[520]Vol.II.p. 414 [the original edition].
One of the most remarkable organs of the larvalLepidosteusis the suctorial disc, placed at the front end of the head, to which we have made numerous allusions in the first section of this memoir.
The external features of the disc have been fully dealt with by Agassiz, and he also explained its function by observations on the habits of the larva. We have already quoted (p.755) a passage from Agassiz' memoir shewing how the young Fishes use the disc to attach themselves firmly to any convenient object. The discs appear in fact to be highly efficient organs of attachment, in that the young Fish can remain suspended by them to the sides of the jar, even after the water has been lowered below the level at which they are attached.
The disc is formed two or three days before hatching, and from Agassiz' statements, it appears to come into use immediately the young Fish is liberated from the egg membranes.
We have examined the histological structure of the disc at various ages of its growth, and may refer the reader to Plate 34,figs. 11 and 13, and Plate 37, figs. 40 and 44. The result of our examination has been to shew that the disc is provided with a series of papillæ often exhibiting a bilateral arrangement. The papillæ are mainly constituted of highly modified cells of the mucous layer of the epidermis. These cells have the form of elongated columns, the nucleus being placed at the base, and the main mass of the cells being filled with a protoplasmic reticulum. They may probably be regarded as modified mucous cells. In the mesoblast adjoining the suctorial disc there are numerous sinus-like vascular channels.
It does not appear probable that the disc has a true sucking action. It is unprovided with muscular elements, and there appears to be no mechanism by which it could act as a sucking organ. We must suppose, therefore, that its adhesive power depends upon the capacity of the cells composing its papillæ to pour out a sticky secretion.
There is a peculiarity in the muscular system ofLepidosteus, which so far as we know has not been previously noticed. It is that the lateral muscles of each side are not divided, either in the region of the trunk or of the tail, into a dorso-lateral and ventro-lateral division.
This peculiarity is equally characteristic of the older larvæ as of the adult, and is shewn in Plate 41, figs. 67, 72, and 73, and Plate 42, figs. 74-76. In the Cyclostomata the lateral muscles are not divided into dorsal and ventral sections; but except in this group such a division has been hitherto considered as invariable amongst Fishes.
This character must, without doubt, be held to be the indication of a very primitive arrangement of the muscular system. In the embryos of all Fishes with the usual type of the lateral muscles, the undivided condition of the muscles precedes the divided condition; and in primitive forms such as the Cyclostomata and Amphioxus the embryonic condition is retained, as it is inLepidosteus.
Part I.—Vertebral column and ribs of the adult.
A typical vertebra from the trunk ofLepidosteushas the following characters (Plate 42, figs. 80 and 81).
The centrum is slightly narrower in the middle than at its two extremities. It articulates with adjacent vertebræ by a convex face in front and a concave face behind, being thus, according to Owen's nomenclature, opisthocœlous. It presents on its under surface a well-marked longitudinal ridge, which in many vertebræ is only united at its two extremities with the main body of the vertebra.
From the lateral borders of the centrum there project, at a point slightly nearer the front than the hind end, a pair of prominent hæmal processes (h.a.), to the ends of which are articulated the ribs. These processes have a nearly horizontal direction in the greater part of the trunk, though bent downwards in the tail.
The neural arches (n.a.) have a somewhat complicated form. They are mainly composed of two vertical plates, the breadth of the basal parts of which is nearly as great as the length of the vertebræ, so that comparatively narrow spaces are left between the neural arches of successive vertebræ for the passage of the spinal nerves. Some little way from its dorsal extremity each neural arch sends a horizontal process inwards, which meets its fellow and so forms a roof for the spinal canal. These processes appear to be confined to the posterior parts of the vertebræ, so that at the front ends of the vertebræ, and in the spaces between them, the neural canal is without an osseous roof. Above the level of this osseous roof there is a narrow passage, bounded laterally by the dorsal extremities of the neural plates. This passage is mainly filled up by a series of cartilaginous elements (Plate 42, figs. 80 and 81,i.c.) (probably fibro-cartilage), which rest upon the roof of the neural canal. Each element is situatedintervertebrally, its anterior end being wedged in between the two dorsal processes of the neural arch of the vertebra in front, and its posterior end extending for somedistance over the vertebra behind. The successive elements are connected by fibrous tissue, and are continuous dorsally with a fibrous band, known as the ligamentum longitudinale superius (Plate 42, figs. 80 and 81,l.l.), characteristic of Fishes generally, and running continuously for the whole length of the vertebral column. Each of the cartilaginous elements is, as will be afterwards shewn, developed as two independent pieces of cartilage, and might be compared with the dorsal element which usually forms the keystone of the neural arch in Elasmobranchii, were not the latter vertebral instead of intervertebral in position. More or less similar elements are described by Götte in the neural arches of many Teleostei, which also, however, appear to be vertebrally placed, and he has compared them and the corresponding elements in the Sturgeon with the Elasmobranch cartilages forming the keystone of the neural arch. Götte does not, however, appear to have distinguished between the cartilaginous elements, and the osseous elements forming the roof of the spinal canal, which are true membrane bones; it is probable that the two are not so clearly separated in other types as inLepidosteus.
The posterior ends of the neural plates of the neural arches are continued into the dorsal processes directed obliquely upwards and backwards, which have been somewhat unfortunately described by Stannius as rib-like projections of the neural arch. The dorsal processes of the two sides do not meet, but between them is placed a median free spinous element, also directed obliquely upwards and backwards, which forms a kind of roof for the groove in which the cartilaginous elements and the ligamentum longitudinale are placed.
The vertebræ are wholly formed of a very cellular osseous tissue, in which a distinction between the bases of the neural and hæmal processes and the remainder of the vertebra is not recognizable. The bodies of the vertebræ are, moreover, directly continuous with the neural and hæmal arches.
The ribs in the region of the trunk are articulated to the ends of the long hæmal processes. They envelop the body-cavity, their proximal parts being placed immediately outside the peritoneal membrane, along the bases of the intermuscular septa. Their distal ends do not, however, remain close to theperitoneal membrane,but pass outwards along the intermuscular septa till their free ends come into very close proximity with the skin. This peculiarity, which holds good in the adult for all the free ribs, is shewn in one of the anterior ribs of an advanced larva in Plate 41, fig. 72 (rb.). We are not aware that this has been previously noticed, but it appears to us to be a point not without interest in all questions which concern the homology of rib-like structures occupying different positions in relation to the muscles. Its bearings are fully dealt with in the section of this paper devoted to the consideration of the homologies of the ribs in Fishes.
As regards the behaviour of the ribs in the transitional region between the trunk and the tail, we cannot do better than translate the description given by Gegenbaur of this region (No.6, p. 411):—“Up to the 34th vertebra the ribs borne by the laterally and posteriorly directed processes present nothing remarkable, though they have gradually become shorter. The ribs of the 35th vertebra exhibit a slight curvature outwards of their free ends, a peculiarity still more marked in the 36th. The last named pair of ribs converge somewhat in their descent backwards so that both ribs decidedly approach before bending outwards. The 37th vertebra is no longer provided with freely terminating ribs, but on the contrary, the same pair of processes which in front was provided with ribs, bears a short forked process as the hæmal arch.The two, up to this point separated ribs, have here formed a hæmal arch by the fusion of their lower ends, which arch is movable just like the ribs, and, like them, is attached to the vertebral column.”
In the region of the tail-fin the hæmal arches supporting the caudal fin-rays are very much enlarged.
Part II.—Development of the vertebral column and ribs.
The first development and early histological changes of the notochord have already been given, and we may take up the history of the vertebral column at a period when the notochord forms a large circular rod, whose cells are already highly vacuolated, while the septa between the vacuoles form a delicatewide-meshed reticulum. Surrounding the notochord is the usual cuticular sheath, which is still thin.
The first indications of the future vertebral column are to be found in the formation of a distinct mesoblastic investment of the notochord. On the dorsal aspect of the notochord, the mesoblast forms two ridges, one on each side, which are prolonged upwards so as to meet above the neural canal, for which they form a kind of sheath. On the ventral side of the notochord there are also two ridges, which are, however, except on the tail, much less prominent than the dorsal ridges.
The changes which next ensue are practically identical with those which take place in Teleostei. Around the cuticular sheath of the notochord there is formed an elastic membrane—the membrana elastica externa. At the same time the basal parts of the dorsal, or as we may perhaps more conveniently call them, the neural ridges of the notochord become enlarged at each intermuscular septum, and the tissue of these enlargements soon becomes converted into cartilage, thus forming a series of independent paired neural processes riding on the membrana elastica externa surrounding the notochord, and extending about two-thirds of the way up the sides of the medullary cord. They are shewn in transverse section in Plate 41, fig. 67 (n.a.), and in a side view in fig. 68 (n.a.).
Simultaneously with the neural arches, the hæmal arches also become established, and arise by the formation of similar enlargements of the ventral or hæmal ridges. In the trunk they are very small, but in the region of the tail their condition is very different. At the front end of the anal fin the paired hæmal arches suddenly enlarge and extend ventralwards (Plate 41, fig. 67,h.a.).
Each succeeding pair of arches becomes larger than the one in front, and the two elements of each arch first nearly meet below the caudal vein (Plate 41, fig. 67) and finally actually do so, forming in this way a completely closed hæmal canal. At the point where they first meet the permanent caudal fin commences, and here (Plate 41, fig. 68) we find that not only do the hæmal arches meet and coalesce below the caudal vein, but they are actually produced into long spines supporting the fin-rays of the caudal fin, which thus differs from the other fins in beingsupported by parts of the true vertebral column and not by independently formed elements of the skeleton.
Each of the large caudal hæmal arches, including the spine, forms a continuous[TN18]whole, and arises at an earlier period of larval life than any other part of the vertebral column. We noticed the first indications of the neural arches in the larva of about a week old, while they are converted into fully formed cartilage in the larva of three weeks.
The neural and hæmal arches, resting on the membrana elastica externa, do not at this early stage in the least constrict the notochord. They grow gradually more definite, till the larva is five or six weeks old and about 26millims.in length, but otherwise for a long time undergo no important changes. During the same period, however, the true sheath of the notochord greatly increases in thickness, and the membrana elastica externa becomes more definite. So far it would be impossible to distinguish the development of the vertebral column ofLepidosteusfrom that of a Teleostean Fish.
Of the stages immediately following we have unfortunately had no examples, but we have been fortunate enough to obtain some young specimens ofLepidosteus[521], which have enabled us to work out with tolerable completeness the remainder of the developmental history of the vertebral column. In the next oldest larva, of about 5.5centims., the changes which have taken place are already sufficient to differentiate the vertebral column ofLepidosteusfrom that of a Teleostean, and to shew how certain of the characteristic features of the adult take their origin.
In the notochord the most important and striking change consists in the appearance of a series of very well marked vertebral constrictionsopposite the insertions of the neural and hæmal arches. The first constrictions of the notochord are thus, as in other Fishes, vertebral; and although, owing to the growth of the intervertebral cartilage, the vertebral constrictions are subsequently replaced by intervertebral constrictions, yet at the same time the primitive occurrence of vertebral constrictions demonstrates that the vertebral column ofLepidosteusis a modification of a type of vertebral column with biconcave vertebræ.
The structure of the gelatinous body of the notochord has undergone no important change. The sheath, however, exhibits certain features which deserve careful description. In the first place the attention of the observer is at once struck by the fact that, in the vertebral regions, the sheath is much thicker (.014millims.) than in the intervertebral (.005millims.), and a careful examination of the sheath in longitudinal sections shews that the thickening is due to the special differentiation of a superficial part (Plate 41, fig. 69,sh.) of the sheath in each vertebral region. This part is somewhat granular as compared to the remainder, especially in longitudinal sections. It forms a cylinder (the wall of which is about .01millim.thick) in each vertebral region, immediately within the membrana elastica externa. Between it and the gelatinous tissue of the notochord within there is a very thin unmodified portion of the sheath, which is continuous with the thinner intervertebral parts of the sheath. This part of the sheath is faintly, but at the same time distinctly, concentrically striated—a probable indication of concentric fibres. The inner unmodified layer of the sheath has the appearance in transverse sections through the vertebral regions of an inner membrane, and may perhaps be Kölliker's“membrana elastica interna.”
We are not aware that any similar modification of the sheath has been described in other forms.
The whole sheath is still invested by a very distinct membrana elastica externa (m.el).
The changes which have taken place in the parts which form the permanent vertebræ will be best understood from Plate 41, figs. 69-71. From the transverse section (fig. 70) it will be seen that there are still neural and hæmal arches resting upon the membrana elastica externa; but longitudinal sections (fig. 69) shew that laterally these arches join a cartilaginous tube, embracing the intervertebral regions of the notochord, and continuous from one vertebra to the next.
It will be convenient to treat separately the neural arches, the hæmal arches with their appendages, and the intervertebral cartilaginous rings.
The neural arches, except in the fact of embracing a relatively smaller part of the neural tube than in the earlier stage, do notat first sight appear to have undergone any changes. Viewed from the side, however, in dissected specimens, they are seen to be prolonged upwards so as to unite above with bars of cartilage directed obliquely backwards. An explanation of this appearance is easily found in the sections. The cartilaginous neural arches are invested by a delicate layer of homogeneous bone, developed in the perichondrium, and this bone is prolonged beyond the cartilage and joins a similar osseous investment of the dorsal bars above mentioned. The whole of these parts may, it appears to us, be certainly reckoned as parts of the neural arches, so that at this stage each neural arch consists of: (1) a pair of basal portions resting on the notochord consisting of cartilage invested by bone, (2) of a pair of dorsal cartilaginous bars invested in bone (n.a´.), and (3) of osseous bars connecting (1) and (2).
Though, in the absence of the immediately preceding stages, it is not perfectly certain that the dorsal pieces of cartilage are developed independently of the ventral, there appears to us every probability that this is so; and thus the cartilage of each neural arch is developed discontinuously, while the permanent bony neural arch, which commences as a deposit of bone partly in the perichondrium and partly in the intervening membrane, forms a continuous structure.
Analogous occurrences have been described by Götte in Teleostei.
The dorsal portion of each neural arch becomes what we have called the dorsal process of the adult arch.
Between the dorsal processes of the two sides there is placed a median rod of cartilage (Plate 41, fig. 70,i.s.), which in its development is wholly independent of the true neural arches, and which constitutes the median spinous element of the adult. In tracing these backwards it becomes obvious that they are homologous with the interspinous elements supporting the dorsal fin, in that they are replaced by these interspinous elements in the region of the dorsal fin, and that the interspinous bones occupy the same position as the median spinous processes. This homology was first pointed out by Götte in the case of the Teleostei.
Immediately beneath this rod is placed the longitudinalligament (Plate 41, fig. 70,l.l.), but there is as yet no trace of a junction between the neural arches of the two sides in the space between the longitudinal ligament and the spinal cord.
The basal parts of the neural arches of the two sides are united dorsally by a thin cartilaginous layer resting on the sheath of the notochord, but they are not united ventrally with the hæmal arches.
The hæmal processes in the trunk are much more prominent than in the preceding stage, and their bases are united ventrally by a tolerably thick layer of cartilage. In the trunk they are continuous with the so-called ribs of the adult (Plate 41, fig. 70); but in order to study the nature of these ribs it is necessary to trace the modifications undergone by the hæmal arches in passing from the tail to the trunk.
It will be remembered that at an earlier stage the hæmal arches in the region of the tail-fin were fully formed, and that through the anterior part of the caudal region the hæmal processes were far advanced in development, and just in front of the caudal fin had actually met below the caudal vein.
The mode of development of the hæmal arches in the tail asunjointedcartilaginous bars investing the caudal arteries and veins is so similar to that of the caudal hæmal arches of Elasmobranchii, that it appears to us impossible to doubt their identity in the two groups[522].
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 processeshave 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 thatthe ribs are originally continuous with the hæmal processes, and that the indications of a separation betweenthose 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 thatthe 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 sametime 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 11centims.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-markedintervertebralconstrictions, by the completion of which the vertebræ ofLepidosteusacquire 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, 0.18millim.
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 wehave 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 18centims.
The chief points in which the vertebral column of this larva differed from ours are: (1) the disappearance of all trace of theprimitive 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.
InLepidosteuswe 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 enlargementssoon 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 5½centims.), a series of very well-markedvertebralconstrictions 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 alsoin 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 (11centims.), 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 ofLepidosteuscaused 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 ofLepidosteusand 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.
InLepidosteusthis 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 inLepidosteusfor the origin of the amphibian type of vertebræ.
The researches which we have recorded demonstrate, however, in a very conclusive manner that the vertebræ ofLepidosteushave 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 opisthocœlous form of the vertebræ ofLepidosteusis 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.
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]maybe regarded as more especially the champion of the second view.
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.
It is admitted by both Gegenbaur and Götte that inLepidosteusthe 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 inLepidosteusthe 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 larvalLepidosteusthe 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 inLepidosteusand 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 inLepidosteusand other Ganoids they immediately girth the body-cavity.
Fig. 1.