XIX. THE SKULL
Three distinct sets of elements may enter into the composition of the skull. These are (1) the cranium proper, composed of true endoskeletal elements originally formed in cartilage, to which are usually added exoskeletal osseous elements, formed in the manner already described p. 542, and known in the higher types as membrane bones. (2) The visceral arches formed primitively as cartilaginous bars, but in the higher types largely supplemented or even replaced by exoskeletal elements. (3) The labial cartilages.
These parts present themselves in the most various forms, and their study constitutes one of the most important departments of vertebrate morphology, and one which has always been a favourite subject of study with anatomists. At the end of the last century and during the first half of the present century the morphology of the skull was handled from the point of view of the adult anatomy by Goethe, Oken, Cuvier, Owen, and many other anatomists, while Dugés and, nearer to our own time, Rathke, laid the foundation of an embryological study of its morphology. A new era in the study of the skull was inaugurated by Huxley in his Croonian lecture in 1858, and in his lectures on Comparative Anatomy subsequently delivered before the Royal College of Surgeons. In these lectures Huxley disproved the then widely accepted view that the skull was composed of four vertebræ; and laid the foundation of a more satisfactory method of dealing with the homologies of its constituent parts. Since then the knowledge of the development of the skull has made great progress. In this country a number of very interesting memoirs have been published on the subject by Parker, which together constitute a most striking contribution to our knowledge of the ontogeny of the skull in a series of types; and in Germany Gegenbaur's monograph on the cephalic skeleton of Elasmobranchii has greatly promoted a scientific appreciation of the nature of the skull.
In the present chapter only the most important features in the development of the skull will be touched on.
It will be convenient to describe, in the first instance, the development of the cartilaginous elements of the skull.
[FIG. 323. HEAD OF EMBRYO DOGFISH, SECOND STAGE; BASAL VIEW OF CRANIUM FROM ABOVE, THE CONTENTS HAVING BEEN REMOVED. (From Parker.)
ol. olfactory sacs; au. auditory capsule; nc. notochord; py. pituitary body; pa.ch. parachordal cartilage; tr. trabecula; inf. infundibulum; C.tr. cornua trabeculæ; pn. prenasal element; sp. spiracular cleft; br. external branchiæ; Cl. 2, 4. visceral clefts.]
The Cranium. The brain is at first enveloped in a continuous layer of mesoblast known as the membranous cranium, into the base of which the anterior part of the notochord is prolonged for some distance. The primitive cartilaginous cranium is formed by a differentiation within the membranous cranium, and is always composed of the following parts (fig. 323):
(1) A pair of cartilaginous plates on each side of the cephalic section of the notochord, known as the parachordals (pa.ch). These plates together with the notochord (nc) enclosed between them form a floor for the hind- and mid-brain. The continuous plate, formed by them and the notochord, is known as the basilar plate.
(2) A pair of bars forming the floor for the fore-brain, known as the trabeculæ (tr). These bars are continued forward from the parachordals. They meet behind and embrace the front end of the notochord; and after separating for some distance bend in again in such a way as to enclose a space--the pituitary space. In front of this space they remain in contact and generally unite. They extend forwards into the nasal region (pn).
(3) The cartilaginous capsules of the sense organs. Of these the auditory (au) and olfactory capsules (ol) unite more or less intimately with the cranial walls; while the optic capsules, forming the usually cartilaginous sclerotics, remain distinct.
The parachordals and notochord. The first of these sets of elements, viz. the parachordals and notochord, forming together the basilar plate, is always an unsegmented continuation of the axial tissue of the vertebral column. It forms the floor for that section of the brain which belongs to the primitive postoral part of the head (vide p. 314), and its extension is roughly that of the basioccipital of the adult skull. Its mode of development is almost identical with that of the vertebral column, except that the notochord, even in many forms where it persists in the vertebral column, disappears in the basilar plate; though in a certain number of cases remnants of it are found in the adult state.
It will be convenient to say a few words here with reference to the notochord in the head. It always extends along the floor of the mid- and hind-brains, but ends immediately behind the infundibulum. The limits of its anterior extension are clearly shewn in fig. 43. The front end of the notochord often becomes more or less ventrally flexed in correspondence with the cranial flexure; its anterior end being in some instances (Elasmobranchii) almost bent backwards (fig. 324).
Kölliker has shewn that in the Rabbit[203], and I believe that a more or less similar phenomenon may also be observed in Birds, the anterior end of the notochord is united to the hypoblast of the throat in immediate contiguity with the opening of the pituitary body; but it is not clear whether this is to be looked upon as the remnant of a primitive attachment of the notochord to the hypoblast, or as a secondary attachment.
[203] "Embryologische Mittheilungen." Festschrift d. Naturfor. Gesell., Halle, 1879.
[FIG. 324. LONGITUDINAL SECTION THROUGH THE BRAIN OF A YOUNG PRISTIURUS EMBRYO.
cer. commencement of the cerebral hemisphere; pn. pineal gland; In. infundibulum; pt. ingrowth from mouth to form the pituitary body; mb. mid-brain; cb. cerebellum; ch. notochord; al. alimentary tract; Iaa. artery of mandibular arch.]
Before the parachordals are formed the anterior end of the notochord has usually undergone a partial atrophy; and its front end often becomes somewhat dorsally flexed. Within the basilar plate it often exhibits two or more dilatations, which have been regarded by Parker and Kölliker as indicative of a segmentation of this plate; but they hardly appear to me to be capable of this interpretation.
In Elasmobranchs where, as shewn above, a very primitive type of development of the vertebral column is retained, we find that the basilar plate is at first formed of (1) the notochord invested by its cartilaginous sheath, and (2) of lateral masses of cartilage, the parachordals, homologous with the arch tissue of the vertebral column. This development probably indicates that the basilar plate contains in itself the same elements as those from which the neural arches and the centra of the vertebral column are formed; but that it never passes beyond the unsegmented stage at first characteristic of the vertebral column. The hinder end of each parachordal forms a condyle articulating with the first vertebra; so that in the cartilaginous skull there are always two occipital condyles. The basilar plate always grows up behind (fig. 326, so), and gives rise to a complete cartilaginous ring enveloping the medulla oblongata, in the same manner that the neural arches envelope the spinal cord. This ring forms an occipital cartilaginous ring; in front of it the basilar plate becomes laterally continuous with the periotic cartilaginous capsules, and the occipital ring above usually spreads forward to form a roof for the part of the brain between these capsules. In the higher Vertebrates the periotic cartilages may be developed continuously with the basilar plate (fig. 325).
The trabeculæ. The trabeculæ, so far as their mere anatomical relations are concerned, play the same part in forming the floor for the front cerebral vesicle as the parachordals for the mid- and hind-brains. They differ however from the parachordals in one important feature, viz. that, except at their hinder end (fig. 323), they do not embrace between them the notochord.
The notochord constitutes, as we have seen, the primitive axial skeleton of the body, and its absence in the greater part of the region of the trabeculæ would probably seem to indicate, as pointed out by Gegenbaur, that these parts, in spite of their similarity to the parachordals, have not the same morphological significance.
[FIG. 325. VIEW FROM ABOVE OF THE INVESTING MASS AND OF THE TRABECULÆ OF A CHICK ON THE FOURTH DAY OF INCUBATION. (After Parker.)
In order to shew this, the whole of the upper portion of the head has been sliced away. The cartilaginous portions of the skull are marked with the dark horizontal shading.
cv 1. cerebral vesicle (sliced off); e. eye; nc. notochord; iv. investing mass; 9. foramen for the exit of the ninth nerve; cl. cochlea; hsc. horizontal semicircular canal; q. quadrate; 5. notch for the passage of the fifth nerve; lg. expanded anterior end of the investing mass; pts. pituitary space; tr. trabeculæ. The reference line tr. has been accidentally made to end a little short of the cartilage.]
The nature of the trabeculæ has been much disputed by morphologists. The view that they cannot be regarded as the anterior section of the vertebral axis is supported by the consideration that the forward limit of the primitive skeletal axis, as marked by the notochord, coincides exactly with the distinction we have found it necessary to recognise, on entirely independent grounds, between the fore-brain, and the remainder of the nervous axis. But while this distinction between the parachordals and the trabeculæ must I think be admitted, I see no reason against supposing that the trabeculæ may be plates developed to support the floor of the fore-brain, for the same physiological reasons that the parachordals have become formed at the sides of the notochord to support the floor of the hind-brain. By some anatomists the trabeculæ have been held to be a pair of branchial bars; but this view has now been generally given up. They have also been regarded as equivalent to a complete pair of neural arches enveloping the front end of the brain. The primitive extension of the base of the fore-brain through the pituitary space is an argument, not without force, which has been appealed to in support of this view.
In the majority of the lower forms the trabeculæ arise quite independently of the parachordals, though the two sets of elements soon unite; while in Birds (fig. 325) and Mammals the parachordals and trabeculæ are formed as a continuous whole. The junction between the trabeculæ and parachordals becomes marked by a cartilaginous ridge known as the posterior clinoid.
[FIG. 326. SIDE VIEW OF THE CARTILAGINOUS CRANIUM OF A FOWL ON THE SEVENTH DAY OF INCUBATION. (After Parker.)
pn. prenasal cartilage; aln. alinasal cartilage; ale. aliethmoid; immediately below this is the aliseptal cartilage. eth. ethmoid; pp. pars plana; ps. presphenoid or interorbital; pa. palatine; pg. pterygoid; z. optic nerve; as. alisphenoid; q. quadrate; st. stapes; fr. fenestra rotunda; hso. horizontal semicircular canal; psc. posterior vertical semicircular canal: both the anterior and the posterior semicircular canals are seen shining through the cartilage. so. supraoccipital; eo. exoccipital; oc. occipital condyle; nc. notochord; mk. Meckel's cartilage; ch. ceratohyal; bh. basihyal; cbr. and ebr. ceratobranchial; bbr. basibranchial.]
The trabeculæ are usually somewhat lyre-shaped, meeting in front and behind, and leaving a large pituitary space between their middle parts (figs. 323 and 325). Into this space there primitively projects the whole base of the fore-brain, but the space itself gradually becomes narrowed, till it usually contains only the pituitary body. The carotid arteries always pass through it in the embryo; but in the higher forms it ceases to be perforated in the adult. The trabeculæ soon unite together both in front and behind and form a complete plate underneath the fore-brain, and extending into the nasal region[204]. A special vertical growth of this plate in the region of the orbit forms the interorbital plate of Teleostei, Lacertilia and Aves (fig. 326, ps), on the upper surface of which the front part of the brain rests. The trabecular floor of the brain does not long remain simple. Its sides grow vertically upwards, forming a lateral wall for the brain, in which in the higher types two regions may be distinguished, viz. an alisphenoidal region (fig. 326, as) behind, growing out from what is known as the basisphenoidal region of the primitive trabeculæ, and an orbitosphenoidal region in front growing out from the presphenoidal region of the trabeculæ. These plates form at first a continuous lateral wall of the cranium. At the front end of the brain they are continued inwards, and more or less completely separate the true cranial cavity from the nasal region in front. The region of the cartilage forming the anterior boundary of the cranial cavity is known as the lateral ethmoid region, and it is always perforated for the passage of the olfactory nerves.
[204] In Man (Kölliker) the trabeculæ form from the first a continuous plate in front of the pituitary space, and the latter very early acquires a cartilaginous floor.
The cartilaginous walls which grow up from the trabecular floor of the cranium generally extend upwards so as to form a roof, though almost always an imperfect roof, for the cranial cavity. In the higher types, in Mammals more especially, this roof can hardly be said to be formed at all. The region of the trabeculæ in front of the brain is the ethmoid region. The basal part of this region forms an internasal plate, from which an internasal septum may grow up (fig. 326). To its sides the olfactory capsules are attached, and there are usually lateral outgrowths in front forming the trabecular cornua, while from the posterior part of the ethmoidal plate, forming the anterior boundary of the cranial cavity, there often grows out a prefrontal or lateral ethmoidal process.
These and other processes growing out from the trabeculæ have occasionally been regarded as rudimentary præoral branchial arches. I have already stated it as my view that the existence of branchial arches in this region is highly improbable, and I may add that the development of these structures as outgrowths of the skull is in itself to my mind a nearly conclusive argument against their being branchial arches, in that true branchial arches hardly ever or perhaps never arise in this way.
The sense capsules. The most important of these is the auditory capsule, which, as we have seen, fuses intimately with the lateral walls of the skull. In front there is usually a cleft separating it from the alisphenoid region of the skull, through which the third division of the fifth nerve passes out. This cleft becomes narrowed to a small foramen (fig. 327, V). The sclerotic cartilage is always free, but profoundly modifies the region of the cranium near which it is placed. The nasal investment forms in Elasmobranchs (fig. 327, Na) a capsule open below, and continuous with the ethmoid region of the trabeculæ. In most types however it becomes more closely united with the ethmoid region and the accessory parts belonging to it.
[FIG. 327. SKULL OF ADULT DOGFISH, SIDE VIEW. (From Parker.)
O.C. occipital condyle; Au. periotic capsule; Pt.O. pterotic ridge; Sp.O. sphenotic process; S.Or. supraorbital ridge; Na. nasal capsule; P.N. prenasal cartilage; II. optic foramen; V. trigeminal foramen; Pl.Pt., Qu. pterygo-quadrate arcade; M.Pt. metapterygoid ligament (including a small cartilage); Pl.Tr. ethmo-palatine or palato-trabecular ligament; Mck. lower jaw; Sp. spiracle; H.M. hyomandibular; C.Hy. ceratohyal; m.h.l. mandibulohyoid ligament; Ph.Br. pharyngobranchial; E.Br. epibranchial; C.br. ceratobranchial; H.Br. hypobranchial; B.Br. basibranchial; Ex.Br. extra-branchial; l^1, [^2], [^3], [^4], [^5]. labial cartilages; the dotted lines within Mck. indicate the basihyal.]
The cartilaginous cranium, the development of which has been thus briefly traced, persists in the adult without even the addition of membrane bones in the Cyclostomata, Elasmobranchii (fig. 327) and Holocephali. In the Selachioid Ganoids it is also found in the adult, but is covered over by membrane bones. In all other types it is invariably present in the embryo, but becomes in the adult more or less replaced by osseous tissue.
Branchial skeleton.
The most primitive type of branchial skeleton in any existing form would appear to be that of the Petromyzonidæ, which is developed in a superficial subdermal tissue, and consists of a series of bars united by transverse pieces, so as to form a basketwork. It is known as an extra-branchial system, and an early stage of its development in the Lamprey is shewn in fig. 47. In the higher forms this system is replaced by a series of bars, known as the branchial bars, so situated as to afford support to the successive branchial pouches. Outside these bars there may be present in some primitive forms (Elasmobranchii) cartilaginous elements, which are supposed to be remnants of the extra-branchial system (fig. 327, Ex.Br); while a series of membrane bones is also usually added to them, which will be dealt with in a separate section. The branchial bars are developed as simple cartilaginous rods in the deeper parts of the mesoblast which constitutes the primitive branchial arches.
The position of the branchial bars in relation to the somatopleure and splanchnopleure can be determined from their relation to the so-called head cavities. These cavities atrophy before the formation of the cartilaginous branchial bars, but it will be observed (fig. 328), that the artery of each arch (aa) is placed on the inner side of the head cavity (pp). The cartilaginous bar arises at a later period on the inner side of the artery, and therefore on the inner side of the section of the body cavity primitively present in the arches.
An anterior arch, known as the mandibular arch, placed in front of the hyomandibular cleft, and a second arch, known as the hyoid arch, placed in front of the hyobranchial cleft, are developed in all types. The succeeding arches are known as the true branchial arches, and are only fully developed in the Ichthyopsida.
In some Sharks (Notidani) seven branchial arches may be present (not including the hyoid and mandibular). In other Ichthyopsida five are usually present, in the embryo at any rate, while in the Amniota there are usually two or three post-hyoid membranous arches, in the interior of which a cartilaginous bar is usually formed. The general form of these bars at an early stage of development is shewn in the dogfish (Scyllium) in fig. 329.
The simple condition of these bars in the embryo renders it highly probable that forms existed at one time with a simple branchial skeleton of this kind: at the present day however such forms no longer exist. The first arch has in all cases changed its function and has become converted into a supporting skeleton for the mouth; the hyoid arch, though retaining in some forms its branchial function, has in most acquired additional functions and has undergone in consequence various peculiar modifications. The true branchial arches retain their branchial functions in Pisces and some Amphibia, but are secondarily modified and largely aborted in the abranchiate forms. Since the changes undergone by the true branchial bars are far less complicated than those of the hyoid and mandibular bars it will be convenient to treat of them in the first instance.
[FIG. 328. HORIZONTAL SECTION THROUGH THE PENULTIMATE VISCERAL ARCH OF AN EMBRYO OF PRISTIURUS.
ep. epiblast; vc. pouch of hypoblast which will form the walls of a visceral cleft; pp. segment of body-cavity in visceral arch; aa. aortic arch.]
[FIG. 329. HEAD OF EMBRYO DOGFISH, 11 LINES LONG. (From Parker.)
Tr. trabecula; Pl.Pt. pterygo-quadrate; M.Pt. metapterygoid region; Mn. mandibular cartilage; Hy. hyoid arch; Br. 1. first branchial arch; Sp. mandibulohyoid cleft; Cl^1. hyobranchial cleft; Lch. groove below the eye; Na. olfactory rudiment; E. eyeball; Au. auditory mass; C 1, 2, 3. cerebral vesicles; Hm. hemispheres; f.n.p. nasofrontal process.]
These bars are, as already mentioned, most numerous in certain very primitive forms (seven in Notidanus), while as we ascend the series there is a gradual tendency for the posterior of them to disappear. This tendency is the result of a gradual atrophy of the posterior branchial pouches, which commenced at a stage in the evolution of the Chordata long prior to the appearance of cartilaginous or osseous branchial bars, and reaches its climax in the Amniota.
In a fully developed branchial bar the primitively simple rod of cartilage becomes divided into a series of segments, usually four, articulated so as to be more or less mobile: and either remaining cartilaginous or becoming partially or wholly ossified. Each bar (fig. 327) forms a somewhat curved structure, embracing the pharynx. The dorsal and somewhat horizontally placed segment is known as the pharyngobranchial (Ph.Br), the next two as the epibranchial (E.Br) and ceratobranchial (C.Br), and the ventral segment as the hypobranchial (H.Br). There is also typically present a basal unpaired segment, uniting the bars of the two sides, known as the basibranchial (B.Br). The arches often bear cartilaginous rays which support the gill lamellæ.
In Teleostei dental plates are usually developed as an exoskeletal covering on parts of the branchial arches.
In the Amphibia four or three branchial arches are present in the embryo. These parts are more or less completely retained in the Perennibranchiata and Caducibranchiata, but in the Myctodera and Anura they become largely reduced, and entirely connected with the hyoid.
In the Anura they never reach any considerable development, and are soon reduced to a plate (fig. 330)--the coalesced basihyal and basibranchial plate--the posterior processes of which represent the remnants of the branchial arches.
According to Parker the posterior process of this plate in the adult is a remnant of the fourth branchial bar; the next one is the third branchial bar, while the anterior lamina behind the hyoid is stated by him (though this is somewhat doubtful) to be a remnant of the first two bars.
[FIG. 330. YOUNG FROG, WITH TAIL JUST ABSORBED; SIDE VIEW OF SKULL. (From Parker.)
Au. auditory capsule; in front of it is the cranial side wall; A.N. external nostril; St. stapes; Mck. Meckelian cartilage; B.Hy. basihyobranchial plate; St.Hy. stylohyal or ceratohyal; Br. 1. first branchial arch.
Bones: E.O. exoccipital; Pr.O. prootic; Pa. parietal; Fr. frontal; Na. nasal; Pmx. premaxillary; Mx. maxillary; Pt. pterygoid; Sq. squamosal; Qu.Ju. quadratojugal; Art. articular; D. dentary.]
In the Amniota, the branchial arches become still more degenerated, in correlation with the total disappearance of a branchial respiration at all periods of life. Their remnants become more or less important parts of the hyoid bone, and are solely employed in support of the tongue. Their basal portions are best preserved, forming parts of the body of the hyoid. The posterior (thyroid) cornua of the hyoid are remnants of the true arches. Of these there are two in the Chelonia and Lacertilia, and one in the Aves and Mammalia. In Aves the cornu formed from the first branchial arch (fig. 331, cbr) is always larger than that of the true hyoid arch (ch).
Mandibular and Hyoid arches. The adaptations of both the mandibular and hyoid bars, to functions entirely distinct from those which they primitively served, are most remarkable; and the adaptations of the two bars are in many cases so intimately bound together, that it is not possible to treat them separately.
[FIG. 331. VIEW FROM BELOW OF THE BRANCHIAL SKELETON OF THE SKULL OF A FOWL ON THE FOURTH DAY OF INCUBATION. (After Parker.)
cv 1. cerebral vesicles; e. eye; fn. frontonasal process; n. nasal pit; tr. trabeculæ; pts. pituitary space; mr. superior maxillary process; pg. pterygoid; pa. palatine; q. quadrate; mk. Meckel's cartilage; ch. ceratohyal; bh. basihyal; cbr. ceratobranchial; ebr. proximal portion of the cartilage in the third visceral (first branchial) arch; bbr. basibranchial; 1. first visceral cleft; 2. second visceral cleft; 3. third visceral arch.]
The most important change of function is undoubtedly that of the mandibular arch, which becomes entirely converted into a skeleton for the jaws. It may be noted as a peculiarity of the mandibular arch that it is never provided with an unpaired basal element.
The simplest forms of metamorphosis are those undergone by Elasmobranchii, of which the Dogfish (Scyllium) and Skate (Raja) have been studied (Parker, No. 456). In some of these forms, e.g. the Skate, part of the mandibular bar is still related to the hyomandibular cleft (the spiracle).
Elasmobranchii. In Scyllium the hyoid and mandibular arches are at first very similar to those which follow. Soon however each of them sends an anteriorly directed dorsal process (fig. 329). The regions which may be distinguished owing to the growth of these processes have received names from ossifications in them which are found in other types. The anterior process of the mandibular arch is known as the pterygo-quadrate bar (Pl.Pt); the dorsal end of the primitive bar from which it starts (M.Pt) is known as the metapterygoid process; while the ventral end of the bar forms the Meckelian cartilage. The upper end of the hyoid arch is known as the hyomandibular.
In a somewhat later stage changes take place which cause these parts practically to assume the adult form (fig. 327). The mandibular arch becomes segmented at its bend into (1) a pterygo-quadrate bar (Pl.Pt) which grows forwards in front of the mouth and forms an upper jaw, and (2) a Meckelian cartilage (Mck) which is placed behind the mouth, and forms a lower jaw. The two jaws are articulated together, and the cartilages of the two sides composing them meet each other distally.
At the articulation of the Meckelian cartilage with the quadrate part of the pterygo-quadrate is situated a ligament (M.Pt), which takes the place of the metapterygoid process of the previous stage, and passes up on the anterior side of the spiracle, to be attached to the cranium in the front part of the auditory region. This ligament, which is supplemented by a second ligament, the ethmo-palatine ligament, passing from the pterygo-quadrate bar to the antorbital region of the skull, is not the most important support of the jaw. The main support is, on the contrary, given by the hyoid arch; the hyomandibular segment of which (H.M) as well as the adjoining segment (ceratohyoid C.Hy) are firmly attached by ligament to the mandibular arch. The hyomandibular is articulated with the cranium beneath the pterotic ridge (Pt.O).
In the type just described, the hyoid and mandibular arches undergo less modification than in almost any other case. The hyoid arch has altered its form, but retains its respiratory function. It has however acquired the secondary function of supporting the mandibular arch. The mandibular arch is divided into two elements, which form respectively the upper and lower jaws. It is not directly articulated with the skull, and its mode of support by the hyoid arch has been called by Huxley (No. 445) hyostylic.
[FIG. 333. HEAD OF EMBRYO SKATE, 1-1/3 IN. LONG. (From Parker.)
Tr. trabecula; Pl.Pt. pterygo-quadrate bar; Mn. mandibular bar; M.Pt. metapterygoid cartilage; H.M. hyomandibular; Hy. remainder of hyoid arch; Br. 1. first branchial arch; Sp. mandibulohyoid cleft or spiracle; Pn. pineal gland; Au. auditory vesicle; C. 1, C. 2, and C. 3. vesicles of the brain.]
The development of the hyoid and mandibular arches in the Skate is characterised by a few important features (fig. 333). The anterior element of the hyoid arch, which forms the hyomandibular (H.M), becomes entirely separate from the posterior part of the arch, and only serves to support the jaws. The posterior part of the arch (Hy) carries on the respiratory functions of the hyoid, and is closely connected with the first branchial arch. The upper or metapterygoid element of the mandibular arch (M.Pt) has a considerable development, and, becoming separated from the remainder of the arch, forms a mass of cartilage with one or two branchial rays, in the front wall of the spiracle, and constitutes a section of the mandibular arch still retaining traces of its primitive function in supporting the wall of a branchial pouch.
Although the development of other Elasmobranch types is not known, it is necessary to call attention to the mode of support of the mandibular arch in certain forms, notably Notidanus, Hexanchus and Cestracion, where the pterygo-quadrate region of the mandibular arch is directly articulated to the cranium between the optic and trigeminal foramina. In the two former genera the metapterygoid region of the arch is moreover continuous with the pterygo-quadrate, and articulates with the postorbital process of the auditory region of the skull. In spite of these attachments the mandibular arch continues to be partially supported by the hyomandibular. The skulls in which the mandibular arch has this double form of support have been called by Huxley amphistylic.
[FIG. 334. CRANIAL SKELETON OF A SALMON FRY, SECOND WEEK AFTER HATCHING; MEMBRANE BONES, EYEBALLS, AND NASAL SACS REMOVED. (From Parker.)
T.Cr. tegmen cranii; S.Or. supraorbital band; Fo. superior fontanelle; Au. auditory capsule; Pa.ch. parachordal cartilage; Ch. notochord; Tr. trabecula; above the trabecula, the interorbital septum is seen, passing into the cranial wall above and reaching the supraorbital band; H. optic foramen; V. trigeminal foramen; l^1, l^2. labial cartilages; Pl.Pt. palatopterygoid bar; M. Pt. metapterygoid tract; Qu. quadrate region; Mck. Meckelian cartilage; H.M. hyomandibular cartilage; Sy. symplectic tract; I.Hy. interhyal; C.Hy. ceratohyal; H.Hy. hypohyal; G.Hy. glossohyal; _Br._1. first branchial arch.]
Considering the in many respects primitive characters of the forms with amphistylic skulls it seems not improbable that they preserve the original mode of support of the mandibular arch; from which differentiations in two directions have taken place, viz. differentiations in the direction of a complete support of the mandibular arch by the hyoid, which is characteristic of most Elasmobranchii and, as will be shewn below, of Ganoidei and Teleostei; and differentiations towards a direct articulation or attachment of the mandibular arch to the cranium, without the intervention of the hyoid. The latter mode of attachment is called by Huxley autostylic. It is found in Holocephala, Dipnoi, Amphibia and the Amniota.
Teleostei. In addition to that of Elasmobranchii, the skull of the Salmon is the only hyostylic skull in which, by the admirable investigation of Parker (No. 451), the ontogeny of the hyoid and mandibular bars has been satisfactorily worked out. Apart from the presence of a series of membrane bones, the development of these bars agrees on the whole with the types already described.
[FIG. 335. YOUNG SALMON OF THE FIRST SUMMER, ABOUT 2 INCHES LONG; SIDE VIEW OF SKULL, EXCLUDING BRANCHIAL ARCHES. (From Parker.)
The palato-mandibular and hyoid tracts are detached from their proper situations, a line indicating the position where the hyomandibular is articulated beneath the pterotic ridge.
ol. olfactory fossa; c.tr. trabecular cornu; ul^a. ul^b. upper labial cartilages; p.s. presphenoid tract; t.cr. tegmen cranii; s.o.b. supraorbital band; fo. superior fontanelle; n.c. notochord; b.o. basilar cartilage; tr. trabecula; p.c. condyle for palatine cartilage; 5. trigeminal foramen; 7_a._ facial foramen; 8. foramen for glossopharyngeal and vagus nerves; mk. Meckelian cartilage; op.c. opercular condyle.
Bones: e.o. exoccipital; s.o. supraoccipital; e.p. epiotic; pt.o. pterotic; sp.o. sphenotic; op. opisthotic; pro. prootic; b.s. basisphenoid; al.s. alisphenoid; o.s. orbitosphenoid; l.e. ectethmoid or lateral ethmoid; pa. palatine; pg. pterygoid; m.pg. mesopterygoid; mt.pg. metapterygoid; qu. quadrate; ar. articular; h.m. hyomandibular; sy. symplectic; i.h. interhyal; ep.h. epiceratohyal; c.h. ceratohyal; h.h. hypohyal; g.h. glosso- or basihyal.]
The hyoid arch, though largely ossified, undergoes a process of development very similar to that in Raja. It is formed as a simple cartilaginous bar, which soon becomes segmented longitudinally into an anterior and a posterior part (fig. 334). The former constitutes the hyomandibular (H.M), while the latter, becoming more and more separated from the hyomandibular, constitutes the hyoid arch proper; owing to the disappearance of the hyobranchial cleft, it loses its primitive function, and serves on the one hand to support the operculum covering the gills, and on the other to support the tongue. It becomes segmented into a series of parts which are ossified (fig. 335) as the epiceratohyal (ep.h) above, then a large ceratohyal (ch), followed by a hypohyal (hh), while the median ventral element forms the basi- or glossohyal (g.h).
The hyomandibular itself is articulated with the skull below the pterotic process (fig. 334, H.M). Its upper element ossifies as the hyomandibular (fig. 335, h.m.), while its lower part (fig. 334, Sy), which is firmly connected with the mandibular arch, ossifies as the symplectic (fig. 335, sy). A connecting element between the two parts of the hyoid bar forms an interhyal (ih).
There are more important differences in the development of the mandibular arch in Elasmobranchii and the Salmon than in that of the hyoid arch, in that, instead of the whole arcade of the upper jaw being formed from the mandibular arch, a fresh element, in the form of an independently developed bar of cartilage, completes the upper arcade in front; but even with this bar the two halves of the upper branch of the arch do not meet anteriorly, but are separated by the ends of the trabeculæ.
The anterior bar of the upper arcade is known as the palatine; but it appears to me as yet uncertain how far it is to be regarded as an element, primitively belonging to the upper arcade of the mandibular arch, which has become secondarily independent in its development; or as an entirely distinct structure which has no counterpart in the Elasmobranch upper jaw. The latter view is adopted by Parker and Bridge, and a cartilage attached to the hinder wall of the nasal capsule of many Elasmobranchii is identified by them with the palatine rod of the Teleostei.
The arch itself is at first very similar to the succeeding arches; its dorsal extremity soon however becomes broadened, and provided with an anteriorly directed process. This part (fig. 334, M.Pt and Qu) is then segmented from the lower region, and forms what may be called the pterygo-quadrate cartilage, though not completely homologous with the similarly named cartilage in Elasmobranchs; while the lower region forms the Meckelian cartilage (Mck), which has already grown inwards, so as to meet its fellow ventrally below the mouth. The whole arch becomes at the same time widely separated from the axial parts of the skull.
Nearly simultaneously with the first differentiation of the mandibular arch, a bar of cartilage--the palatine bar already spoken of--is formed on each side, below the eye, in front of the mouth. The dilated anterior extremity of this bar soon comes in contact with an anterior process of the trabeculæ, known as the ethmo-palatine process.
In a later stage the pterygoid end of the pterygo-quadrate cartilage unites with the distal end of the palatine bar (fig. 334, Pl.Pt), and there is then formed a continuous cartilaginous arcade for the upper jaw, which is strikingly similar to the cartilaginous upper jaw of Elasmobranchii.
A large dorsal process of the primitive pterygo-quadrate now forms a large metapterygoid tract (M.Pt); while the whole arch becomes firmly bound to the hyomandibular (H.M).
In the later stages the parts formed in cartilage become ossified (fig. 335). The palatine is first ossified, the pterygoid region of the pterygo-quadrate is next ossified as a dorsal mesopterygoid (m.pg) and a ventral pterygoid proper (pg). The quadrate region, articulating with the Meckelian cartilage, becomes ossified as a distinct quadrate (qu), while the dorsal region becomes also ossified as a metapterygoid (mt.pg).
In the Meckelian cartilage a superficial ossification of the ventral edge and inner surface forms an articulare (ar); but the greater part of the cartilage persists through life.
Some of the above ossifications, at any rate those of the palatine and pterygoid, seem to be started by dental osseous plates adjoining the cartilage. They will be spoken of further in the section dealing with the membrane bones.
Amphibia. The development of the autostylic piscine skulls has unfortunately not yet been studied; and the most primitive autostylic types whose development we are acquainted with are those of the Amphibia; on which a large amount of light has been shed by the researches of Huxley and Parker.
The modifications of the hyoid arch are comparatively simple and uniform. It forms a rod of cartilage, which soon articulates in front with the quadrate element of the mandibular arch, and is subsequently attached by ligaments both to the quadrate and to the cranium. In those Amphibia in which external gills and gill clefts are lost, it fuses with the basal element of the hyoid (fig. 330), which, together with the basal portions of the following arches, forms a continuous cartilaginous plate. On the completion of these changes the paired parts of the hyoid arch have the form of two elongated rods, known as the anterior cornua of the hyoid, which attach the basihyal plate to the cranium behind the auditory capsule.
It is still uncertain whether there is any distinct element corresponding to the hyomandibular of fishes.
Parker holds that the columella auris of the Anura is the homologue of the hyomandibular. The columella develops comparatively late and independently of the remainder of the hyoid arch, but the similarity between its relations to the nerves and those of the hyomandibular is put forward by Parker as an argument in favour of his view. The early ligamentous connection between the quadrate and the upper end of the primitive hyoid is however an argument in favour of regarding the upper end of the primitive hyoid as the hyomandibular element, not separated from the remainder of the arch.
The history of the mandibular arch is more complicated than that of the hyoid. The part of it which corresponds with the upper jaw of Elasmobranchii exhibits most striking variations in development; so striking indeed as to suggest that the secondary modifications it has undergone are sufficiently considerable to render great caution necessary in drawing morphological conclusions from the processes which are in some instances observable. A more satisfactory judgment on this point will be possible after the publication of a memoir with which Parker is now engaged on the skulls of the different Anura.
The membrane bones applying themselves to the sides of the mandibular arch are relatively far more important than in the lower types. This is especially the case with the upper jaw where the maxillary and premaxillary bones functionally replace the primitive cartilaginous jaw; while membranous pterygoids and palatines apply themselves to, and largely take the place of, the cartilaginous palatine and pterygoid bars.
Two types worked out by Parker, viz. the Axolotl and the common Frog, may be selected to illustrate the development of the mandibular arch.
[FIG. 336. YOUNG AXOLOTL, 2-1/4 INCHES LONG; UNDER VIEW OF SKULL, DISSECTED, THE LOWER JAW AND GILL ARCHES HAVING BEEN REMOVED. (From Parker.)
nc. notochord; oc.c. occipital condyle; f.o. fenestra ovalis; st. stapes; tr. trabecular cartilage; i.n. internal nares; c.tr. cornu trabeculæ; pd. pedicle of quadrate; q. quadrate; pg. outline of pterygoid cartilage; 5´. orbito-nasal nerve; 7. facial nerve.
Bones: pa.s. parasphenoid; e.o. exoccipital; v. vomer; px. premaxillary; mx. maxillary; pa. palatine; pg. pterygoid.]
In the Axolotl, which may be taken as the type for the Urodela, the mandibular arch is constituted at a very early stage of (1) an enlarged dorsal element, corresponding with the pterygo-quadrate of the lower types, but usually known as the quadrate; and (2) a ventral or Meckelian element. The Meckelian bar very early acquires its investing bones, while the dorsal part of the quadrate becomes divided into two characteristic processes, viz. an anterior dorsal process which grows towards and soon permanently fuses with the trabecular crest, and a posterior process known as the otic process, which applies itself to the outer side of the auditory region. The anterior of these processes, as pointed out by Huxley, is probably homologous with the anterior process of the pterygo-quadrate bar in Notidanus, which articulates with the trabecular region of the cranium, while the otic process is homologous with the metapterygoid process. Hardly any trace is present of an anterior process to form a pterygoid bar, but dentigerous plates forming a dermal palatopterygoid bar have already appeared.
At a somewhat later stage a fresh process, called by Huxley the pedicle, grows out from the quadrate, and articulates with the ventral side of the auditory region (fig. 336, pd). Shortly afterwards a rod of cartilage grows forward from the quadrate under the membranous pterygoid (pg), which corresponds with the cartilaginous pterygoid bar of other types (fig. 336), and an independent palatine bar, arising even before the pterygoid process, is formed immediately dorsal to the dentigerous palatine plate (pa), and is attached to the trabecula. These two bars eventually meet, but never become firmly united to the more important membrane bones placed superficially to them.
The mandibular arch in the Frog stands, so far as development is concerned, in striking contrast to the mandibular arch of the Axolotl, in spite of the obvious similarity in the arrangement of the adult parts in the two types.
[FIG. 337. EMBRYO FROG, JUST BEFORE HATCHING; SIDE VIEW OF HEAD, WITH SKIN REMOVED. (From Parker.)
Na. olfactory sack; E. involution for eyeball; Au. auditory sack; Tr. trabecula; Mn. mandibular; Hy. hyoid; Br.I. first branchial arch; the gill-buds are seen on the first two branchial arches; l. labial cartilages.]
In the earliest stage it forms a simple bar in the membranous mandibular arch, parallel to and very similar to the hyoid bar behind (fig. 337, Mn). In the next stage observed, that is to say in Tadpoles of four, five, to six lines long, an astonishing transformation has taken place. The mandibular arch (fig. 338) is turned directly forwards parallel to the trabecula, to which it is attached in front (p.pg) and behind (pd). The proximal part of the arch thus forms a subocular bar, and the space between it and the trabecula a subocular fenestra. In front of the anterior attachment it is continued forwards for a short distance, and to the free end of this projecting part is articulated a small Meckelian cartilage directed upwards (mk). The Meckelian cartilage is at this stage placed in front of the nasal sacks, in the lower lip of the suctorial mouth. The greater part of the arch, parallel with the trabeculæ, is equivalent to what has been called in the Axolotl the quadrate, while its anterior attachment to the trabeculæ is the rudiment of the palatopterygoid cartilage. The posterior attachment is known as the pedicle.
[FIG. 338. TADPOLE OF COMMON TOAD, ONE-THIRD OF AN INCH LONG; CRANIAL AND MANDIBULAR CARTILAGES SEEN FROM ABOVE; THE PARACHORDAL CARTILAGES ARE NOT YET DEFINITE. (From Parker.)
nc. notochord; ms. muscular segments; au. auditory capsule; py. region of pituitary body; tr. trabecula; c.tr. cornu trabeculæ; p.pg. palatopterygoid bar; pd. pedicle; q. quadrate condyle; mk. Meckelian piece of mandibular arch; so.f. subocular fenestra; u.l. upper labial cartilage. The dotted circle within the quadrate region indicates the position of the internal nostril.]
The condition of the mandibular arch during this and the next stage (fig. 339) is very perplexing. Its structure appears adapted in some way to support the suctorial mouth of the Tadpole.
Reasons have been offered in a previous part of this volume for supposing that the suctorial mouth of the Tadpole is probably not simply a structure secondarily acquired by this larva, but is an organ inherited from an ancestor provided through life with a suctorial mouth.
The question thus arises, is the peculiar modification of the mandibular arch of the Tadpole an inherited or an acquired feature?
If the first alternative is accepted we should have to admit that the mandibular arch became first of all modified in connection with the suctorial mouth, before it was converted into the jaws of the Gnathostomata; and that the peculiar history of this arch in the Tadpole is a more or less true record of its phylogenetic development. In favour of this view is the striking similarity which Huxley has pointed out between the oral skeleton of the Lamprey and that of the Tadpole; and certain peculiarities of the mandibular arch of Chimæra and the Dipnoi can perhaps best be explained on the supposition that the oral skeleton of these forms has arisen in a manner somewhat similar to that in the Frog; though with reference to this point further developmental data are much required.
On the other hand the above suppositions would necessitate our admitting that a great abbreviation has occurred in the development of the mandibular arch of the otherwise more primitive Urodela; and that the simple mode of growth of the jaws in Elasmobranchii, from the primitive mandibular arch, is phylogenetically a much abbreviated and modified process, instead of being, as usually supposed, a true record of ancestral history.
If the view is accepted that the characters of the mandibular arch of the Tadpole are secondary, it will be necessary to admit that the adaptation of the mandibular arch to the suctorial mouth took place after the suctorial mouth had come to be merely a larval organ.
In view of our imperfect knowledge of the development of most Piscine skulls I would refrain from expressing a decided opinion in favour of either of these alternatives.
[FIG. 339. TADPOLE WITH TAIL BEGINNING TO SHRINK; SIDE VIEW OF SKULL WITHOUT THE BRANCHIAL ARCHES. (From Parker.)
n.c. notochord; au. auditory capsule; between it and eth. the low cranial side wall is seen; eth. ethmoidal region; st. stapes; 5. trigeminal foramen; 2. optic foramen; ol. olfactory capsules, both seen owing to slight tilting of the skull; c.tr. cornu trabeculæ; u.l. upper labial, in outline; su. suspensorium (quadrate); pd. its pedicle; ot.pr. its otic process; or.p. its orbitar process; t.m. temporal muscle, indicated by dotted lines passing beneath the orbitar process; pa.pg. palatopterygoid bar; mk. Meckelian cartilage; l.l. lower labial, in outline; c.h. ceratohyal; b.h. basihyal. The upper outline of the head is shewn by dotted lines.]
As the tail of the Tadpole gradually disappears, and the metamorphosis into the Frog becomes accomplished, the mandibular arch undergoes important changes (fig. 339): the palatopterygoid attachment (pa.pg) of the quadrate subocular bar becomes gradually elongated; and, as it is so, the front end of the subocular bar (su) rotates outwards and backwards, and soon forms a very considerable angle with the trabeculæ. The Meckelian cartilage (mk) at its free end becomes at the same time considerably elongated. These processes of growth continue till (fig. 330) the palatopterygoid bar (Pt) forms a subocular bar, and is considerably longer than the original subocular region of the quadrate; while the Meckelian cartilage (Mck) has assumed its permanent position on the hinder border of the no longer suctorial mouth, and has grown forwards so as nearly to meet its fellow in the median line.
[FIG. 340. YOUNG FROG, NEAR END OF FIRST SUMMER; UPPER VIEW OF SKULL, WITH LEFT MANDIBLE REMOVED, AND THE RIGHT EXTENDED OUTWARDS. (From Parker.)
b.o. basioccipital tract; s.o. supraoccipital tract; fo. frontal fontanelle; e.n. external nostril; internal to it, internasal plate; a.t. tympanic annulus.
Bones: e.o. exoccipital; pr.o. prootic, partly overlapped by p. parietal; f. frontal; eth. rudiment of sphenethmoid; na. nasal; pmx. premaxillary; mx. maxillary; pg. pterygoid, partly ensheathing the reduced cartilage; q.j. quadratojugal; sq. squamosal; ar. articular; d. dentary; m.mk. mento-Meckelian.]
The metapterygoid region of the quadrate gives rise to a posterior and dorsal process (fig. 339, ot.pr), the end of which is constricted off as the tympanic annulus (fig. 340, a.t); while the proximal part of the process remains as the otic (metapterygoid) process, articulating with the auditory cartilage.
The pedicle (pd) retains its original attachment to the skull.
The palatopterygoid soon becomes segmented into a transversely placed palatine, and a longitudinally placed pterygoid (fig. 340). With the exception of a few ossifications, which present no features of special interest, the parts of the mandibular arch have now reached their final condition, which is not very different from that in the Axolotl.
Sauropsida. In the Sauropsida the modifications of the hyoid and mandibular arches are fairly uniform.
The lower part of the hyoid arch, including the basihyoid, unites with the remnants of the arches behind to form the hyoid bone, to which it contributes the anterior cornu and anterior part of the body.
The columella is believed by Huxley and Parker to represent, as in the Anura, the independently developed dorsal (hyomandibular) element of the hyoid, together with the stapes with which it has become united[205].
[205] The strongest evidence in favour of Huxley's and Parker's view of the nature of the columella is the fusion in the adult Sphenodon of the upper end of the hyoid with the columella (vide Huxley, No. 445). From an examination of a specimen in the Cambridge museum I do not feel satisfied that the fusion is not secondary, but have not been able to examine the junction of the hyoid and columella in section. For a different view to that of Huxley vide Peters, "Ueb. d. Gehörknochelchen u. ihr Verhältniss zu. Zungenbeinbogen b. Sphenodon." Berlin Monatsberichte, 1874.
The membranous mandibular arch gives off in the embryos of all the Sauropsida an obvious bud to form the superior maxillary process, and the formation of this bud appears to represent the growth forwards of the pterygoid process in Elasmobranchii, which is indeed accompanied by the formation of a similar bud; but the skeletal rod, which appears in the axis of this bud, is as a rule independent of that in the true arch (fig. 331, pa, pg). The former is the pterygo-palatine bar; the latter the Meckelian and quadrate cartilages.
The pterygo-palatine bar is usually if not always ossified directly, without the intervention of cartilage.
Born has recently shewn that Parker was mistaken in supposing that the palatopterygoid bone is cartilaginous in Birds. In the Turtle a short cartilaginous pterygoid process of the quadrate would seem to be present (Parker, No. 458).
The quadrate and Meckelian cartilages are either from the first separate, or very early become so.
The quadrate cartilage ossifies as the quadrate bone, and supplies the permanent articulation for the lower jaw. Its upper end exhibits a tendency to divide into two processes, corresponding with the pedicle and otic processes of the Amphibia. The Meckelian cartilage becomes soon covered by investing bones, and its proximal end ossifies as the articulare. The remainder of the cartilage usually disappears.
Mammalia. The most extraordinary metamorphosis of the hyoid and mandibular arches occurs in the Mammalia, and has been in part known since the publication of the memoir of Reichert (No. 461).
[FIG. 341. EMBRYO PIG, TWO-THIRDS OF AN INCH LONG; ELEMENTS OF THE SKULL SEEN SOMEWHAT DIAGRAMMATICALLY FROM BELOW. (From Parker.)
pa. ch. parachordal cartilage; nc. notochord; au. auditory capsule; py. pituitary body; tr. trabeculæ; c.tr. trabecular cornu; pn. prenasal cartilage; e.n. external nasal opening; ol. nasal capsule; p.pg. palatopterygoid tract enclosed in the maxillopalatine process; mn. mandibular arch; hy. hyoid arch; th.h. first branchial arch; 7_a._ facial nerve; 8_a._ glossopharyngeal; 8_b._ vagus; 9. hypoglossal.]
Both the hyoid and mandibular arches develop at first more completely than in any of the other types above Fishes; and are articulated to each other above, while the pterygo-palatine bar is quite distinct. The main features of the subsequent development are undisputed, with the exception of that of the upper end of the hyoid, which is still controverted. The following is Parker's (No. 452) account for the Pig, which confirms in the main the view originally put forward by Huxley (No. 445).
The mandibular and hyoid arches are at first very similar (fig. 341 mn and hy), their dorsal ends being somewhat incurved, and articulating together.
In a somewhat later stage (fig. 342) the upper end of the mandibular bar (mb), without becoming segmented from the ventral part, becomes distinctly swollen, and clearly corresponds to the quadrate region of other types. The ventral part of the bar constitutes the Meckelian cartilage (mk).
[FIG. 342. EMBRYO PIG, AN INCH AND A THIRD LONG; SIDE VIEW OF MANDIBULAR AND HYOID ARCHES. THE MAIN HYOID ARCH IS SEEN AS DISPLACED BACKWARDS AFTER SEGMENTATION FROM THE INCUS. (From Parker.)
tg. tongue; mk. Meckelian cartilage; ml. body of malleus; mb. manubrium or handle of the malleus; t.ty. tegmen tympani; i. incus; st. stapes; i.hy. interhyal ligament; st.h. stylohyal cartilage; h.h. hypohyal; b.h. basibranchial; th.h. rudiment of first branchial arch; 7a. facial nerve.]
The hyoid arch has in the meantime become segmented into two parts, an upper part (i), which eventually becomes one of the small bones of the ear--the incus--and a lower part which remains permanently as the anterior cornu of the hyoid (st.h). The two parts continue to be connected by a ligament.
The incus is articulated with the quadrate end of the mandibular arch, and its rounded head comes in contact with the stapes (fig. 342, st) which is segmented from the fenestra ovalis. The main arch of the hyoid becomes divided into a hypohyal (h.h) below and a stylohyal (st.h) above, and also becomes articulated with the basal element of the arch behind (bh).
In the course of further development the Meckelian part of the mandibular arch becomes enveloped in a superficial ossification forming the dentary. Its upper end, adjoining the quadrate region, becomes calcified and then absorbed, and its lower, with the exception of the extreme point, is ossified and subsequently incorporated in the dentary.
The quadrate region remains relatively stationary in growth as compared with the adjacent parts of the skull, and finally ossifies to form the malleus bone of the ear. The processus gracilis of the malleus is the primitive continuation into Meckel's cartilage.
The malleus and incus are at first embedded in the connective tissue adjoining the tympanic cavity (hyomandibular cleft, vide p. 528); and externally to them a bone known as the tympanic bone becomes developed so that they become placed between the tympanic bone and the periotic capsule. In late foetal life they become transported completely within the tympanic cavity, though covered by a reflection of the tympanic mucous membrane.
The dorsal end of the part of the hyoid separated from the incus becomes ossified as the tympano-hyal, and is anchylosed with the adjacent parts of the periotic capsule. The middle part of the bar just outside the skull forms the stylohyal (styloid process in Man) which is attached by ligament to the anterior cornu of the hyoid (ceratohyal).
While the account of the formation of the malleus, incus, and stapes just given is that usually accepted in this country, a somewhat different view of the development of these parts has as a rule been adopted in Germany. Reichert (No. 461) held that both the malleus and the incus were derived from the mandibular bar; and this view has been confirmed by Günther, Kölliker and other observers, and has recently been adopted by Salensky (No. 462) after a careful research especially directed towards this point. Reichert also held that the stapes was derived from the hyoid bar; but, though his observations on this point have been very widely accepted, they have not met with such universal recognition as his views on the origin of the malleus and incus. Salensky has recently arrived at a view, which is in accord with that of Parker, in so far as the independence of the stapes of both the hyoid and mandibular arches is concerned. Salensky however holds that it is formed from a mass of mesoblast surrounding the artery of the mandibular arch, and that the form of the stapes is due to its perforation by the mandibular artery. A product of this artery permanently perforates the stapes in a few Mammalia, though in the majority it atrophies.
In view of the different accounts of the origin of the incus the exact nature of this bone must still be considered as an open question, but should Reichert's view be confirmed the identification of the incus with the columella of the Amphibia and Sauropsida must be abandoned.
Membrane bones and ossifications of the cranium.
The membrane bones of the skull may be divided into two classes, viz. (1) those derived from dermal osseous plates, which as explained above (p. 542) are primitively formed by the coalescence of the osseous plates of scales; and (2) those formed by the coalescence of the osseous plates of teeth lining the oral cavity. Some of the bones sheathing the edge of the mouth have been formed partly by the one process and partly by the other.
In the Fishes there are found all grades of transition between simple dermal scutes, and true subdermal osseous plates forming an integral part of the internal skeleton. Dermal scutes are best represented in Acipenser and some Siluroid Fishes.
Where the membrane bones still retain the character of dermal plates, those on the dorsal surface of the cranium are usually arranged in a series of longitudinal rows, continuing in the region of the head the rows of dermal scutes of the trunk; while the remaining cranial scutes are connected with the visceral arches. The dermal bones on the dorsal surface of the head are very different in number, size, and arrangement in different types of Fishes; but owing to their linear disposition it is usually possible to find a certain number both of the paired and unpaired bones which have a similar situation in the different forms. These usually receive the same names, but both from general considerations as to their origin, as well as from a comparison of different species, it appears to me probable that there is no real homology between these bones in different species, but only a kind of general correspondence[206].
[206] For some interesting remarks on the arrangement of these bones in Fishes, vide Bridge, "On the Osteology of Polyodon folium." Phil. Trans., 1878.
It is not in fact till we get to the types above the Fishes that we can find a series of homologous dorsal membrane bones covering the roof of the skull. In these types three paired sets of such bones are usually present, viz. from behind forwards the parietals, frontals and nasals, the latter bounding the posterior surface of the external nasal opening. Even in the higher types these bones are liable to vary very greatly from the usual arrangement.
Besides these bones there is usually present in the higher forms a lacrymal bone on the anterior margin of the orbit derived from one of a series of periorbital membrane bones frequently found in Fishes. Various supraorbital and postorbital bones, etc. are also frequently found in Lacertilia, etc. which are not impossibly phylogenetically independent of the membrane bones inherited from Fishes; and may have been evolved as bony scutes in the subdermal tissue of the papillæ of the sauropsidan scales.
The visceral arches of Fishes, especially of the Teleostei, are usually provided with a series of membrane bones. In the true branchial arches these take the form of dentigerous plates; but no such plates are found in the Amphibia or Amniota.
The opercular flap attached to the hyoid arch is usually supported by a series of membrane bones, which attain their highest development in the Teleostei. One of these bones, the præopercular, is very constant and is primitively attached along the outer edge of the hyomandibular. It seems to be retained in Amphibia as a membrane bone, overlapping the attachment of the quadrate and known as the squamosal; though it is not impossible that this bone may be derived from a superficial membrane bone, widely distributed in Teleostei and Ganoids, which is known as the supra-temporal. In Dipnoi the bone which appears to be clearly homologous with the squamosal would seem from its position to belong to the series of dorsal plates, and therefore to be the supra-temporal; but it is regarded by Huxley (No. 446) as the præopercular[207].
[207] It is not impossible that the solution of the difficulty about the præopercular is to be found by supposing that the præopercular as it exists in Teleostei is derived from a dorsal dermal plate, and that in the Dipnoi this plate retains more nearly than in Teleostei its primitive position.
In the Amniota the squamosal forms an integral part of the osseous roof of the skull; but in the Sauropsida it continues, as in Amphibia, to be closely related to the quadrate.
A larger series of persistent membrane bones are related to the mandibular, and its palato-quadrate process.
Overlying the palato-quadrate process are two rows of bones, one row lying at the edge of the mouth, on the outer side of the pterygo-palatine process, and the other set on the roof of the mouth superficial to the pterygo-palatine process.
The outer row is formed of the præmaxilla, maxilla, jugal, and very often quadratojugal. Of these bones the maxilla and præmaxilla, as is more especially demonstrated by their ontogeny in the Urodela, are partly derived from dentigerous plates and partly from membrane plates outside the mouth; while the jugal, and quadratojugal when present, are entirely extra-oral. In the Amphibia and Amniota the præmaxillæ and maxillæ are the most important bones in the facial region, and are quite independent of any cartilaginous substratum.
The second row of bones is clearly constituted in the Dipnoi and Amphibia by the vomer in front, then the palatine, and finally the pterygoid behind. Of these bones the vomer is never related to a cartilaginous tract below, while the palatines and pterygoids usually are so. The position and growth of the three bones in many Urodela (Axolotl) are especially striking (Hertwig. No. 442). In the Axolotl they form a continuous series, the vomer and palatine being covered by teeth, but the pterygoid being without teeth. The vomer and palatine originate from the united osseous plates of the bases of the teeth, while the pterygoid is in the first instance continuous with the palatine.
In Teleostei, Amia, etc., there are dentigerous plates forming a palatine and pterygoid, which in position, at any rate, closely correspond with the similarly named bones in Amphibia; and there is also a dentigerous vomer which may fairly be considered as equivalent to that in Amphibia.
In the Amniota the three bones found in Amphibia are always present, but with a few exceptions amongst the Lacertilia and Ophidia, are no longer dentigerous. The cartilaginous bars, which in the lower types are placed below the palatine and pterygoid membrane bones, are usually imperfectly or not at all developed.
On Meckel's cartilage important membrane bones are almost always grafted. On the outside and distal part of the cartilage a dentary is usually developed, which may envelope and replace the cartilage to a larger or smaller extent. Its oral edge is usually dentigerous. The splenial membrane bone is the most important bone on the inner side of Meckel's cartilage, but other elements known as the coronoid and angular may also be added. In Mammalia the dentary is the only element present (vide p. 590).
On the roof of the mouth a median bone, the parasphenoid, is very widely present in the Amphibia and Fishes, except the Elasmobranchii and Cyclostomata, and has no doubt the same phylogenetic origin as the vomer and membranous palatines and pterygoids.
It is less important in the Sauropsida, and becomes indistinguishably fused with the sphenoid in the adult, while in Mammalia it is no longer found.
Ossification of the Cartilaginous Cranium. In certain Fishes the cartilaginous cranium remains quite unossified, while completely enveloped in dermal bones. Such for instance is its condition in the Selachioid Ganoids. In most instances, however, the investment of the cartilaginous cranium by membrane bones is accompanied by a more or less complete ossification of the cartilage itself.
In the Dipnoi this occurs to the smallest extent, the only ossifications occurring in the lateral parts of the occipital region, and forming the exoccipitals.
In Teleostei and bony Ganoids, a considerably greater number of ossifications occur in the cartilage.
In the region of the occipital cartilaginous ring there appears a basioccipital and supraoccipital and two exoccipitals. The basioccipital is the only bone on the floor of the skull ossifying that part into which the notochord is primitively continued[208].
[208] The notochord appears also to enter into the posterior part of the region which ossifies as the basisphenoid.
In the region of the periotic cartilage a large number of bones may appear. In front there is the prootic, which often meets the exoccipital behind; behind there is above and in close connection with the supraoccipital the epiotic, and below in close connection with the exoccipital the opisthotic. On the dorsal side of the cartilage there is a projecting ridge composed mainly of a bone known as the pterotic, sometimes erroneously called the squamosal, and continued in front by the sphenotic. The pterotic, or the cartilaginous region corresponding to it, always supplies the articular surface for the hyomandibular.
In the floor of the skull, in the region of the pituitary body, there is formed a basisphenoid; while in the lateral parts of the wall of this part of the cranium, there is a bone known as the alisphenoid.
In front, parts of the lateral walls of the cranium ossify as the orbitosphenoids.
In view of the very imperfect ossification of the cartilaginous cranium of the Dipnoi, and of the fact that there is certainly no direct genetic connection between the Teleostei on the one hand, and the Amphibia and Amniota on the other, it is very difficult to believe that most of the ossifications of the cranium in the Amphibia and Amniota have more than a general correspondence with those in the Teleostei.
In the Amphibia the ossifications in the cartilage are comparatively few. In the occipital region there is a lateral ossification on each side of the exoccipital, the basioccipital region being unossified, and the supraoccipital at the utmost indurated by a calcareous deposit.
The periotic capsule is ossified by a prootic centre, which meets the exoccipital behind.
The front part of the cartilaginous cranium is ossified by a complete ring of bone--the sphenethmoid bone--which embraces part of the ethmoid region, and of the orbitosphenoid and presphenoid regions.
In the Amphibia the cartilaginous cranium, with its centres of ossification, is easily separable from the membranous investing bones.
In the Amniota the cartilaginous cranium, whose development in the embryo has already been described, becomes in the adult much more largely ossified, and the bones which replace the primitive cartilage unite with the membrane bones to form a continuous bony cranium.
The centres of ossification become again much more numerous. In the occipital segment analogous centres to those of Teleostei are again found; and it is probable that the exoccipitals are homologous throughout the series, the supraoccipital and basioccipital bones of the higher types being merely identical in position with the similarly named bones in Fishes.
In the periotic there are usually three centres of ossification, first recognised by Huxley. These are the prootic, the epiotic and opisthotic, the situations of which have already been defined. Of these the prootic is the most constant.
In Reptiles, the prootic and opisthotic frequently remain distinct even in the adult.
In Birds, the epiotic and opisthotic are early united with the supra- and exoccipital; and at a later period the prootic is also indistinguishably fused with the adjacent parts.
In Mammals the three ossifications fuse into a continuous whole--the periotic bone--which may be partially united with the adjacent parts.
In the pituitary region of the base of the cranium a pair of osseous centres or in the higher types a single centre (Parker[209]) gives rise to the basisphenoid bone, and in front of this another basal or pair of basal ossifications forms the presphenoid, while laterally to these two centres there are formed centres of ossification in the alisphenoid and orbitosphenoid regions, which may be extremely reduced in various Sauropsida, leaving the side walls of the skull almost entirely formed of membrane or cartilage.
[209] According to Kölliker there are two centres in Man in both the basisphenoid and presphenoid.
In the ethmoid region there may arise a median ossification forming the mesethmoid and lateral ossifications forming the lateral ethmoids or prefrontals; which may assist in forming the front wall of the brain-case, or be situated quite externally to the brain-case and be only related to the olfactory capsules.
The labial cartilages. In most Fishes a series of skeletal structures, known as the labial cartilages, are developed at the front and sides of the mouth, and in connection with the olfactory capsules; and these cartilages still persist in connection with the olfactory capsules, though in a reduced form, in the higher types. They are more developed in the Cyclostomata than in any other Vertebrate type.
The meaning of these cartilages is very obscure; but, from their being in part employed to support the lips and horny teeth of the Cyclostomata and the Tadpole, I should be inclined to regard them as remnants of a primitive skeleton supporting the suctorial mouth, with which, on the grounds already stated (p. 317), I believe the ancestors of the present Vertebrata to have been provided.
BIBLIOGRAPHY.
(439) A. Dugès. "Recherches sur l'Ostéologie et la myologie des Batraciens à leur différents âges." Paris, Mém. savans étrang. 1835, and An. Sci. Nat. Vol. I. 1834.
(440) C. Gegenbaur. _Untersuchungen z. vergleich. Anat. d. Wirbelthiere_, III. Heft. Das Kopfskelet d. Selachier. Leipzig, 1872.
(441) Günther. Beob. üb. die Entwick. d. Gehörorgans. Leipzig, 1842.
(442) O. Hertwig. "Ueb. d. Zahnsystem d. Amphibien u. seine Bedeutung f. d. Genese d. Skelets d. Mundhöhle." Archiv f. mikr. Anat., Vol. XI. 1874, suppl.
(443) T. H. Huxley. "On the theory of the vertebrate skull." Proc. Royal Soc., Vol. ix. 1858.
(444) T. H. Huxley. The Elements of Comparative Anatomy. London, 1869.
(445) T. H. Huxley. "On the Malleus and Incus." Proc. Zool. Soc., 1869.
(446) T. H. Huxley. "On Ceratodus Forsteri." Proc. Zool. Soc., 1876.
(447) T. H. Huxley. "The nature of the craniofacial apparatus of Petromyzon." Journ. of Anat. and Phys., Vol. X. 1876.
(448) T. H. Huxley. The Anatomy of Vertebrated Animals. London, 1871.
(449) W. K. Parker. "On the structure and development of the skull of the Common Fowl (Gallus Domesticus)." Phil. Trans., 1869.
(450) W. K. Parker. "On the structure and development of the skull of the Common Frog (Rana temporaria)." Phil. Trans., 1871.
(451) W. K. Parker. "On the structure and development of the skull in the Salmon (Salmo salar)." Bakerian Lecture, Phil. Trans., 1873.
(452) W. K. Parker. "On the structure and development of the skull in the Pig (Sus scrofa)." Phil. Trans., 1874.
(453) W. K. Parker. "On the structure and development of the skull in the Batrachia." Part II. Phil. Trans., 1876.
(454) W. K. Parker. "On the structure and development of the skull in the Urodelous Amphibia." Part III. Phil. Trans., 1877.
(455) W. K. Parker. "On the structure and development of the skull in the Common Snake (Tropidonotus natrix)." Phil. Trans., 1878.
(456) W. K. Parker. "On the structure and development of the skull in Sharks and Skates." Trans. Zoolog. Soc., 1878. Vol. X. pt. IV.
(457) W. K. Parker. "On the structure and development of the skull in the Lacertilia." Pt. I. Lacerta agilis, L. viridis and Zootoca vivipara. Phil. Trans., 1879.
(458) W. K. Parker. "The development of the Green Turtle." The Zoology of the Voyage of H. M. S. Challenger. Vol. I. pt. V.
(459) W. K. Parker. "The structure and development of the skull in the Batrachia." Pt. III. Phil. Trans., 1880.
(460) W. K. Parker and G. T. Bettany. The Morphology of the Skull. London, 1877.
(460*) H. Rathke. Entwick. d. Natter. Königsberg, 1839.
(461) C. B. Reichert. "Ueber die Visceralbogen d. Wirbelthiere." Müller's Archiv, 1837.
(462) W. Salensky. "Beiträge z. Entwick. d. knorpeligen Gehörknöchelchen." Morphol. Jahrbuch, Vol. VI. 1880.
Vide also Kölliker (No. 298), especially for the human and mammalian skull; Götte (No. 296).
Chapter XX
THE PECTORAL AND PELVIC GIRDLES AND THE SKELETON OF THE LIMBS.
The Pectoral girdle.
Pisces. Amongst Fishes the pectoral girdle presents itself in its simplest form in Elasmobranchii, where it consists of a bent band of cartilage on each side of the body, of somewhat variable form, meeting and generally uniting with its fellow ventrally. Its anterior border is in close proximity with the last visceral arch, and a transverse ridge on its outer and posterior border, forming the articular surface for the skeleton of the limb, divides it into a dorsal part, which may be called the scapula, and a ventral part which may be called the coracoid.
In all the remaining groups of Fishes there is added to the cartilaginous band, which may wholly or partially ossify, an osseous support composed of a series of membrane bones.
In the types with such membrane bones the cartilaginous parts do not continue to meet ventrally, except in the Dipnoi where there is a ventral piece of cartilage, distinct from that bearing the articulation of the limb. The cartilage is moreover produced into two ventral processes, an anterior and a posterior, below the articulation of the limb; which may be called, in accordance with Gegenbaur's nomenclature, the præcoracoid and coracoid. Of these the præcoracoid is far the most prominent, and in the majority of cases the coracoid can hardly be recognised. The coracoid process is however well developed in the Selachioid Ganoids, and the Siluroid Teleostei. In Teleostei the scapular region often ossifies in two parts, the smaller of which is named by Parker præcoracoid, though it is quite distinct from Gegenbaur's præcoracoid. The membrane bones, as they present themselves in their most primitive state in Acipenser and the Siluroids, are dermal scutes embracing the anterior edge of the cartilaginous girdle. In Acipenser there are three scutes on each side. A dorsal scute known as the supra-clavicle, connected above with the skull by the post-temporal; a middle piece or clavicle, and a ventral or infra-clavicle (interclavicle), which meets its fellow below.
In most Fishes the primitive dermal scutes have become subdermal membrane bones, and the infra-clavicle is usually not distinct, but the two clavicles form the most important part of the membranous elements of the girdle. Additional membrane bones (post-clavicles) are often present behind the main row.
The development of these parts in Fishes has been but little studied.
In Scyllium, amongst the Elasmobranchii, I find that each half of the pectoral girdle develops as a vertical bar of cartilage at the front border of the rudimentary fin, and externally to the muscle plates.
Before the tissue forming the pectoral girdle has acquired the character of true cartilage, the bars of the two sides meet ventrally by a differentiation in situ of the mesoblastic cells, so that, when the girdle is converted into cartilage, it forms an undivided arc, girthing the ventral side of the body. There is developed in continuity with the posterior border of this arc on the level of the fin a horizontal bar of cartilage, which is continued backwards along the insertion of the fin, and, as will be shewn in the sequel, becomes the metapterygium of the adult (figs. 344, bp and 348, mp). With this bar the remaining skeletal elements of the fin are also continuous.
The foramina of the pectoral girdle are not in the first instance formed by absorption, but by the non-development of the cartilage in the region of pre-existing nerves and vessels.
The development of these parts in Teleostei has been recently investigated by 'Swirski (No. 472) who finds in the Pike (Esox) that the cartilaginous pectoral girdle is at first continuous with the skeleton of the fin. It forms a rod with a dorsal scapular and ventral coracoid process. An independent mass of cartilage gives rise to a præcoracoid, which unites with the main mass, forming a triradiate bar like that of Acipenser or the Siluroids. The coracoid process becomes in the course of development gradually reduced.
'Swirski concludes that the so-called præcoracoid bar is to some extent a secondary element, and that the coracoid bar corresponds to the whole of the ventral part of the girdle of Elasmobranchii, but his investigations do not appear to me to be as complete as is desirable.
Amphibia and Amniota. The pectoral girdle contains a more or less constant series of elements throughout the Amphibia and Amniota; and the differences in structure between the shoulder girdle of these groups and that of Fishes are so great that it is only possible to make certain general statements respecting the homologies of the parts in the two sets of types.
The generally accepted view, founded on the researches of Parker, Huxley, and Gegenbaur, is to the effect that there is a primitively cartilaginous coraco-scapular plate, homologous with that in Fishes, and that the membrane bones in Fishes are represented by the clavicle and interclavicle in the Sauropsida and Mammalia, which are however usually admitted to be absent in Amphibia. These views have recently been challenged by Götte (No. 466) and Hoffmann (No. 467), on the ground of a series of careful embryological observations; and until the whole subject has been worked over by other observers it does not seem possible to decide satisfactorily between the conflicting views. It is on all hands admitted that the scapulo-coracoid elements of the shoulder girdle are formed as a pair of cartilaginous plates, one on each side of the body. The dorsal half of each plate becomes the scapula, which may subsequently become divided into a supra-scapula and scapula proper; while the ventral half forms the coracoid, which is not always separated from the scapula, and is usually divided into a coracoid proper, a præcoracoid, and an epicoracoid. By the conversion of parts of the primitive cartilaginous plates into membranous tissue various fenestræ may be formed in the cartilage, and the bars bounding these fenestræ both in the scapula and coracoid regions have received special names; the anterior bar of the coracoid region, forming the præcoracoid, being especially important. At the boundary between the scapula and the coracoid, on the hinder border of the plate, is placed the glenoid articular cavity to carry the head of the humerus.
The grounds of difference between Götte and Hoffmann and other anatomists concern especially the clavicle and interclavicle. The clavicle is usually regarded as a membrane bone which may become to some extent cartilaginous. By the above anatomists, and by Rathke also, it is held to be at first united with the coraco-scapular plate, of which it forms the anterior limb, free ventrally, but united dorsally with the main part of the plate; and Götte and Hoffmann hold that it is essentially a cartilage bone, which however in the majority of the Reptilia ossifies directly without passing through the condition of cartilage.
The interclavicle (episternum) is held by Götte to be developed from a paired formation at the free ventral ends of the clavicles, but he holds views which are in many respects original as to its homologies in Mammalia and Amphibia. Even if Götte's facts are admitted, it does not appear to me necessarily to follow that his deductions are correct. The most important of these is to the effect that the dermal clavicle of Pisces has no homologue in the higher types. Granting that the clavicle in these groups is in its first stage continuous with the coraco-scapular plate, and that it may become in some forms cartilaginous before ossifying, yet it seems to me all the same quite possible that it is genetically derived from the clavicle of Pisces, but that it has to a great extent lost even in development its primitive characters, though these characters are still partially indicated in the fact that it usually ossifies very early and partially at least as a membrane bone[210].
[210] The fact of the clavicle going out of its way, so to speak, to become cartilaginous before being ossified, may perhaps be explained by supposing that its close connection with the other parts of the shoulder girdle has caused, by a kind of infection, a change in its histological characters.
In treating the development of the pectoral girdle systematically it will be convenient to begin with the Amniota, which may be considered to fix the nomenclature of the elements of the shoulder girdle.
Lacertilia. The shoulder girdle is formed as two membranous plates, from the dorsal part of the anterior border of each of which a bar projects (Rathke, Götte), which is free at its ventral end. This bar, which is usually (Gegenbaur, Parker) held to be independent of the remaining part of the shoulder girdle, gives rise to the clavicle and interclavicle. The scapulo-coracoid plate soon becomes cartilaginous, while at the same time the clavicular bar ossifies directly from the membranous state. The ventral ends of the two clavicular bars enlarge to form two longitudinally placed plates, which unite together and ossify as the interclavicle.
Parker gives a very different account of the interclavicle in Anguis. He states that it is formed of two pairs of bones 'strapped on to the antero-inferior part of the præsternum,' which subsequently unite into one.
Chelonia. The shoulder girdle of the Chelonia is formed (Rathke) of a triradiate cartilage on each side, with one dorsal and two ventral limbs. It is admitted on all hands that the dorsal limb is the scapular element, and the posterior ventral limb the coracoid; but, while the anterior ventral limb is usually held to be the præcoracoid, Götte and Hoffmann maintain that, in spite of its being formed of cartilage, it is homologous with the anterior bar of the primitive shoulder-plates of Lacertilia, and therefore the homologue of the clavicle.
Parker and Huxley (doubtfully) hold that the three anterior elements of the ventral plastron (entoplastron and epiplastra) are homologous with the interclavicle and clavicles, but considering that these plates appear to belong to a secondary system of dermal ossifications peculiar to the Chelonia, this homology does not appear to me probable.
Aves. There are very great differences of view as to the development of the pectoral arch of Aves.
About the presence in typical forms of the coraco-scapular plate and two independent clavicular bars all authors are agreed. With reference to the clavicle and interclavicle Parker (No. 468) finds that the scapular end of the clavicle attaches itself to and ossifies a mass of cartilage, which he regards as the mesoscapula, while the interclavicle is formed of a mass of tissue between the ends of the clavicles where they meet ventrally, which becomes the dilated plate at their junction.
Gegenbaur holds that the two primitive clavicular bars are simply clavicles, without any element of the scapula; and states that the clavicles are not entirely ossified from membrane, but that a delicate band of cartilage precedes the osseous bars. He finds no interclavicle.
Götte and Rathke both state that the clavicle is at first continuous with the coraco-scapular plate, but becomes early separated, and ossifies entirely as a membrane bone. Götte further states that the interclavicles are formed as outgrowths of the median ends of the clavicles, which extend themselves at an early period of development along the inner edges of the two halves of the sternum. They soon separate from the clavicles, which subsequently meet to form the furculum; while the interclavicular rudiments give rise, on the junction of the two halves of the sternum, to its keel, and to the ligament connecting the furculum with the sternum. The observations of Götte, which tend to shew the keel of the sternum is really an interclavicle, appear to me of great importance.
A præcoracoid, partially separated from the coracoid by a space, is present in Struthio. It is formed by a fenestration of a primitively continuous cartilaginous coracoid plate (Hoffmann). In Dromæus and Casuarius clavicles are present (fused with the scapula in the adult Dromæus), though absent in other Ratitæ (Parker, etc.).
Mammalia. The coracoid element of the coraco-scapular plate is much reduced in Mammalia, forming at most a simple process (except in the Ornithodelphia) which ossifies however separately[211].
[211] This process, known as the coracoid process, is held by Sabatier to be the præcoracoid; while this author also holds that the upper third of the glenoid cavity, which ossifies by a special nucleus, is the true coracoid. The absence of a præcoracoid in the Ornithodelphia is to my mind a serious difficulty in the way of Sabatier's view.
With reference to the clavicles the same divergencies of opinion met with in other types are found here also.
The clavicle is stated by Rathke to be at first continuous with the coraco-scapular plate. It is however soon separated, and ossifies very early, in the human embryo before any other bone. Gegenbaur however shewed that the human clavicle is provided with a central axis of cartilage, and this observation has been confirmed by Kölliker, and extended to other Mammalia by Götte. The mode of ossification is nevertheless in many respects intermediate between that of a true cartilage bone and a membrane bone. The ends of the clavicles remain for some time, or even permanently, cartilaginous, and have been interpreted by Parker, it appears to me on hardly sufficient grounds, as parts of the mesoscapula and præcoracoid. Parker's so-called mesoscapula may ossify separately. The homologies of the episternum are much disputed. Götte, who has worked out the development of the parts more fully than any other anatomist, finds that paired interclavicular elements grow out backwards from the ventral ends of the clavicles, and uniting together form a somewhat T-shaped interclavicle overlying the front end of the sternum. This condition is permanent in the Ornithodelphia, except that the anterior part of the sternum undergoes atrophy. But in the higher forms the interclavicle becomes almost at once divided into three parts, of which the two lateral remain distinct, while the median element fuses with the subjacent part of the sternum and constitutes with it the presternum (manubrium sterni). If Götte's facts are to be trusted, and they have been to a large extent confirmed by Hoffmann, his homologies appear to be satisfactorily established. As mentioned on p. 563 Ruge (No. 438) holds that Götte is mistaken as to the origin of the presternum.
Gegenbaur admits the lateral elements as parts of the interclavicle, while Parker holds that they are not parts of an interclavicle but are homologous with the omosternum of the Frog, which is however held by Götte to be a true interclavicle.
Amphibia. In Amphibia the two halves of the shoulder girdle are each formed as a continuous plate, the ventral or coracoid part of which is forked, and is composed of a larger posterior and a smaller anterior bar-like process, united dorsally. In the Urodela the two remain permanently free at their ventral ends, but in the Anura they become united, and the space between them then forms a fenestra. The anterior process is usually (Gegenbaur, Parker) regarded as the præcoracoid, but Götte has pointed out that in its mode of development it strongly resembles the clavicle of the higher forms, and behaves quite differently to the so-called præcoracoid of Lizards. It is however to be noticed that it differs from the clavicle in the fact that it is never segmented off from the coraco-scapular plate, a condition which has its only parallel in the equally doubtful case of the Chelonia. Parker holds that there is no clavicle present in the Amphibia, while Gegenbaur maintains that an ossification which appears in many of the Anura (though not in the Urodela) in the perichondrium on the anterior border of the cartilaginous bar above mentioned is the representative of the clavicle. Götte's observations on the ossification of this bone throw doubt upon this view of Gegenbaur; while the fact that the cartilaginous bar may be completely enclosed by the bone in question renders Gegenbaur's view, that there is present both a clavicle and præcoracoid, highly improbable.
No interclavicle is present in Urodela, but in this group and in a number of the Anura, a process grows out from the end of each of the bars (præcoracoids) which Götte holds to be the clavicles. The two processes unite in the median line, and give rise in front to the anterior unpaired element of the shoulder girdle (omosternum of Parker). They sometimes overlap the epicoracoids behind, and fusing with them bind them together in the median line. Parker who has described the paired origin of the so-called omosternum, holds that it is not homologous with the interclavicle, but compares it with his omosternum in Mammals.
BIBLIOGRAPHY.
(463) Bruch. "Ueber die Entwicklung der Clavicula und die Farbe des Blutes." Zeit. f. wiss. Zool., iv. 1853.
(464) A. Dugès. "Recherches sur l'ostéologie et la myologie des Batraciens à leurs différens âges." Mémoires des savants étrang. Académie royale des sciences de l'institut de France, Vol. VI. 1835.
(465) C. Gegenbaur. Untersuchungen zur vergleichenden Anatomie der Wirbelthiere, 2 Heft. Schultergürtel der Wirbelthiere. Brustflosse der Fische. Leipzig, 1865.
(466) A. Götte. "Beiträge z. vergleich. Morphol. d. Skeletsystems d. Wirbelthiere, Brustbein u. Schultergürtel." Archiv f. mikr. Anat. Vol. XIV. 1877.
(467) C. K. Hoffmann. "Beiträge z. vergleichenden Anatomie d. Wirbelthiere." Niederländisches Archiv f. Zool., Vol. V. 1879.
(468) W. K. Parker. "A Monograph on the Structure and Development of the Shoulder-girdle and Sternum in the Vertebrata." Ray Society, 1868.
(469) H. Rathke. Ueber die Entwicklung der Schildkröten. Braunschweig, 1848.
(470) H. Rathke. Ueber den Bau und die Entwicklung des Brustbeins der Saurier, 1853.
(471) A. Sabatier. Comparaison des ceintures et des membres antérieurs et postérieurs d. la Série d. Vertébrés. Montpellier, 1880.
(472) Georg 'Swirski. Untersuch. üb. d. Entwick. d. Schultergürtels u. d. Skelets d. Brustflosse d. Hechts. Inaug. Diss. Dorpat, 1880.
Pelvic girdle.
Pisces. The pelvic girdle of Fishes is formed of a cartilaginous band, to the outer and posterior side of which the basal element of the pelvic fin is usually articulated. This articulation divides it into a dorsal iliac, and ventral pubic section. The iliac section never articulates with the vertebral column.
In Elasmobranchii the two girdles unite ventrally, but the iliac section is only slightly developed. In Chimæra there is a well developed iliac process, but the pubic parts of the girdle are only united by connective tissue.
In the cartilaginous Ganoids the pelvic girdle is hardly to be separated from the skeleton of the fin. It is not united with its fellow, and is represented by a plate with slightly developed pubic and iliac processes.
In the Dipnoi there is a simple median cartilage, articulated with the limb, but not provided with an iliac process. In bony Ganoids and Teleostei there is on each side a bone meeting its fellow in the ventral line, which is usually held to be the rudiment of the pelvic girdle; while Davidoff attempts to shew that it is the basal element of the fin, and that, except in Polypterus, a true pelvic girdle is absent in these types.
From my own observations I find that the mode of development of the pelvic girdle in Scyllium is very similar to that of the pectoral girdle. There is a bar on each side, continuous on its posterior border with the basal element of the fin (figs. 345 and 347). This bar meets and unites with its fellow ventrally before becoming converted into true cartilage, and though the iliac process (il) is never very considerable, yet it is better developed in the embryo than in the adult, and is at first directed nearly horizontally forwards.
Amphibia and Amniota. The primitive cartilaginous pelvic girdle of the higher types exhibits the same division as that of Pisces into a dorsal and a ventral section, which meet to form the articular cavity for the femur, known as the acetabulum. The dorsal section is always single, and is attached by means of rudimentary ribs to the sacral region of the vertebral column, and sometimes to vertebræ of the adjoining lumbar or caudal regions. It always ossifies as the ilium.
The ventral section is usually formed of two more or less separated parts, an anterior which ossifies as the pubis, and a posterior which ossifies as the ischium. The space between them is known as the obturator foramen. In the Amphibia the two parts are not separated, and resemble in this respect the pelvic girdle of Fishes. They generally meet the corresponding elements of the opposite side ventrally, and form a symphysis with them. The symphysis pubis, and symphysis ischii may be continuous (Mammalia, Amphibia).
The observations on the development of the pelvic girdle in the Amphibia and Amniota are nearly as scanty as on those of Fishes.
Amphibia. In the Amphibia (Bunge, No. 473) the two halves of the pelvic girdle are formed as independent masses of cartilage, which subsequently unite in the ventral line.
In the Urodelous Amphibia (Triton) each mass is a simple plate of cartilage divided into a dorsal and ventral section by the acetabulum. The ventral parts, which are not divided into two regions, unite in a symphysis comparatively late.
The dorsal section ossifies as the ilium. The ventral usually contains a single ossification in its posterior part which forms the ischium; while the anterior part, which may be considered as representing the pubis, usually remains cartilaginous; though Huxley (No. 475) states that it has a separate centre of ossification in Salamander, which however does not appear to be always present (Bunge). There is a small obturator foramen between the ischium and pubis, which gives passage to the obturator nerve. It is formed by the part of the tissue where the nerve is placed not becoming converted into cartilage.
There is a peculiar cartilage in the ventral median line in front of the pubis, which is developed independently of and much later than the true parts of the pelvic girdle. It may be called the præpubic cartilage.
Reptilia. In Lacertilia the pelvic girdle is formed as a somewhat triradiate mass of cartilage on each side, with a dorsal (iliac) process, and two ventral (pubic and ischiad) processes. The acetabulum is placed on the outer side at the junction of the three processes, each of which may be considered to have a share in forming it. The distal ends of the pubis and ischium are close together when first formed, but subsequently separate. Each of them unites at a late stage with the corresponding process of the opposite side in a ventral symphysis. A centre of ossification appears in each of the three processes of the primitive cartilage.
Aves. In Birds the parts of the pelvic girdle no longer develop as a continuous cartilage (Bunge). Either the pubis may be distinct, or, as in the Duck, all the elements. The ilium early exhibits a short anterior process, but the pubis and ischium are at first placed with their long axes at right angles to that of the ilium, but gradually become rotated so as to lie parallel with it, their distal ends pointing backwards, and not uniting ventrally excepting in one or two Struthious forms.
Mammalia. In Mammalia the pelvic girdle is formed in cartilage as in the lower forms, but in Man at any rate the pubic part of the cartilage is formed independently of the remainder (Rosenberg). There are the usual three centres of ossification, which unite eventually into a single bone--the innominate bone. The pubis and ischium of each side unite with each other ventrally, so as completely to enclose the obturator foramen.
Huxley holds that the so-called marsupial bones of Monotremes and Marsupials, which as shewn by Gegenbaur (No. 474) are performed in cartilage, are homologous with the præpubis of the Urodela; but considering the great gap between the Urodela and Mammalia this homology can only be regarded as tentative. He further holds that the anterior prolongations of the cartilaginous ventral ends of the pubis of Crocodilia are also structures of the same nature.
BIBLIOGRAPHY.
(473) A. Bunge. Untersuch. z. Entwick. d. Beckengürtels d. Amphibien, Reptilien u. Vögel. Inaug. Diss. Dorpat, 1880.
(474) C. Gegenbaur. "Ueber d. Ausschluss des Schambeins von d. Pfanne d. Hüftgelenkes." Morph. Jahrbuch, Vol. II. 1876.
(475) Th. H. Huxley. "The characters of the Pelvis in Mammalia, etc." Proc. of Roy. Soc., Vol. XXVIII. 1879.
(476) A. Sabatier. Comparaison des ceintures et des membres antérieurs et postérieurs dans la Série d. Vertébrés. Montpellier, 1880.
Comparison of Pectoral and Pelvic girdles.
Throughout the Vertebrata a more or less complete serial homology may be observed between the pectoral and pelvic girdles.
In the cartilaginous Fishes each girdle consists of a continuous band, a dorsal and ventral part being indicated by the articulation of the fin; the former being relatively undeveloped in the pelvic girdle, while in the pectoral it may articulate with the vertebral column. In the case of the pectoral girdle secondary membrane bones become added to the primitive cartilage in most Fishes, which are not developed in the case of the pelvic girdle.
In the Amphibia and Amniota the ventral section of each girdle becomes divided into an anterior and a posterior part, the former constituting the præcoracoid and pubis, and the latter the coracoid and ischium; these parts are however very imperfectly differentiated in the pelvic girdle of the Urodela. The ventral portions of the pelvic girdle usually unite below in a symphysis. They also meet each other ventrally in the case of the pectoral girdle in Amphibia, but in most other types are separated by the sternum, which has no homologue in the pelvic region, unless the præpubic cartilage is to be regarded as such. The dorsal or scapular section of the pectoral girdle remains free; but that of the pelvic girdle acquires a firm articulation with the vertebral column.
If the clavicle of the higher types is derived from the membrane bones of the pectoral girdle of Fishes, it has no homologue in the pelvic girdle; but if, as Götte and Hoffmann suppose, it is a part of the primitive cartilaginous girdle, the ordinary view as to the serial homologies of the ventral sections of the two girdles in the higher types will need to be reconsidered.
Limbs.
It will be convenient to describe in this place not only the development of the skeleton of the limbs but also that of the limbs themselves. The limbs of Fishes are moreover so different from those of the Amphibia and Amniota that the development of the two types of limb may advantageously be treated separately.
In Fishes the first rudiments of the limbs appear as slight longitudinal ridge-like thickenings of the epiblast, which closely resemble the first rudiments of the unpaired fins.
These ridges are two in number on each side, an anterior immediately behind the last visceral fold, and a posterior on the level of the cloaca. In most Fishes they are in no way connected, but in some Elasmobranch embryos, more especially in Torpedo, they are connected together at their first development by a line of columnar epiblast cells[212]. This connecting line of columnar epiblast is a very transitory structure, and after its disappearance the rudimentary fins become more prominent, consisting (fig. 343, b) of a projecting ridge both of epiblast and mesoblast, at the outer edge of which is a fold of epiblast only, which soon reaches considerable dimensions. At a later stage the mesoblast penetrates into this fold and the fin becomes a simple ridge of mesoblast, covered by epiblast. The pectoral fins are usually considerably ahead of the pelvic fins in development.
[212] F. M. Balfour. Monograph on Elasmobranch Fishes, pp. 101-2.
For the remaining history it is necessary to confine ourselves to Scyllium as the only type which has been adequately studied.
The direction of the original ridge which connects the two fins of each side is nearly though not quite longitudinal, sloping somewhat obliquely downwards. It thus comes about that the attachment of each pair of limbs is somewhat on a slant, and that the pelvic pair nearly meet each other in the median ventral line a little way behind the anus.
[FIG. 343. SECTION THROUGH THE VENTRAL PART OF THE TRUNK OF A YOUNG EMBRYO OF SCYLLIUM AT THE LEVEL OF THE UMBILICAL CORD.
b. pectoral fin; ao. dorsal aorta; cav. cardinal vein; ua. vitelline artery; u.v. vitelline vein; al. duodenum; l. liver; sd. opening of segmented duct into the body cavity; mp. muscle plate; um. umbilical canal.]
The elongated ridge, forming the rudiment of each fin, gradually projects more and more, and so becomes broader in proportion to its length, but at the same time its actual attachment to the side of the body becomes shortened from behind forwards, so that what was originally the attached border becomes in part converted into the posterior border. This process is much more completely carried out in the case of the pectoral fins than in that of the pelvic, and the changes of form undergone by the pectoral fin in its development may be gathered from figs. 344 and 348.
Before proceeding to the development of the skeleton of the fin it may be pointed out that the connection of the two rudimentary fins by a continuous epithelial line suggests the hypothesis that they are the remnants of two continuous lateral fins[213].
[213] Both Maclise and Humphry (Journal of Anat. and Phys., Vol. V.) had previously suggested that the paired fins were related to the unpaired fins.
Shortly after the view that the paired fins were remnants of continuous lateral fins had been put forward in my memoir on Elasmobranch Fishes, two very interesting papers were published by Thacker (No. 489) and Mivart (No. 484) advocating this view on the entirely independent grounds of the adult structure of the skeleton of the paired fins in comparison with that of the unpaired fins[214].
[214] Davidoff in a Memoir (No. 477) which forms an important contribution to our knowledge of the structure of the pelvic fins has attempted from his observations to deduce certain arguments against the lateral fin theory of the limbs. His main argument is based on the fact that a variable but often considerable number of the spinal nerves in front of the pelvic fin are united, by a longitudinal commissure, with the true plexus of the nerves supplying the fin. From this he concludes that the pelvic fin has shifted its position, and that it may once therefore have been situated close behind the visceral arches. If this is the strongest argument which can be brought against the theory advocated in the text, there is I trust a considerable chance of its being generally accepted. For even granting that Davidoff's deduction from the character of the pelvic plexus is correct, there is, so far as I see, no reason in the nature of the lateral fin theory why the pelvic fins should not have shifted, and on the other hand the longitudinal cord connecting some of the spinal nerves in front of the pelvic fin may have another explanation. It might for instance be a remnant of the time when the pelvic fin had a more elongated form than at present, and accordingly extended further forwards.
In any case our knowledge of the nature and origin of nervous plexuses is far too imperfect to found upon their character such conclusions as those of Davidoff.
The development of the skeleton has unfortunately not been as yet very fully studied. I have however made some investigations on this subject on Scyllium, and 'Swirski has also made some on the Pike.
In Scyllium the development of both the pectoral and pelvic fins is very similar.
In both fins the skeleton in its earliest stage consists of a bar springing from the posterior side of the pectoral or pelvic girdle, and running backwards parallel to the long axis of the body. The outer side of this bar is continued into a plate which extends into the fin, and which becomes very early segmented into a series of parallel rays at right angles to the longitudinal bar.
In other words, the primitive skeleton of both the fins consists of a longitudinal bar running along the base of the fin, and giving off at right angles series of rays which pass into the fin. The longitudinal bar, which may be called the basipterygium, is moreover continuous in front with the pectoral or pelvic girdle as the case may be.
[FIG. 344. PECTORAL FIN OF A YOUNG EMBRYO OF SCYLLIUM IN LONGITUDINAL AND HORIZONTAL SECTION.
The skeleton of the fin was still in the condition of embryonic cartilage.
b.p. basipterygium (eventual metapterygium); fr. fin rays; p.g. pectoral girdle in transverse section; f. foramen in pectoral girdle; pc. wall of peritoneal cavity.]
The primitive skeleton of the pectoral fin is shewn in longitudinal section in fig. 344, and that of the pelvic fin at a slightly later stage in fig. 345.
A transverse section shewing the basipterygium (mpt) of the pectoral fin, and the plate passing from it into the fin, is shewn in fig. 346.
Before proceeding to describe the later history of the two fins it may be well to point out that their embryonic structure completely supports the view which has been arrived at from the consideration of the soft parts of the fin.
My observations shew that the embryonic skeleton of the paired fin consists of a series of parallel rays similar to those of the unpaired fins. These rays support the soft part of the fin which has the form of a longitudinal ridge, and are continuous at their base with a longitudinal bar, which may very probably be due to secondary development. As pointed out by Mivart, a longitudinal bar is also occasionally formed to support the cartilaginous rays of unpaired fins. The longitudinal bar of the paired fins is believed by both Thacker and Mivart to be due to the coalescence of the bases of primitively independent rays, of which they believe the fin to have been originally composed. This view is probable enough in itself, but there is no trace in the embryo of the bar in question being formed by the coalescence of rays, though the fact of its being perfectly continuous with the bases of the rays is somewhat in favour of this view[215].
[215] Thacker more especially founds his view on the adult form of the pelvic fins in the cartilaginous Ganoids; Polyodon, in which the part which constitutes the basal plate in other forms is divided into separate segments, being mainly relied on. It is possible that the segmentation of this plate, as maintained by Gegenbaur and Davidoff, is secondary, but Thacker's view that the segmentation is a primitive character seems to me, in the absence of definite evidence to the reverse, the more natural one.
[FIG. 345. PELVIC FIN OF A VERY YOUNG FEMALE EMBRYO OF SCYLLIUM STELLARE.
bb. basipterygium; pu. pubic process of pelvic girdle; il. iliac process of pelvic girdle.]
A point may be noticed here which may perhaps appear to be a difficulty, viz. that to a considerable extent in the pectoral, and to some extent in the pelvic fin the embryonic cartilage from which the fin-rays are developed is at first a continuous lamina, which subsequently segments into rays. I am however inclined to regard this merely as a result of the mode of conversion of the indifferent mesoblast into cartilage; and in any case no conclusion adverse to the above view can be drawn from it, since I find that the rays of the unpaired fin are similarly segmented from a continuous lamina. In all cases the segmentation of the rays is to a large extent completed before the tissue in question is sufficiently differentiated to be called cartilage by an histologist.
Thacker and Mivart both hold that the pectoral and pelvic girdles have been evolved by ventral and dorsal growths of the anterior end of the longitudinal bar supporting the fin-rays.
There is, so far as I see, no theoretical objection to be taken to this view, and the fact of the pectoral and pelvic girdles originating continuously, and long remaining united with the longitudinal bars of their respective fins is in favour of rather than against this view. The same may be said of the fact that the first part of each girdle to be formed is that in the neighbourhood of the longitudinal bar (basipterygium) of the fin, the dorsal and ventral prolongations being subsequent growths.
The later development of the skeleton of the two fins is more conveniently treated separately.
[FIG. 346. TRANSVERSE SECTION THROUGH THE PECTORAL FIN OF A YOUNG EMBRYO OF SCYLLIUM STELLARE.
mpt. basipterygial bar (metapterygium); fr. fin ray; m. muscles; hf. horny fibres.]
The pelvic fin. The changes in the pelvic fin are comparatively slight. The fin remains through life as a nearly horizontal lateral projection of the body, and the longitudinal bar--the basipterygium--at its base always remains as such. It is for a considerable period attached to the pelvic girdle, but eventually becomes segmented from it. Of the fin rays the anterior remains directly articulated with the pelvic girdle on the separation of the basipterygium (fig. 347), and the remaining rays finally become segmented from the basipterygium, though they remain articulated with it. They also become to some extent transversely segmented. The posterior end of the basipterygial bar also becomes segmented off as the terminal ray.
The pelvic fin thus retains in all essential points its primitive arrangement.
The pectoral fin. The earliest stage of the pectoral fin differs from that of the pelvic fin only in minor points. There is the same longitudinal or basipterygial bar to which the fin-rays are attached, whose position at the base of the fin is clearly seen in the transverse section (fig. 346, mpt). In front the bar is continuous with the pectoral girdle (figs. 344 and 348).
[FIG. 347. PELVIC FIN OF A YOUNG MALE EMBRYO OF SCYLLIUM STELLARE.
bp. basipterygium; m.o. process of basipterygium continued into clasper; il. iliac process of pectoral girdle; pu. pubis.]
[FIG. 348. PECTORAL FIN OF AN EMBRYO OF SCYLLIUM STELLARE.
mp. metapterygium (basipterygium of earlier stage); me.p. rudiment of future pro- and mesopterygium; sc. cut surface of scapular process; cr. coracoid process; fr. foramen; f. horny fibres.]
The changes which take place in the course of the further development are however very much more considerable in the case of the pectoral than in that of the pelvic fin.
By the process spoken of above, by which the attachment of the pectoral fin to the body wall becomes shortened from behind forwards, the basipterygial bar is gradually rotated outwards, its anterior end remaining attached to the pectoral girdle. In this way this bar comes to form the posterior border of the skeleton of the fin (figs. 348 and 349, mp), constituting what Gegenbaur called the metapterygium, and eventually becomes segmented off from the pectoral girdle, simply articulating with its hinder edge.
The plate of cartilage, which is continued outwards from the basipterygium, or as we may now call it, the metapterygium, into the fin, is not nearly so completely divided up into fin-rays as in the case of the pelvic fin, and this is especially the case with the basal part of the plate. This basal part becomes in fact at first only divided into two parts (fig. 348) a small anterior part at the front end (me.p), and a larger posterior along the base of the remainder of the fin. The anterior part directly joins the pectoral girdle at its base, resembling in this respect the anterior fin-ray of the pelvic girdle. It constitutes the rudiment of the mesopterygium and propterygium of Gegenbaur. It bears four fin-rays at its extremity, the anterior not being well marked. The remaining fin-rays are borne by the edge of the plate continuous with the metapterygium.
The further changes in the cartilages of the limb are not important, and are easily understood by reference to fig. 349 representing the limb of a nearly full-grown embryo. The front end of the anterior basal cartilage becomes segmented off as a propterygium, bearing a single fin-ray, leaving the remainder of the cartilage as a mesopterygium. The remainder of the now considerably segmented fin-rays are borne by the metapterygium.
The mode of development of the pectoral fin demonstrates that, as supposed by Mivart, the metapterygium is the homologue of the basal cartilage of the pelvic fin.
From the mode of development of the fins of Scyllium conclusions may be drawn adverse to the views recently put forward on the structure of the fin by Gegenbaur and Huxley, both of whom consider the primitive type of fin to be most nearly retained in Ceratodus, and to consist of a central multisegmented axis with numerous rays. Gegenbaur derives the Elasmobranch pectoral fin from a form which he calls the archipterygium, nearly like that of Ceratodus, with a median axis and two rows of rays; but holds that in addition to the rays attached to the median axis, which are alone found in Ceratodus, there were other rays directly articulated to the shoulder-girdle. He considers that in the Elasmobranch fin the majority of the lateral rays on the posterior (median or inner according to his view of the position of the limb) side have become aborted, and that the central axis is represented by the metapterygium; while the pro- and mesopterygium and their rays are, he believes, derived from those rays of the archipterygium which originally articulated directly with the shoulder-girdle.
Gegenbaur's view appears to me to be absolutely negatived by the facts of development of the pectoral fin in Scyllium; not so much because the pectoral fin in this form is necessarily to be regarded as primitive, but because what Gegenbaur holds to be the primitive axis of the biserial fin is demonstrated to be really the base, and it is only in the adult that it is conceivable that a second set of lateral rays could have existed on the posterior side of the metapterygium. If Gegenbaur's view were correct we should expect to find in the embryo, if anywhere, traces of the second set of lateral rays; but the fact is that, as may easily be seen by an inspection of figs. 344 and 346, such a second set of lateral rays could not possibly have existed in a type of fin like that found in the embryo[216]. With this view of Gegenbaur's it appears to me that the theory held by this anatomist to the effect that the limbs are modified gill arches also falls; in that his method of deriving the limbs from gill arches ceases to be admissible, while it is not easy to see how a limb, formed on the type of the embryonic limb of Elasmobranchs, could be derived from a visceral arch with its branchial rays[217].
[216] If, which I very much doubt, Gegenbaur is right in regarding certain rays found in some Elasmobranch pectoral fins as rudiments of a second set of rays on the posterior side of the metapterygium, these rays will have to be regarded as structures in the act of being evolved, and not as persisting traces of a biserial fin.
[217] Some arguments in favour of Gegenbaur's theory adduced by Wiedersheim as a result of his researches on Protopterus are interesting. The attachment which he describes between the external gills and the pectoral girdle is no doubt remarkable, but I would suggest that the observations we have on the vascular supply of these gills demonstrate that this attachment is secondary.
[FIG. 349. SKELETON OF THE PECTORAL FIN AND PART OF PECTORAL GIRDLE OF A NEARLY RIPE EMBRYO OF SCYLLIUM STELLARE.
m.p. metapterygium; me.p. mesopterygium; pp. propterygium; cr. coracoid process.]
Gegenbaur's older view that the Elasmobranch fin retains a primitive uniserial type appears to me to be nearer the truth than his more recent view on this subject; though I hold that the fundamental point established by the development of these parts in Scyllium is that the posterior border of the adult Elasmobranch fin is the primitive base line, i.e. the line of attachment of the fin to the side of the body.
Huxley holds that the mesopterygium is the proximal piece of the axial skeleton of the limb of Ceratodus, and derives the Elasmobranch fin from that of Ceratodus by the shortening of its axis and the coalescence of some of its elements. The secondary character of the mesopterygium, and its total absence in the embryo Scyllium, appears to me as conclusive against Huxley's view, as the character of the embryonic fin is against that of Gegenbaur; and I should be much more inclined to hold that the fin of Ceratodus has been derived from a fin like that of the Elasmobranchii by a series of steps similar to those which Huxley supposes to have led to the establishment of the Elasmobranch fin, but in exactly the reverse order.
With reference to the development of the pectoral fin in the Teleostei there are some observations of 'Swirski (No. 488) which unfortunately do not throw very much light upon the nature of the limb.
'Swirski finds that in the Pike the skeleton of the limb is formed of a plate of cartilage, continuous with the pectoral girdle; which soon becomes divided into a proximal and a distal portion. The former is subsequently segmented into five basal rays, and the latter into twelve parts, the number of which subsequently becomes reduced.
These investigations might be regarded as tending to shew that the basipterygium of Elasmobranchii is not represented in Teleostei, owing to the fin rays not having united into a continuous basal bar, but the observations are not sufficiently complete to admit of this conclusion being founded upon them with any certainty.
The cheiropterygium.
Observations on the early development of the pentadactyloid limbs of the higher Vertebrata are comparatively scanty.
The limbs arise as simple outgrowths of the sides of the body, formed both of epiblast and mesoblast. In the Amniota, at all events, they are processes of a special longitudinal ridge known as the Wolffian ridge. In the Amniota they also bear at their extremity a thickened cap of epiblast, which may be compared with the epiblastic fold at the apex of the Elasmobranch fin.
Both limbs have at first a precisely similar position, both being directed backwards and being parallel to the surface of the body.
In the Urodela (Götte) the ulnar and fibular sides are primitively dorsal, and the radial and tibial ventral: in Mammalia however Kölliker states that the radial and tibial edges are from the first anterior.
The exact changes of position undergone by the limbs in the course of development are not fully understood. To suit a terrestrial mode of life the flexures of the two limbs become gradually more and more opposite, till in Mammalia the corresponding joints of the two limbs are turned in completely opposite directions.
Within the mesoblast of the limbs a continuous blastema becomes formed, which constitutes the first trace of the skeleton of the limb. The corresponding elements of the two limbs, viz. the humerus and femur, radius and tibia, ulna and fibula, carpal and tarsal bones, metacarpals and metatarsals, and digits, become differentiated within this, by the conversion of definite regions into cartilage, which may either be completely distinct or be at first united. These cartilaginous elements subsequently ossify.
The later development of the parts, more especially of the carpus and tarsus, has been made the subject of considerable study; and important results have been thereby obtained as to the homology of the various carpal and tarsal bones throughout the Vertebrata; but this subject is too special to be treated of here. The early development, including the succession of the growth of the different parts, and the extent of continuity primitively obtaining between them, has on the other hand been but little investigated; recently however the development of the limbs in the Urodela has been worked out in this way by two anatomists, Götte (No. 482) and Strasser (No. 487), and their results, though not on all points in complete harmony, are of considerable interest, more especially in their bearing on the derivation of the pentadactyloid limb from the piscine fin. Till however further investigations of the same nature have been made upon other types, the conclusions to be drawn from Götte and Strasser's observations must be regarded as somewhat provisional, the actual interpretation of various ontological processes being very uncertain.
The forms investigated are Triton and Salamandra. We may remind the reader that the hand of the Urodela has four digits, and the foot five, the fifth digit being absent in the hand[218]. In Triton the proximal row of carpal bones consists (using Gegenbaur's nomenclature) of (1) a radiale, and (2 and 3) an intermedium and ulnare, partially united. The distal row is formed of four carpals, of which the first often does not support the first metacarpal; while the second articulates with both the first and second metacarpals. In the foot the proximal row of tarsals consists of a tibiale, an intermedium and a fibulare. The distal row is formed of four tarsals, the first, like that in the hand, often not articulating with the first metatarsal, the second supporting the first and second metatarsals; and the fourth the fourth and fifth metatarsals.
[218] This seems to me clearly to follow from Götte and Strasser's observations.
The mode of development of the hand and foot is almost the same. The most remarkable feature of development is the order of succession of the digits. The two anterior (radial or tibial) are formed in the first instance, and then the third, fourth and fifth in succession.
As to the actual development of the skeleton Strasser, whose observations were made by means of sections, has arrived at the following results.
The humerus with the radius and ulna, and the corresponding parts in the hind limb, are the first parts to be differentiated in the continuous plate of tissue from which the skeleton of the limb is formed. Somewhat later a cartilaginous centre appears at the base of the first and second fingers (which have already appeared as prominences at the end of the limb) in the situation of the permanent second carpal of the distal row of carpals; and the process of chondrification spreads from this centre into the fingers and into the remainder of the carpus. In this way a continuous carpal plate of cartilage is established, which is on the one hand continuous with the cartilage of the two metacarpals, and on the other with the radius and ulna.
In the cartilage of the carpus two special columns may be noticed, the one on the radial side, most advanced in development, being continuous with the radius; the other less developed column on the side of the ulna being continuous both with the ulna and with the radius. The ulna and radius are not united with the humerus.
In the further growth the third and fourth digits, and in the foot the fifth digit also, gradually sprout out in succession from the ulnar side of the continuous carpal plate. The carpal plate itself becomes segmented from the radius and ulna, and divided up into the carpal bones.
The original radial column is divided into three elements, a proximal the radiale, a middle element the first carpal, and a distal the second carpal already spoken of. The first carpal is thus situated between the basal cartilage of the second digit and the radiale, and would therefore appear to be the representative of a primitive middle row of carpal bones, of which the centrale is also another representative.
The centrale and intermedium are the middle and proximal products of the segmentation of the ulnar column of the primitive carpus, the distal second carpal being common both to this column and to the radial column.
The ulnar or fibular side of the carpus or tarsus becomes divided into a proximal element--the ulnare or fibulare--the ulnare remaining partially united with the intermedium. There are also formed from this plate two carpals to articulate with digits 3 and 4; while in the foot the corresponding elements articulate respectively with the third digit, and with the fourth and fifth digits.
Götte, whose observations were made in a somewhat different method to those of Strasser, is at variance with him on several points. He finds that the primitive skeleton of the limb consists of a basal portion, the humerus, continued into a radial and an ulnar ray, which are respectively prolonged into the two first digits. The two rays next coalesce at the base of the fingers to form the carpus, and thus the division of the limb into the brachium, antebrachium and manus is effected.
The ulna, which is primitively prolonged into the second digit, is subsequently separated from it and is prolonged into the third; from the side of the part of the carpus connecting the ulna with the third digit the fourth digit is eventually budded out, and in the foot the fourth and fifth digits arise from the corresponding region. Each of the three columns connected respectively with the first, second, and third digits becomes divided into three successive carpal bones, so that Götte holds the skeleton of the hand or foot to be formed of a proximal, a middle, and a distal row of carpal bones each containing potentially three elements. The proximal row is formed of the radiale, intermedium and ulnare; the middle row of carpal 1, the centrale and carpal 4, and the distal of carpal 2 (consisting according to Götte of two coalesced elements) and carpal 3.
The derivation of the cheiropterygium from the ichthyopterygium. All anatomists are agreed that the limbs of the higher Vertebrata are derived from those of Fishes, but the gulf between the two types of limbs is so great that there is room for a very great diversity of opinion as to the mode of evolution of the cheiropterygium. The most important speculations on the subject are those of Gegenbaur and Huxley.
Gegenbaur holds that the cheiropterygium is derived from a uniserial piscine limb, and that it consists of a primitive stem, to which a series of lateral rays are attached on one (the radial) side; while Huxley holds that the cheiropterygium is derived from a biserial piscine limb by the "lengthening of the axial skeleton, accompanied by the removal of its distal elements further away from the shoulder-girdle and by a diminution in the number of the rays."
Neither of these theories is founded upon ontology, and the only ontological evidence we have which bears on this question is that above recorded with reference to the development of the Urodele limb.
Without holding that this evidence can be considered as in any way conclusive, its tendency would appear to me to be in favour of regarding the cheiropterygium as derived from a uniserial type of fin. The humerus or femur would appear to be the basipterygial bars (metapterygium), which have become directed outwards instead of retaining their original position parallel to the length of the body at the base of the fin. The anterior (proximal) fin-rays and the pro- and mesopterygium must be supposed to have become aborted, while the radius or ulna, and tibia or fibula are two posterior fin-rays (probably each representing several coalesced rays like the pro- and mesopterygium) which support at their distal extremities more numerous fin-rays consisting of the rows of carpal and tarsal bones.
This view of the cheiropterygium corresponds in some respects with that put forward by Götte as a result of his investigations on the development of the Urodele limbs, though in other respects it is very different. A difficulty of this view is the fact that it involves our supposing that the radial edge of the limb corresponds with the metapterygial edge of the piscine fin. The difficulties of this position have been clearly pointed out by Huxley, but the fact that in the primitive position of the Urodele limbs the radius is ventral and the ulna dorsal shews that this difficulty is not insuperable, in that it is easy to conceive the radial border of the fin to have become rotated from its primitive Elasmobranch position into the vertical position it occupies in the embryos of the Urodela, and then to have been further rotated from this position into that which it occupies in the adult Urodela and in all higher forms.
BIBLIOGRAPHY of the Limbs.
(477) M. v. Davidoff. "Beiträge z. vergleich. Anat. d. hinteren Gliedmaassen d. Fische I." Morphol. Jahrbuch, Vol. V. 1879.
(478) C. Gegenbaur. Untersuchungen z. vergleich. Anat. d. Wirbelthiere. Leipzig, 1864-5. Erstes Heft. Carpus u. Tarsus. Zweites Heft. Brustflosse d. Fische.
(479) C. Gegenbaur. "Ueb. d. Skelet d. Gliedmaassen d. Wirbelthiere im Allgemeinen u. d. Hintergliedmaassen d. Selachier insbesondere." Jenaische Zeitschrift, Vol. V. 1870.
(480) C. Gegenbaur. "Ueb. d. Archipterygium." Jenaische Zeitschrift, Vol. VII. 1873.
(481) C. Gegenbaur. "Zur Morphologie d. Gliedmaassen d. Wirbelthiere." Morphologisches Jahrbuch, Vol. II. 1876.
(482) A. Götte. Ueb. Entwick. u. Regeneration d. Gliedmaassenskelets d. Molche. Leipzig, 1879.
(483) T. H. Huxley. "On Ceratodus Forsteri, with some observations on the classification of Fishes." Proc. Zool. Soc. 1876.
(484) St George Mivart. "On the Fins of Elasmobranchii." Zoological Trans., Vol. X.
(485) A. Rosenberg. "Ueb. d. Entwick. d. Extremitäten-Skelets bei einigen d. Reduction ihrer Gliedmaassen charakterisirten Wirbelthieren." Zeit. f. wiss. Zool., Vol. XXIII. 1873.
(486) E. Rosenberg. "Ueb. d. Entwick. d. Wirbelsäule u. d. centrale carpi d. Menschen." Morphologisches Jahrbuch, Vol. I. 1875.
(487) H. Strasser. "Z. Entwick. d. Extremitätenknorpel bei Salamandern u. Tritonen." Morphologisches Jahrbuch, Vol. V. 1879.
(488) G. 'Swirski. Untersuch. üb. d. Entwick. d. Schultergürtels u. d. Skelets d. Brustflosse d. Hechts. Inaug. Diss. Dorpat, 1880.
(489) J. K. Thacker. "Median and paired fins. A contribution to the history of the Vertebrate limbs." Trans. of the Connecticut Acad., Vol. III. 1877.
(490) J. K. Thacker. "Ventral fins of Ganoids." Trans. of the Connecticut Acad., Vol. IV. 1877.