brain.bc.Body-cavity.bd.Bile duct.bd´.Aperture of bile duct into duodenum.bl.Coalesced portion of segmental ducts, forming urinogenital bladder.bra.Branchial arches.brc.Branchial clefts.c.Pyloric caæca.c´.Apertures of caæca into duodenum.cb.Cerebellum.cdv.Cardinal vein.ce.Cerebrum: in figs. 47A and B, anterior lobe of cerebrum.ce´.Posterior lobe of cerebrum.cf.Caudal fin.cn.Centrum.ch.Choroidal fissure.crv.Circular vein of vascular membrane of eye.csh.Cuticular sheath of notochord.cv.Caudal vein.d.Duodenum.dc.Dorsal cartilage of neural arch.df.Dermal fin-rays.dl.Dorsal lobe of caudal fin.dlf.Dorsal fin.e.Eye.ed.Epidermis.ep.Epiblast.fb.Fore-brain.fe.Pyriform bodies surrounding the zona radiata of the ovum, probably the remains of epithelial cells.gb.Gall-bladder.gd.Genital duct.gl.Glomerulus.gr.Genital ridge.h.Heart.ha.Hæmal arch.hb.Hind-brain.hc.Head-cavity.hpd.Hepatic duct.hm.Hyomandibular cleft.hop.Operculum.hy.Hypoblast; in fig. 10, hyoid arch.hyl.Hyaloid membrane.ic.Intercalated cartilaginous elements of the neural arches.in.Infundibulum.ir.Iris.is.Interspinous cartilage or bones.iv.subintestinal vein.ivr.Intervertebral ring of cartilage.k.Kidney.l.Lens.lc.Longitudinal canal, formed by union of the vasa efferentia.lin.Lobi inferiores.ll.Ligamentum longitudinale superius.lr.Liver.lt.Lateral line.ly.Lymphatic body in front of kidney.m.Mouth.mb.Mid-brain.mc.Medullary cord.mel.Membrana elastica externa.mes.Mesorchium.mn.Mandible.md.andmo.Medulla oblongata.ms.Mesoblast.na.Neural arch.na´.Dorsal element of neural arch.nc.Notochord.nve.Network formed by vasa efferentia on inner face of testis.od.Oviduct.od´.Aperture of oviduct into bladder.ol.Nasal pit or aperture.olf.Olfactory lobe.op.Optic vesicle.opch.Optic chiasma.opl.Optic lobes.opth.Optic thalami.orep.Oral epithelium.ov.Ovary.p.Pancreas.pc.Pericardium.pcf.Pectoral fin.pch.Pigmented layer of choroid.pf.Peritoneal funnel of segmental tube of mesonephros.pfp.Peritoneal funnel leading into pronephric chamber.pg.Pectoral girdle.plf.Pelvic fin.pn.Pineal gland.po.Primitive germinal cells.pr.Mesoblastic somite.prc.Pronephric chamber.prn.Pronephros.prn´.Opening of pronephros into pronephric chamber.pt.Pituitary body.py.Pyloric valve.pz.Parietal zone of blastoderm.r.Rostrum.rb.Rib.rc.Rectum.s.Spleen.sc.Seminal vessels passing from the longitudinal canal into the kidney.sd.Suctorial disc.sg.Segmental or archinephric duct.sgt.Segmental tubules.sh.Granular outer portion of the sheath of the notochord in the vertebral regions.smx.Superior maxillary process.snc.subnotochordal rod.so.Somatic mesoblast.sp.Splanchnic mesoblast.spn.Spinal nerve.spv.Spiral valve.st.Stomach.st.Seminal tubes of the testis.sup.Suctorial papillæ.t.Testis.th.Thalamencephalon.thl.Lobes of the roof of the thalamencephalon.tr.Trabeculæ.ug.Urinogenital aperture.v.Ventricle.ve.Vasa efferentia.vh.Vitreous humour.vl.Ventral lobe of the caudal fin.vmt.Ventral mesentery.vn.Vein.vs.Blood-vessel.vsh.Vascular sheath between the hyaloid membrane and the vitreous humour.vth.Vesicle of the thalamencephalon.x.Groove in epiblast, probably formed in process of hardening.y.Yolk.z.Commissure in front of pineal gland.zr.Outer striated portion of investing membrane (zona radiata) of ovum.zr´.Inner non-striated portion of investing membrane of ovum. I. Olfactory nerve. II. Optic nerve. III. Oculomotor nerve. V. Trigeminal nerve. VIII. Facial and auditory nerves.