Book - The development of the chick (1919) 14

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Lillie FR. The development of the chick. (1919) Henry Holt And Company New York, New York.

Lillie 1919: Introduction | Part 1 - 1 The Egg | 2 Development Prior to Laying | 3 Outline of development, orientation, chronology | 4 From Laying to Formation of first somite | 5 Head-fold to twelve somites | 6 From twelve to thirty-six somites | Part 2 - 7 External form of embryo and embryonic membranes | 8 Nervous system | 9 Organs of special sense | 10 Alimentary tract and appendages | 11 The body-cavities, mesenteries and septum transversum | 12 Later development of the vascular system | 13 Urinogenital system | 14 Skeleton | Appendix | Frank Lillie

Part II The Forth Day to Hatching, Organogeny, Development of the Organs

Chapter XIV The Skeleton

I. General

From an embryological point of view, tlie bones of the body, their associated cartilages, the ligaments that unite them together in various ways, and the joints should be considered together, as they have a common origin from certain aggregations of mesenchyme. The main source of the latter is the series of sclerotomes, but most of the bones of the skull are derived from the unsegmented cephalic mesenchyme.

Most of the bones of the body pass through three stages in their embryonic development: (1) a membranous or prechondral stage, (2) a cartilaginous stage, (3) the stage of ossification. Such bones are known as cartilage bones, for the reason that they are preformed in cartilage. Many (see p. 433 for list) of the bones of the skull, the clavicles and the uncinate processes of the ribs do not pass through the stage of cartilage, but ossification takes place directly in the membrane; these are known as membrane or covering bones. The ontogenetic stages of bone formation parallel the phylogenetic stages, membrane preceding cartilage, and the latter preceding bone in the taxonomic series. Thus, in Amphioxus, the skeleton (excluding the notochord) is membranous; in the lamprey eel it is partly membranous and partly cartilaginous; in the selachia it is mainly cartilaginous; in higher forms bone replaces cartilage to a greater or less degree. The comparative study of membrane bones indicates that they were primitively of dermal origin, and only secondarily grafted on to the underlying cartilage to strengthen it. Thus the cartilage bones belong to an older category than the membrane bones.

The so-called membranous or prechondral stage of the skeleton is characterized simply by condensation of the mesenchyme. Such condensations arise at various times and places described beyond, and they often represent the primordia of several future bony elements. In such an area the cells are more closely aggregated, the intercellular spaces are therefore smaller, and the area stains more deeply than the surrounding mesenchyme. There are, of course, stages of condensation in each case, from the first vague and undefined areas shading off into the indifferent mesenchyme, up to the time of cartilage or bone formation, when the area is usually well defined. In most of the bones, however, the process is not uniform in all parts; the growing extremities may be in a membranous condition while cartilage formation is found in intermediate locations and ossification has begun in the original center of formation; so that all three stages may be found in the primordium of a single bone {e.g., scapula). Usually, however, the entire element is converted into cartilage before ossification begins.

The formation of cartilage (chondrification) is brought about by the secretion of a homogeneous matrix of a quite special character, which accumulates in the intercellular spaces, and thus gradually separates the cells; and the latter become enclosed in separate cavities of the matrix; when they multiply, new deposits of matrix form between the daughter cells and separate them. As the original membranous primordium becomes converted into cartilage, the superficial cells flatten over the surface of the cartilage and form a membrane, the perichondrium, which becomes the periosteum when ossification takes place.

The process of ossification in the long bones involves the following stages in the chick:

  1. Formation of Perichondral Bone. The perichondrium deposits a layer of bone on the surface of the cartilage near its center, thus forming a bony ring, which gradually lengthens into a hollow cylinder by extending towards the ends of the cartilage. This stage is well illustrated in Fig. 231 A and in the long bones of Fig. 242; the bones of the wing and leg furnish particularly good examples; the perichondral bone is naturally thickest in the center of the shaft and thins towards the extremity of the cartilages.
  2. Absorption of Cartilage. The matrix softens in the center of the shaft and becomes mucous, thus liberating the cartilage cells and transforming the cartilage into the fundamental tissue of the bone marrow. This begins about the tenth day in the femur of the chick. The process extends towards the ends, and faster at the periphery of the cartilage {i.e., next to the perichondral bone) than in the center. In this way there remain two terminal, cone-shaped cartilages, and the ends of the cones project into the marrow cavity (Fig. 231 A).
  3. Calcification of Cartilage. Salts of lime are deposited in the matrix of the cartilage at the ends of the marrow cavity; such cartilage is then removed by osteoclasts, large multinucleated cells, of vascular endothelial origin, according to Brachet (seventeenth or eighteenth day of incubation).
  4. Endochondral Ossification. Osteoblasts within the marrow cavity deposit bone on the surface of the rays of calcified cartilage that remain between the places eaten out by osteoclasts, and on the irmer surface of the perichondral bone.

These processes gradually extend towards the ends of the bone, and there is never any independent epiphysial center of ossification in long bones of birds, as there is in mammals. The ends of the bones remain cartilaginous and provide for growth in length. Growth in diameter of the bones takes place from the periosteum, and is accompanied by enlargement of the marrow cavity, owing to simultaneous absorption of the bone from within. It is thus obvious that all of the endochondral bone is removed from the shaft in course of time; some remains in the spongy ends.

The details of the process of ossification will not be described here, and it only remains to emphasize a few points. At a stage shortly after the beginning of absorption of the cartilage in the center of the shaft, the perichondral bone is invaded by capillary vessels and connective tissue that break through into the cavity formed by absorption; it is supposed by many that osteoblasts from the periosteum penetrate at the same time. The marrow of birds is derived, according to the best accounts, from the original cartilage cells, which form the fundamental substance, together with the intrusive blood-vessels and mesenchyme. The endochondral osteoblasts are believed by some to be of endochondral origin (i.e., derived from cartilage cells), by others of periosteal origin. For birds, the former view seems to be the best supported.

Fig. 231 A. — Longitudinal section of the femur of a chick of 196 hours' incubation; semi-diagrammatic. (After Brachet.)

art. Cart., Articular cartilage. C. C, Calcified cartilage, end. B., Endochondral bone. M., Marrow cavity. P'ch., Perichondrium. P'os., Periosteum, p'os. B., Periosteal bone. Z. Gr., Zone of growth. Z. Pr., Zone of proliferation. Z. R., Zone of resorption.

In birds, calcification does not precede absorption of the cartilage, as it does in mammals, until the greater part of the marrow cavity is formed. The cones of cartilage, referred to above, that are continuous with the articular cartilages, are absorbed about ten days after hatching.

On the whole, perichondral ossification plays a more extensive role in birds than in mammals. The endochondral bone formation begins relatively much later and is less extensive. The bodies of the vertebrae, which ossify almost exclusively in an endochondral fashion, form the main exception to this rule.

Ossification in membrane proceeds from bony spicules deposited between the cells in the formative center of any given membrane bone. It spreads out from the center, the bony spicules forming a network of extreme delicacy and beauty. After a certain stage, the membrane bounding the surface becomes a periosteum which deposits bone in dense layers. Thus a membrane bone consists of superficial layers of dense bone, enclosing a spongy plate that represents the primitive bone before the establishment of the periosteum.

The formation of bones proceeds from definite centers in all three stages of their formation; thus we have centers of membrane formation, centers of chondrification and centers of ossification. Membranous centers expand by peripheral growth, cartilage centers expand by the extension of cartilage formation in the membrane from the original center of chondrification, and bony centers expand in the original cartilage or membrane. Several centers of chondrification may arise in a single primitive membranous center; for instance, in the membranous stage, the skeleton of the fore-limb and pectoral girdle is absolutely continuoiis; cartilage centers then arise separately in different parts for each of the bones: similarly for the hind-limbs and pelvic girdle, etc. Separate centers of ossification may likewise appear in a continuous embryonic cartilage, as for instance, in the base of the skull or in the cartilaginous coraco-scapula, or ischioilium. Such centers may become separate bones or they may subsequently fuse together. In the latter case, they may represent bones that were phylogenetically perfectly distinct elements, as for instance, the prootic, epiotic, and opisthotic centers in the cartilaginous otic capsule; or they may be of purely functional significance, as for instance, the separate ossifications in the sternum of birds, or the epiphysial and diaphysial ossifications of the long bones of mammals. It is usually possible on the basis of comparative anatomy to distinguish these two categories of ossification centers.

Phylogenetic reduction of the skeleton is also usually indicated in some manner in the embryonic history. Where elements have completely disappeared in the ph3dogenic history, as for instance, the missing digits of birds, they often appear as membrane formations in the embrvo, which then fade out without reaching the stage of cartilage; if the latter stage is reached the element usually fuses with some other and is therefore not really missing, e.g., elements of the carpus and tarsus of birds (though not all). But the ontogenetic reduction may go so far that the missing elements are never distinguishable at any stage of the embryonic history; thus, though the missing digits of birds are indicated in the membranous stage, their component phalanges are not indicated at all.

II. The Vertebral Column

The primordia of the vertebral column are the notochord and sclerotomes. The former is the primitive axial support of the body, both ontogenetically and phylogenetically. In both components, notochord and sclerotomes, we may recognize a cephalic and trunk portion. The notochord, as we have seen, extends far into the head, and the sclerotomes of the first four somites contribute to the formation of the occipital portion of the skull. The cephalic parts are dealt with in the development of the skull. The history of the notochord and sclerotomes will be considered together, but we may note in advance that the notochord is destined to be completely replaced by the bodies of the vertebrae, derived from the sclerotomes.

The Sclerotomes and Vertebral Segmentation. The vertebral segmentation does not agree with the primitive divisions of the somites, but alternates with it; or in other words, the centers of the vertebrae do not coincide with the centers of the original somites, but with the intersomitic septa in which the segmental arteries run. Thus each myotome extends over half of two vertebral segments, and the spinal ganglia and nerves tend to alternate with the vertebrae. It therefore happens that each myotome exerts traction on two vertebrae, obviously an advantageous arrangement, and the spinal nerves lie opposite the intervertebral foramina.

This arrangement is brought about by the development of each vertebra from the caudal half of one sclerotome and the cephalic half of the sclerotome immediately behind; parts of two somites enter into the composition of each vertebra, as is very obvious at an early stage: Fig. 232 represents a section through the base of the tail of a chick embryo of ninety-six hours; it is approximately frontal, but is inclined ventro-dorsally from behind forwards. The original somites are indicated by the myotomes and the segmental arteries. In the region of the notochord one can plainly distinguish three parts to each sclerotome, viz., (1) a narrow, median, or perichordal part abutting on the notochord, in which no cUvisions occur either within or between somites; (2) a caudal lateral cUvision distinguished by the denser aggregation of the cells from (3) the cephalic division. Between the caudal and cephalic cUvisions of the sclerotome is a fissure (intervertebral fissure) which marks the boundary of the future vertebrae. Each vertebra in fact arises from the caudal component of one sclerotome and the cephalic component of the sclerotome immediately behind. Between adjacent sclerotomes is the intersomitic septum containing the segmental artery. If one follows these conditions back into successively earlier stages, one finds that the intervertebral fissure arises from the primitive somitic cavity, and that the distinction between caudal and cephalic divisions of the sclerotome is marked continuously from a very early stage by the presence of the intervertebral fissure and the greater density of the caudal division, i.e., the cephalic component of each definitive vertebra.

Fig. 232.— Frontal section through the base of the tail of a chick embryo of 96 hours. The anterior end of the section (above in the figure) is at a higher plane than the posterior end. caud. Scl., Caudal division of the sclerotome, ceph Scl Cephalic division of the sclerotome. Derm., Dermatome. Ep., Epidermis. Gn., Ganglion, int's. F., Intersomitic fissure int'v F Intervertebral fissure. My., Mvotome. N'ch., Notochord Nt' Neural tube, per'ch. Sh., Perichordal sheath, s. A., Segmental artery.

Now, if one follows these components as they appear at successively higher levels in such a frontal section as Fig. 232, one finds that the perichordal layer disappears in the region of the neural tube, and that the spinal ganglia appear in the cephalic division of the sclerotome, and almost completely replace it. Thus the caudal division of the sclerotome is more extensive, as well as denser, than the cephalic division.

In transverse sections one finds that the sclerotomic mesenchyme spreads towards the middle line and tends to fill all the interspaces between the notochord and neural tube, on the one hand, and the myotomes on the other. But there is no time at which the sclerotome tissue of successive somites forms a continuous unsegmented mass in which the vertebral segmentation appears secondarily, as maintained by Froriep, except in the thin perichordal layer; on the contrary, successive sclerotomes and vertebral components may be continuously distinguished, except in the perichordal layer; and the fusion of caudal and cephalic sclerotome halves to form single vertebrae may be continuously followed. Thus, although the segmentation of the vertebrae is with reference to the myotomes and ganglia, it is dependent upon separation of original sclerotome halves, and not secondarily produced in a continuous mass.

Summarizing the conditions at ninety-six hours, we may say that the vertebrae are represented by a continuous perichordal layer of rather loose mesenchvme and two mesenchvmatous arches in each segment, that ascend from the perichordal layer to the sides of the neural tube; in each segment the upper part of the cephalic sclerotomic arch is occupied almost completely by the spinal ganglion, but the caudal arch ascends higher, though not to the dorsal edge of the neural tube. The cranial and caudal arches of any segment represent halves of contiguous, not of the same, definitive vertebra.

Membranous Stage of the Vertebrae. In the following or membranous stage, the definitive segmentation of the vertebrae is established, and the principal parts are laid down in the membrane. These processes are essentially the same in all the vertebrae, and the order of development is in the usual anteroposterior direction. As regards the establishment of the vertebral segments: Figs. 233 and 234 represent frontal sections through the same vertebral primordia at different levels from the thoracic region of a five-day chick. The notochord is slightly constricted intervertebrally, and the position of the intersegmental artery, of the myotomes and nerves, shows that each vertebral segment is made up of two components representing succeeding sclerotomes. In the region of the neural arches (Fig. 234) the line of union of cranial and caudal vertebral components is indicated by a slight external indentation at the place of union, and by the arrangement of the nuclei on each side of the plane of union.

Fig. 233. — Frontal section through the notochord and pri mordia of two vertebrae of a 5-day chick; thoracic region.

Note intervertebral constrictions of the notochord. The

anterior end of the section is above.

N., Spinal nerve. Symp., Part of sympathetic cord. v. C, Region of pleurocentrum, in which the formation of cartilage has hegun.

Other abbreviations as in Fig. 232.

The parts of the vertebrae formed in the membranous stage are as follows: (1) The vertebral body is formed by tissue of both vertebral components that grows around the perichordal sheath; (2) a membranous process (neural arch) extends from the vertebral body dorsally at the sides of the neural canal; but the right and left arches do not yet unite dorsally; (3) a lateral or costal process extends out laterally and caudally (Fig. 233) from the vertebral body between the successive myotomes.

The union of the right and left cephalic vertebral components (caudal sclerotome halves) beneath the notochorcl is known as the subnotochordal bar (Froriep). It forms earlier than the remainder of the body of the vertebra and during the membranous stage is thicker, thus forming a ventral projection at the cephalic end of the vertebral body that is very conspicuous (Fig. 235).

Fig. 234. — Frontal section including the same vertebral primordia as Fig. 233, at a higher level through the neural arches, a. C, Anterior commissure of the spinal cord. v. R., Ventral root of spinal nerve. Other abbreviations as before (Fig;. 232).

It chondrifies separately from the vertebral body and earlier. Except in the case of the first vertebra it fuses subsequently with the remainder of the vertebral body, and disappears as a separate component. Schauinsland has interpreted it as the homologue of the haemal arches of reptilia {e.g., Sphenodon).

The membrane represents not only the future bony parts but the ligaments and periosteum as well. Hence we find that the successive membranous vertebrae are not separate structures but are united by membrane, i.e., condensed mesenchyme, and are distinguishable from the future ligaments at first only by greater condensation. In the stage of Fig. 233, chondrification has already begun in the vertebral body, hence there is a sharp

Fig. 235. — Median sagittal section of the cervical region at

the end of the sixth day of incubation. (After Froriep.) x 40.

b. C, Basis cranii. iV. L. 1, 2, 3, First, second, and third intervertebral ligaments, s. n. b. 1, 2, 3, 4, First, second, third, and fourth subnotochordal bars (hypocentra). v. C. 3, 4, Pleurocentra of third and fourth vertebrae.

distinction in this region l^etween the vertebral bod}^ and intervertebral discs. The centers of chondrification, however, grade into the membranous costal processes and neural arches.

The vertebral segmentation has now become predominant as contrasted with the primitive somitic.

The development of the vertebrae during the fifth day comprises: (1) Fusion of successive caudal and cephalic divisions of the sclerotomes to form the definitive vertebrae; (2) union of the cephaUc vertebral components beneath the notochord to form the subnotochordal bar; (3) origin of the membranous vertebral bodies and of the neural arch and costal processes.

Chondrification, or development of cartilage, sets in from the following centers in each vertebra: (1) the cephalic neural arches and subnotochordal bar, forming a horseshoe-shaped cartilage at the cephalic end of each vertebra; (2) and (3) right and left centers in the body of each vertebra behind the subnotochordal bar, which soon fuse around the notochord; (the subnotochordal bar probably corresponds to the hypocentrum, and the lateral centers (2 and 3) to the pleurocentra of palaeontologists) ; (4) and (5) centers in each costal process (Figs. 235 and 236). These centers are at first separated by membrane, l)ut except in the case of the costal processes, which form the ribs, the cartilage centers flow together. The neural arches end in membrane which gradually extends dcrsally around the upper part of the neural tube, finally uniting above with the corresponding arches of the other side to form the memhrana reuniens. The chondrification follows the extension of the membrane. During this time the transverse processes of the neural arch and the zygopophyses are likewise formed as extensions of the membrane.

The distinction that some authors make between a primary vertebral l^ody formed ]:)y chondrification within the perichordal sheath, and a secondary vertebral body formed by the basal ends of the arches surrounding the primary, is not a clear one in the case of the chick.

On the seventh and eighth days the process of chondrification extends into all parts of the vertebra; the entire vertebra is, in fact, laid down in cartilage on the eighth da}', although the neural spine is somewhat membranous. Fig. 237 shows the right side of four trunk vertebrae of an eight-day chick, prepared according to the methylene b,lue method of Van Wijhe. The notochord runs continuously through the centra of the four vertebrae shown. It is constricted intra vertebrally and expanded intervertebrally, so that the vertebral bodies are amphicoelous. The intervertebral discs are not shown. A pre- and postzygapophysis is formed on each arch. It is by no means certain that the parts separated by the clear streak shown in the figure extending through centra and arches correspond to the sclerotomal components of the primitive vertebrae, though this was the interpretation of Schauinsland as shown in the figure; further study seems necessary to determine the exact relations of the primitive sclerotomal components to the parts of the definitive vertebra. The successive vertebrae have persistent membranous connections in the regions of the neural spines, zygapophyses and centra. These are shown in Figs. 238 and 239 (cf. also Fig. 150) ; they are continuous with the perichondrium and all are derived from unchondrified parts of the original membranous vertebrae.

Fig. 236. — Frontal section of the vertebral column and neighboring structures of a 6-day chick. Upper thoracic region. Note separate centers of chondrification of the neural arch, centrum, and costal processes. Anterior end of section above. B. n. A., Base of neural arch. br. N. 1, 2, 3, First, second, and third brachial nerves. Cp. R., Capitulum of rib. iv. D., Intervertebral disc. Mu., Muscles. N. A., Neural arch. T. R., Tuberculum of rib. V. C, Centrum of vertebra. Other abbreviations as before.

Fig. 237. — The right side of four bisected vertebrse of the trunk

of an 8-day chick. (After Schauinsland.)

caud. V. A., Caudal division of vertebral arch. ceph. v. A., Cephalic division of vertebral arch. N'ch., Xotochord.

Atlas and Axis (epistropheus). The first and second vertebrae agree with the others in the membranous stage. But, when chondrification sets in, the hypochordal bar of the first vertebra does not fuse with the body, but remains separate and forms its floor (Figs. 238 and 239). The body of the first vertebra chondrifies separately and is attached by membrane to the anterior end of the body of the second vertebra, representing in fact the odontoid process of the latter. It has later a separate center of ossification, but fuses subsequently wdth the body of the second vertebra, forming the odondoid process (Fig. 240).

Formation of Vertebral Articulations. In the course of development the intervertebral discs differentiate into a peripheral intervertebral ligament and a central suspensory ligament which at first contains remains of the notochord. There is a synovial cavity between the intervertebral and suspensory ligaments. This differentiation takes place by a process of loosening and resorption

Fig. 238. — Median sagittal section of the basis

cranii and first three vertebral centra of an

8-day chick.

B. C, Basi-cranial cartilage, iv. D. 1, 2, 3, 4,

First, second, third, and fourth intervertebral

discs. N. T., Floor of neural tube. s. n. b. 1, 2,

First and second subnotochordal bars. V. C.

1, 2, 3, First, second, and third pleurocentra.

of cells just external to the perichordal sheath (Fig. 241). The intervertebral ligament takes the form of paired, fibrous menisci, or, in other words, the intervertebral ligaments are incomplete around the bodies of the vertebrae dorsally and ventrally (Schwarck). Ossification is well advanced in the clavicles, long bones, and membrane bones of the skull before it begins in the vertebrae. It takes place in antero-posterior order, so that a series of stages may be followed in a single embryo (cf. Fig. 242). There are three main centers for each vertebra, viz., one in the body and one in each neural arch. The ossification of the centrum is almost

Fig. 239. — Lateral sagittal section of the same vertebrse (as in Fig.

238). At 1, 2, Floor and roof of atlas. B. C, Basis cranii. Cerv. n. 1, 2, First and second cervical nerves. Med. Obi., Medulla oblongata. R. V. 2, 3, 4, Ribs of the second, third, and fourth vertebrse. V . A. 2, 3, Arches of the second and third vertebrse. XII 2, Second root of hypoglossus.

entirely endochondral, though traces of perichondral ossification may be found on the ventral and dorsal surfaces of each centrum before the endochondral ossification sets in. The perichondral centers soon cease activity. The endochondral centers arise just outside the perichordal sheath near the center of each vertebra on each side of the middle line, but soon fuse around the notochord, and rapidly spread in all directions, but particularly towards the surface, leaving cartilaginous ends (Fig. 241). The notochord is gradually reduced and exhibits two constrictions

Fig. 240. — The first cervical vertebrae of a young

embryo of Haliplana fuliginosa. (After Schauins land.)

s.n.b. 1,2, First and second subnotochordal bars. R. 3, 4, 5, 6, Ribs of the third, fourth, fifth, and sixth cervical vertebrae.

and three enlargements within each centrum. The main enlargement occupies the center and the two smaller swellings the cartilaginous ends, the constriction occurring at the junction of the ossified areas and cartilaginous ends (Fig. 241).

Fig. 241. — Section through the body of a cervical vertebra of a chick embryo of about 12 days. (After Schwarck.)

1, Endochondral ossification. 2, Articular cartilages. 3, Notochord. 4, Loosening of cells of the intervertebral disc, forming a synovial cavity. 5, Periosteum. 6, Ligamentum suspensorium surrounding the notochord.

The centers of ossification in the neural arches arise from tlie perichondrium a short distance above the body of the vertebra, and form bony rings about the cartilaginous arch. They gradually extend into all the processes of the neural arch. Thus the neural arches are separated from the vertebral centra by a disc of cartilage which is, however, finally ossified, fusing the arches and centra. At what time this occurs, and at what time endochondral ossification begins in the arches, is not known exactly for the chick.

The vertebral column of birds is characterized by an extensive secondary process of coalescence of vertebrae. Thus the two original sacral vertebra? coalesce with a considerable number of vertebrae, both in front and behind, to form an extensive basis of support for the long iliac bones. The definitive sacrum may be divided into an intermediate primary portion composed of two vertebrge, an anterior lumbar portion, and a posterior caudal portion. The development of these fusions has not been, apparently, worked out in detail for the chick. The bony centers are all separate on the sixteenth day of incubation (cf. Fig. 249). Similarly, the terminal caudal vertebrae fuse to form the so-called pygostyle, which furnishes a basis of support for the tail feathers.

III. Development of the Ribs and Sternal Apparatus

In the membranous stage of the vertebral column, all of the trunk vertebra? possess membranous costal processes the subsequent history of which is different in different regions. In the cervical region these remain relatively short, and subsequently acquire independent centers of chondrification and ossification. The last two cervical ribs, however, acquire considerable length. In the region of the thorax, the membranous costal processes grow ventralward between the successive myotomes and finally unite in the formation of the sternum (q.v.). In the lumbar and sacral regions the membranous costal processes remain short. The primary costal process is an outgrowth of the membranous centrum, corresponding in position to the capitulum of the definitive ril). The tuberculum arises from the primary costal process while the latter is still in the membranous condition and grows dorsal ward to unite with the neural arch in the region of the transverse process. (See Fig. 236.)

The centers of chondrification and ossification of the typical ribs (cervical and thoracic) arise a short distance lateral to the vertebral centers, with which they are connected only by the intervening membrane, which forms the vertebro-costal ligaments. Chondrification then proceeds distally.

The cervical ribs chondrify from a single center. The thoracic ribs have two centers of chondrification; a proximal one, corresponding to the vertebral division of the rib. and a distal one corresponding to the sternal division. The lumbar and sacral membranous costal processes do not chondrify separately from the vertebral bodies; if they persist at all, therefore, they appear as processes of the vertebrae, and are not considered further.

In the fowl the atlas does not bear ribs, and in the embryo the primary costal processes of this vertebra do not chondrify. The second to the fourteenth vertebrae bear short ribs, with capitulum and tuberculum bounding the vertebrarterial canal. The fourteenth is the shortest of the cervical series. The fifteenth and sixteenth vertebrae bear relatively long ribs, but, as these do not reach the sternum, they are classed as cervical. The entire embryonic history, however, puts them in the same class as the following sternal ribs; on an embryological basis they should be classed as incomplete thoracic ribs. They possess no sternal division, but the posterior one has an uncinate process like the true thoracal ribs. The following five pairs of ribs (vertebrae 17-21) possess vertebral and sternal portions, but the last one fails to reach the sternal rib in front of it.

The vertebral and sternal portions of the true thoracal ribs meet at about a right angle in a membranous joint. This bend is indicated in the membranous stage of the ribs.

The membranous ribs growing downwards and backwards in the wall of the thorax make a sudden bend forward, and their distal extremities fuse (seven and eight days) in a common membranous expansion (primordium of the sternum), which, however, is separated from the corresponding expansion of the opposite side bv a considerable area of the body-wall.

The vertebral and sternal portions of the ribs ossify separately; the ossification of the ribs is exclusively perichondral up to at least the sixteenth day (cf. Fig. 242).

The uncinate processes were not formed in any of the embryos studied. Apparently they arise as separate membranous ossifications after hatching.

The sternum takes its origin from a pair of membranous expansions formed by the fusion of the distal ends of the first four true thoracal ribs; the fifth pair of thoracal ribs does not take part in the formation of the sternum. The sternum thus arises as two distinct halves, which lie at first in the wall of the thorax at the posterior end of the pericardial cavity (eight days). The greatest extension of the sternal primordia is do rso- ventral, the ventral extremities corresponding to the anterior end of the definitive sternum, which is formed by concrescence of the lateral halves in the middle line beginning at the anterior end. The concrescence then proceeds posteriorly, as the dorsal ends of the priraordia rotate backwards and downwards towards the middle line.

Fig. 242. — Photograph of the skeleton of a 13-day chick embryo. Prepared by the potash method. (Preparation and photograph by Roy L. Moodie.) 1, Premaxilla. 2, NasaL 3, lachrymaL 4, Parasphenoid. 5, Frontal. 6, Squamosal. 7, Parietal. 8, Exoccipital. 9, Cervical rib. 10, Coracoid. 11, Scapula. 12, Humerus. 13, Ilium. 14, Ischium. 15, Pubis. 16, Metatarsus. 17, Tibiofibula. 18, Palatine. 19, Jugal. 20, Maxilla. 21, Clavicle.

Although there are two lateral centers of chondrification, these soon fuse. The carina arises as a median projection very soon after concrescence in any region, and progresses backwards, rapidly following the concrescence. There is, therefore, no stage in which the entire sternum of the chick is ratite, though this condition exists immediately after concrescence in any region. The various outgrowths of the sternum (episternal process, anterolateral and abdominal processes), arise as processes of the membranous sternum and do not appear to have independent centers of chondrification.

The sternum ossifies from five centers, viz., a median anterior center and paired centers in the antero-lateral and abdominal processes. The last appear about the seventeenth day of incubation. On the nineteenth day a point of ossification appears at the base of the anterior end of the keel. At hatching centers also appear in the antero-lateral processes. The centers gradually extend, but do not completely fuse together until about the third month. The posterior end of the median division of the sternum remains cartilaginous for a much longer period. In the duck and many other birds there are only two lateral centers of ossification; the existence of five centers in the chick is, therefore, probably not a primitive condition.

IV. Development of the Skull

The skull arises in adaptation to the component organs of the head, viz., the brain, the sense organs (nose, eye, and ear) and cephalic visceral organs (oral cavity and pharynx); it thus consists primarily of a case for the brain, capsules for the sense organs, and skeletal bars developed in connection with the margins of the mouth and the visceral arches. In the chick, the primordia of the auditory and olfactory capsules are continuous ab initio with the primordial cranium; the protecting coat of the eye (sclera) never forms part of the skull. Therefore, we may consider the development of the skull in two sections, first the dorsal division associated with brain and sense organs (neurocranium), and second, the visceral division or splanchnocranium. Although the investment of the eyes forms no part of the skull, yet the eyes exert an immense effect on the form of the skull.

Development of the Cartilaginous or Primordial Cranium.

(1) The Neurocranium. The neurocranium is derived from the mesenchyme of the head, the origin of which has been described previously. The mesenchyme gradually increases in amount and forms a complete investment for the internal organs of the head. It is not all destined, however, to take part in the formation of the skeleton, for the most external portion forms the derma and subdermal tissue; and, internal to the skeletogenous layer, the membranes of the brain and of the auditory labyrinth, etc., are formed from the same mesenchyme.

The notochord extends forward in the head to the hypophysis (Figs. 67, 88, etc.), and furnishes a basis for division of the neurocranium into chordal and prechordal regions. Within the chordal division again, we may distinguish pre-otic, otic, and post-otic regions according as they are placed in front of, around, or behind the auditory sac. The part of the postotic region behind the vagus nerve is the only part of the neurocranium that is primarily segmental in origin. The sclerotomes of the first four somites (Figs. 63 and 117) form this part of the skull; and at least three neural arches, homodynamous with the vertebral arches, are formed in an early stage, but fuse together while still membranous, leaving only the two pairs of foramina of the twelfth cranial nerve as evidence of the former segmentation. It is also stated that membranous costal processes are found in connection with these arches, but they soon disappear without chondrifying.

The primordial neurocranium is performed in cartilage and corresponds morphologically to the cranium of cartilaginous fishes. However, it never forms a complete investment of the brain; except in the region of the tectum synoticum it is wide open dorsally and laterally. It is subsequently replaced by bone to a very great extent, and is completed and reinforced by numerous membrane bones.

The neurocranium takes its origin from two quite distinct primordia situated below the brain, viz., the parachordals and the trabecular. The former develop on each side of and around the notochord, being situated, therefore, behind the cranial flexure and beneath the mid- and hind-brain; the trabeculae are prechordal in position, being situated beneath the twixt-brain and cerebral hemispheres, and extending forward through the interorbital region to the olfactory sacs. It is obvious, therefore, that the parachordals and trabeculse must form with relation to one another the angle defined by the cranial flexure.

The parachordals appear in fishes as paired structures on either side of the notochord, uniting secondarily around the latter; but in the chick the perichordal portion is formed at the same time as the thicker lateral portions, so that the parachordals exist in the form of an unpaired basilar plate from the first. The trabeculae are at first paired (in the earliest membranous condition), but soon fuse in front, while the posterior ends form a pair of curved limbs (fenestra hypophyseos) that surrounds the infundibulum and hypophysis, and joins the basilar plate behind the latter. At the same time that the parachordals and trabeculae are formed by condensations of mesenchyme, the latter condenses also around the auditory sacs and olfactory pits in direct continuity with the parachordals and trabeculae respectively; so that the auditory and olfactory capsules are in direct continuity with the base of the neurocranium from the beginning.

Chondrification begins in the primordial cranium about the sixth day; it appears first near the middle line on each side, and extends out laterally. Somewhat distinct centers corresponding to the occipital sclerotomes may be found in some birds, but they soon run together, and the entire neurocranium forms a continuous mass of cartilage (sixth, seventh, and eighth days).

During this process the trabecular region increases greatly in length simultaneouslv with the outgrowth of the facial region, and the angle defined by the cranial flexure becomes thus apparently reduced. The posterior border of the fenestra hypophyseos marks the boundary between the basilar plate and trabecular region.

In the region of the basilar plate the following changes take place: (1) in the post-otic or occipital region a dorso-lateral extension (Fig. 244) fuses with the hinder portion of the otic capsule, thus defining an opening that leads from the region of the cavity of the middle ear into the cranial cavity (fissure metotica). This expansion is pierced by the foramina of the ninth tenth and eleventh nerves. (2) The otic region becomes greatly expanded by the enlargement of the membranous labyrinth. The cochlear process grows ventrally and towards the middle line and thus invades the original parachordal region (Fig. 168). The posterior region of the otic capsule expands dorsally above the hind-brain, and forms a bridge of cartilage extending from one capsule to the other, known as the tectum synoticum (Fig. 244, 33). (3) The preotic region expands laterally and dorsally in the form of a wide plate (alisphenoidal plate) which is expanded transversely, and thus possesses an anterior face bounding the orbit posteriorly and a posterior face forming part of the anterior wall of the cranial cavity. This plate arises first between the ophthalmic and maxillo-mandibular branches of the trigeminus, and subsequently sends a process over the latter that fuses with the anterior face of the otic capsule, thus establishing the foramen prooticum.

For an account of numerous lesser changes, the student is referred to Gaupp (1905), and the special literature (especially Parker, 1869). The various foramina for the fifth to the twelfth cranial nerves are defined during the process of chondrification ; the majority of these are shown in the figures.

The trabecular region may be divided into interorbital and ethmoidal (nasal) regions. The basis of the skeleton in this region is formed by the trabecule alread}^ described. The median plate formed by fusion of the trabeculse extends from the pituitary space (fenestra hypophyseos) to the tip of the head; a high median keel-like plate develops in the interorbital and internasal regions and fuses with the trabeculse, forming the septum interorbitale and septum nasi (Fig. 243). The free posterior border of this plate hes in front of the optic nerves; an interorbital aperture arises in tlie plate secondarily (Fig. 243).

Fig. 243. — Skull of an embryo of 65 mm. length; right side. Membrane bones in yellow. Cartilage in blue. (Drawn from the model of W. Tonkoff ; made by Ziegler.)

Fig. 244. — View of the base of the same model.

24.3-244. — 1, Squamosum. 2, Parietale. 3, Capsula auditiva. 4, Capsula auditiva (cochlear part). 5, Fissura metotica. 6, Epibranchial cartilage. 7, Sphenolateral plate. 8, Foramen prooticum. 9, Columella. 10. Otic process of quadratum. 11, Basitemporal (postero-lateral part of the parasphenoid). 12, Articular end of Meckel's cartilage. 13, Angulare. 14, Supra-angulare. 15, Dentale. 16, Skeleton of tongue. 17, Pterygoid. 18, Palatine. 19, Rostrum of parasphenoid. 20, Quadrato-jugal. 21, Jugal (zygomaticum). 22, Vomer. 23, Maxilla. 24, Premaxilla. 25, Anterior turbinal. 26, Posterior turbinal. 27, Nasale. 28, Prefrontal (lachrymale). 29, Antorbital plate. 30, Interorbital foramen. 31, Interorbital septum. 32,Frontale. 33, Tectum synoticum. 34, Foramen magnum. 35, Prenasal cartilage. 36, Orbital process of quadrate. 37, Articular process of Quadrate. 38. Fenestra basicranialis posterior. 39, Chorda. IX, Foramen glossopharyngei. X, Foramen vagi. XII, Foramina hypoglossei.

Fig. 245. — Visceral skeleton of the same model.

1, Dentale. 2, Operculare. 3, Angulare. 4, Supra-angulare. 5. Meckel's cartilage. 6, Entoglossum (cerato-hyal). 7, Copula (1). 8, Pharyngobranchial (1). 9, Epibranchial. 10, Copula (2),

In the ethmoidal region the septum nasi arises as an anterior continuation of the interorbital plate; and the trabecular plate is continued forward as a prenasal cartilage in front of the olfactory sacs. Curved, or more or less rolled, plates of cartilage develop in the axis of the superior, middle, and inferior turbinals (see olfactory organ), and these are continuous with the lateral wall of the olfactory capsules, which in its turn arises from the dorsal border of the septum nasi (Figs. 243 and 244).

(2) The Origin of the Visceral Chondrocranium (Cartilaginous Splanchnocranium) . The visceral portion of the cartilaginous skull arises primarily in connection with the arches that bound the cephalic portion of the alimentary tract, viz., oral cavity and pharynx. In the chick, cartilaginous bars are formed in the mandibular arch, hyoid arch, and third visceral arch. In fishes, the posterior visceral arches also have an axial skeleton, but hi the chick the mesenchyme of these arches does not develop to the stage of cartilage formation. The elements of these arches are primarily quite distinct. The upper ends of the mandibular and hyoid skeletal arches are attached to the skull; and the lower ends of the three arches concerned meet in the middle line. Two medial elements or copulse are formed in the floor of the throat, one behind the angle of the hyoid arch, and one behind the third visceral arch (Fig. 245).

Mandibular Arch. Two skeletal elements arise in the mandibular arch on each side, a proximal one (the palato-quadrate) and a distal one (Meckel's cartilage). The former is relatively compressed, and the latter an elongated element (Fig. 243, 10). The palato-quadrate lies external to the antero-vertral part of the auchtory capsule, and soon develops a triradiate form. The processes are: the processus oticus, which applies itself to the auditory capsule, the processus articidaris, which furnishes the articulation for the lower jaw, and the processus orhitalis, Avhich is directed anteromedially towards the orbit. A small nodule of cartilage of unknown significance lies above the junction of the processus oticus and otic labyrinth. Meckel's cartilage is the primary skeleton of the lower jaw, corresponding to the definitive lower jaw of selachians. It consists of two rods of cartilage in the rami of the mandibular arch, which articulate proximally with the processus articularis of the palatoquadrate cartilage,, and meet distally at the symphysis of the lower jaw. The form of the articulation of the lower jaw is early defined in the cartilage (seven to eight days).

Hyoid Arch. The skeletal elements of the hyoid arch consist of proximal and distal pieces (with reference to the neurocranium) which have no connection at any time. The former are destined to form the columella, and the latter parts of the hyoid apparatus. The columella apparently includes two elements (in Tinnunculus according to Suschkin, quoted from Gaupp) : a dorsal element, interpreted as hyomandibular, in contact with the wall of the otic capsule, and a small element (stylohyal) beneath the former. The two elements fuse to form the columella, the upper end of which is shown in Fig. 168. The stapedial plate (operculum of the columella) is stated to arise in Tinnunculus from the wall of the otic capsule, being cut out by circular cartilage resorption and fused to the columella.

The distal elements of the hyoid arch consist of (1) a pair of ceratohyals, which subsequently fuse in the middle line to form the entoglossal cartilage, the proximal ends remaining free as the lesser cornua of the hyoid, and (2) a median unpaired piece (copula I or basihyal) behind the united ceratohyals (Fig. 245).

First Branchial Arch. The skeletal elements of the third visceral (first branchial) arch are much more extensive than those of the hyoid arch. They are laid down as paired cerato- and epi-branchial cartilages on each side, and an unpaired copula II (basibranchial I) in the floor of the pharynx, in the angle of the other elements (Fig. 245). The cerato- and epibranchials increase greatly in length, and form the long curved elements (greater cornua) of the hyoid, which attain an extraordinary development in many birds.

Ossification of the Skull. The bones of the skull are of two kinds as to origin: (1) those that arise in the primordial cranium, and thus replace cartilage (cartilage bones or replacement bones), and (2) those that arise by direct ossification of membrane (membrane or covering bones).

The cartilage bones of the bird's skull are: (a) in the occipital region; the basioccipital, two exoccipitals, and the supraoccipitals; {h) in the otic region: prootic, epiotic, and opisthotic;

(c) in the orbital region: the basisphenoid, the orbitosphenoids, the ahsphenoids and ossifications of the interorbital septum; (d) in the ethmoidal region the bony ethmoidal skeleton; (e) the palatoquadrate cartilage furnishes the quadrate bone; (/) a proximal ossification, the articulare, arises in Meckel's cartilage and fuses later with membrane bones; (g) the upper part of the hyoid arch furnishes the columella, and the ceratohyals the os entoglossum; (h) the cerato- and epibranchials ossify independently, as also do the two copulse. (See Figs. 243, 244 and 245.)

The membrane bones of the skull are: (a) in the region of the cranium proper: parietals, frontals, squamosals; (6) in the facial region: lachrymals, nasals, premaxillae, maxillae, jugals, quadrato-jugals, pterygoids, palatines, parasphenoid, and vomer; (c) surrounding Meckel's' cartilage and forming the lower jaw: angulare, supra-angulare, operculare, and dentale. (See Figs. 243, 244 and 245.)

The embryonic bird's skull is characterized by a wealth of distinct bones that is absolutely reptilian; but in the course of development these fuse together so completely that it is only in the facial and visceral regions that the sutures can be distinguished readily.

In order of development the membrane bones precede the cartilage bones, though the latter are phylogenetically the older. Thus, about the end of the ninth day, the following bones are present in the form of delicate reticulated bars and plates: all four bones of the mandible, the faint outline of the premaxillae, the central part of the maxillae, the jugal and quadratojugal, the nasals, the palatines and pterygoids. The base of the squamosal is also indicated by a small triangular plate ending superiorly in branching trabeculae, delicate as frost-work. A faint band of perichondral bone is beginning to appear around the otic process of the quadrate, the first of the cartilage bones to show any trace of ossification. These ossifications appear practically simultaneously as shown by the examination of the earlier stages.

On the twelfth day these areas have expanded considerably, and the frontals and prefrontals (lachrymals) are formed; the rostrum of the parasphenoid is also laid down, and the exoccipitals appear in the cartilage at the sides of the foramen magnum. The parietals appear behind the squamosal (Fig. 242) about the thirteenth day; the basioccipitals soon after. The supraoccipital appears as a pair of ossifications in the tectum synoticum on each side of the dorsal middle line, subsequently fusing together.

A detailed history of the mode of ossification of all the various bones of the skull would be out of place in this book. The figures illustrate some points not described in the text. The reader is referred to W. K. Parker (1869) and to Gaupp (1905).

V. Appendicular Skeleton

The appendicular skeleton includes the skeleton of the limbs and of the girdles that unite the limbs to the axial skeleton. The fore and hind-limbs, being essentially homonymous structures, exhibit many resemblances in their development.

The Fore-limb

The pectoral girdle and skeleton of the wing develop from the mesenchyme that occupies the axis and base of the w^ng-bud, as it exists on the fourth day of incubation. It is probably of sclerotomic origin, but it is not known exactly how many somites are concerned in the chick, nor which ones. After the wing has gained considerable length (fifth day) it can be seen from the innervation that three somites are principally involved in the wing proper, viz., the fourteenth, fifteenth, and sixteenth of the trunk. But it is probable that the mesenchyme of the base of the wing-bud, from which the pectoral girdle is formed, is derived from a larger number of somites.

It is important, then, to note first of all that the scapula, coracoid, clavicle, humerus, and distal skeletal elements of the wing are represented on the fourth day by a single condensation of mesenchyme, which corresponds essentially to the glenoid region of the definitive skeleton. From this common mass a projection grows out distally in the axis of the wing-bud, and three projections proximally in different directions in the bodywall. These projections are (1) the primordium of the wingskeleton, (2) of the scapula, (3) of the coracoid, (4) of the clavicle.

The Pectoral Girdle

The elements of the pectoral girdle are thus outgrowths of a common mass of mesenchyme. The scapula process grows backward dorsal to the ribs; the coracoid process grows ventralward and slightly posterior towards the primordium of the sternum, thus forming an angle slightly less than a right angle with the scapular process; and the clavicular process grows out in front of the coracoid process ventrally and towards the middle hne. ThevSe processes are quite well developed on the fifth day, and increase considerably in length on the sixth day, when the hind end of the scapula nearly reaches the anterior end of the ilium, and the lower end of the coracoid is very close to the sternum. The elements are still continuous in the glenoid region.

About the end of the sixth day independent centers of chondrification appear in the scapula and coracoid respectively near their imion; these spread distally and fuse centrally, so that on the seventh day the coraco-scapula is a single bent cartilaginous element. In the angle of the bend, however (the future coraco-scapular joint), the cartilage is in a less advanced condition than in the bodies of the two elements. The clavicular process, on the other hand, never shows any trace of cartilage formation, either in early or more advanced stages, but ossifies directly from the membrane. It separates from the other elements of the pectoral girdle, though not completel}', on the eighth day.

The scapula and coracoid ossify in a perichondral fashion, beginning on the twelfth da}^, from independent centers, which approach but never fuse, leaving a permanent cartilaginous connection (Fig. 242). The clavicle, on the other hand, is a purely membrane bone; bony deposit begins in the axis of the membranous rods on the eighth or ninth days, soon forming fretted rods that approach in the mid-ventral line by enlarged ends, which fuse directly without the intervention of any median element about the twelfth to thirteenth day, thus forming the furcula or wish-bone (Fig. 246).

The nature of the clavicle in birds has been the subject of a sharp difference of opinion. On the one hand, it has been maintained that it is double in its origin, consisting of a cartilaginous axis (procoracoid) on which a true membrane bone is secondarily grafted (Gegenbaur, Fiirbringer, Parker, and others) ; on the other hand, all cartilaginous preformation in its origin has been denied by Rathke, Goette, and Kulczycki. After careful examination of series of sections in all critical stages, and of preparations made by the potash method, I feel certain that in the chick at least there is no cartilaginous preformation. It is still possible (indeed probable on the basis of comparative anatomy) that the theory of its double origin is correct phylogenetically; but it is certain that the procoracoid component does not develop beyond the membranous stage in the chick. It is interesting that the clavicle is the first center of ossification in the body, though perichondral ossification of some of the long bones begins almost as soon.

The Wing-bones

The primordium of the wing-bones is found in the axial mesenchyme of the wing-bud, which is originally continuous with the primordium of the pectoral girdle, and shows no trace of the future elements of the skeleton. The differentiation of the elements accompanies in general the external differentiation of the wing illustrated in Figs. 121 to 124, Chapter VII. The humerus, radius, and ulna arise by membranous differentiation in the mesenchyme in substantially their definitive relations; they pass through a complete cartilaginous stage and then ossify in a perichondral fashion (see Fig. 242). In the carpus, metacarpus, and phalanges, more elements are formed in the membrane and cartilage than persist in the adult. Elimination as well as fusion takes place. These parts will therefore require separate description.

Fig. 246. — Photograph of the pectoral girdle of a chick embryo of 274 hours; prepared by the potash method. (Preparation and photograph by Roy L. Moodie.)

1, Coracoid. 2, Clavicle. 3, Scapula. 4, Humerus.

As birds have descended from pentadactyl ancestors with subsequent reduction of carpus, metacarpus, and phalanges, it is naturally of considerable interest to learn how much of the ancestral history is preserved in the embryology. The hand is represented in the embryo of six days by the spatulate extremity of the fore-limb, which includes the elements of carpus, metacarpus, and phalanges. From this expansion five digital rays grow out simultaneously, the first and fifth being relatively small; the second, third, and fourth represent the persistent digits. In each ray is a membranous skeletal element, which, however, soon disappears in the first and fifth. Thus there are distinct indications of a i^entadactyl stage in the development of the bird's wing.

In the definitive skeleton there are but two carpal bones, viz., a radiale at the extremity of the radius, and an ulnare at the extremity of the ulna. In the embryo there is evidence of seven transitory pieces in the carpus arranged in two rows, proximal and distal (Fig. 247). In the proximal row only two cartilages appear, viz., the radiale and ulnare; but in earlier stages each appears to be derived from two centers: the radiale from a radiale s.s. and an intermedium, the ulnare from an ulnare s.s. and a centrale. Evidence of such double origin of each is found also in the cartilaginous condition {v. Parker, 1888). Four elements in all enter into the composition of this proximal row. In the distal row there are three distinct elements corresponding to the three persistent digits, and representing, therefore, carpalia II, III, and IV. These subsequently fuse with one another, and with the heads of the metacarpals to produce the carpometacarpus.

Fig. 247. — Skeleton of the wing of a chick embryo of 8 days. (After W. K. Parker.)

Cp. 2, 3, and 4, Second, third, and fourth carpalia. C. U., Centraloiilnare. H., Humerus. I. R., Intermedio-radiale. M'c. 2, 3, 4, Second, third, and fourth metacarpalia. P'ch., Perichondral bone R., Radius. U., Ulna.

On the seventh day the metacarpus is represented Ijy three cartilages corresponding to the three persistent digits, viz., II, III, IV. Metacarpal II is only about one third the length of III. Metacarpal IV is much more slender than III, and is bowed out in the middle, meeting III at both ends. The elements are at first distinct, but II and III fuse at their proximal ends in the process of ossification. Cartilaginous rudiments of metacarpals I and V have also been found by Parker, Rosenberg, and Leighton. As to the phalanges, Parker finds two cartilages in II, three in III, and two in IV on the seventh day; but already on the eighth day the distal phalanges of III and I^' have fused with the next proximal one.

As regards the homology of the digits of the wing, the author has adopted the views of Owen, Mehnert, Norsa, and Leighton, that they represent numbers II, III, and IV, which seem to be better supported by the embryological evidence than the view of ^Meckel, Gegenbauer, Parker, and others, that they represent I, II, and HI.

The Skeleton of the Hind-limb

The skeleton of the hindlimb and pelvic girdle develops from a continuous mass of mesenchyme situated at the base of the leg-bud. The original center of the mass represents the acetabular region; it grows out in four processes: (1) a lateral projection in the axis of the leg-bud, the primordium of the leg-skeleton proper, (2) a dorsal process, the primordium of the ilium; and two diverging ventral processes, one in front of the acetabulum (3) the pubis, and one behind (4) the ischium. In the membranous condition the elements are continuous. The definitive elements develop either as separate cartilao-e centers in the common mass (usually), or as separate centers of ossification in a common cartilaginous mass (ilium and ischium).

The Pelvic Girdle. The primitive relations of the elements of the pelvic girdle in Larus ridibundus is shown in Fig. 248, which represents a section in the sagittal plane of the body, and thus does not necessarily show the full extent of any of the cartilaginous elements, but only their general relations. The head of the femur is seen in the acetabulum, the broad plate of the ilium above and the pubis and ischium as cartilaginous rods of almost equal width below, the pubis in front and the ischiimi behind the acetabuhmi. In this stage the pehdc girdle, in this and many other species of birds, consists of three separate elements on each side in essentially reptilian relations.

In the chick at a corresponding age the ihum is much more extensive, and the ischium is united with it by cartilage- the pubis, however, has only a membranous connection with the ilium (contra Johnson). In the course of development the distal ends of the ischium and pubis rotate backwards until the two elements come to lie substantially parallel to the ilium (Figs. 242 and 249). The displacement of the ischium and pubis may

Fig. 248. — Sagittal section of the right half of the body of Lams ridibundus, to show the composition of the pelvic girdle; x 35. Length of the leg-bud of the embryo, 0.4 mm. (After Mehnert.) F., Femur, cr. N., Crural nerve. II., Ihum. I. s., Ischium. Is. N., Ischial nerve, ob. N., Obturator nerve. P., Pubis.

be associated wdth the upright gait of birds; it is fully established on the eighth day in the chick. The mode of ossification, which is perichondral, is shown in Fig. 249.

Later, the ilium obtains a very extensive pre- and postacetabular union with the vertebrae. I have fomid no evidence in a complete series of preparations (potash) of attachment by ribs arising as indei^endent ossifications. The ischium also fuses with the ventral posterior border of the iUum, and the pubis, except at its anterior and posterior ends, with the free border of the ischium.

The spina iliaca, a pre-acetabular, bony process of the ihum, requires special mention inasmuch as it has been interpreted (by Marsh) as the true pubis of birds, and the element ordinarily named the pubis as homologous to the post-pubis of some reptiles. There is no evidence for this in the development. The spina iliaca develops as a cartilaginous outgrowth of the ilium and ossifies from the latter, not from an independent center (Mehnert).

The Leg-skeleton. The skeleton of the leg develops from the axial mesenchyme, which is at first continuous with the primordium of the pelvic girdle. In the process of chondrification it segments into a larger number of elements than found in the adult, some of which are suppressed and others fuse together. The digits grow out from the palate-like expansion of the primitive limb in the same fashion as in the wing. In general the separate elements arise in the proximo-distal order (Figs. 242 and 249).

The femur requires no special description; ossification begins on the ninth day.

Fig. 249. — Photograph of the skeleton of the leg of a chick embryo of 15 days' incubation. Prepared by the potash method. (Preparation and photograph by Roy L. Moodie.)

1, Tibia. 2, Fibula. 3, Patella. 4, Femur. 5, Ilium. 6, Pleurocentra of sacral vertebrae. 7, Ischium. 8, Pubis. 9, Tarsal ossification. 10, Second, third, and fourth metatarsals. 11, First metatarsal. I, II, III, IV, First, second, third, and fourth digits.

The primordium of the fibula is from the first more slender than that of the tibia, though relatively far larger than the adult fibula. The fibular cartilage extends the entire length of the crus, but ossification is confined largely to its proximal end; on the fourteenth day its lower half is represented by a thread-like filament of bone. '

No separate tarsal elements are found in the adult; but in the embryo there are at least three cartilages, viz., a fibulare, tibiale and a large distal element opposite the three main metatarsals. In the course of development, the two proximal elements fuse with one another, and with the distal end of the tibia. The distal element fuses with the three main metatarsals, first with the second, then with the fourth, and lastly with the third (Johnson).

Five digits are formed in the membranous stage of the skeleton. In the case of the fifth chgit, only a small nodule of cartilage (fifth metatarsal) develops and soon disappears. The second, third, and fourth are the chief digits; the first is relatively small. ^Metatarsals 2, 3, and 4 are long and ossify separately in a perichondral fashion. They become applied near their middle and fuse with one another and with the distal tarsal element to form the tarso-metatarsus of the adult (Fig. 250). The first metatarsal is short, lying on the preaxial side of the distal end of the others (Fig. 249); it ossifies after the first phalanx. The number of phalanges is 2, 3, 4, and 5 in the first, second, third, and fourth digits respectively (Fig. 249).

The patella is clearly seen in potash preparations of thirteen-day chicks. At the same time there is a distinct, though iiiiiuite, separate center of ossification in the tarsal region (Fig. 249).

Fig. 250. — Photograph of the skeleton of the foot of a chick embryo of 15 days' incubation. (Preparation and photograph by Roy L. Moodie) 1, 2, 3, 4, First, second, third, and fourth digits. M 2, M 3, M 4, Second, third, and fourth metatarsals.

Lillie 1919: Introduction | Part 1 - 1 The Egg | 2 Development Prior to Laying | 3 Outline of development, orientation, chronology | 4 From Laying to Formation of first somite | 5 Head-fold to twelve somites | 6 From twelve to thirty-six somites | Part 2 - 7 External form of embryo and embryonic membranes | 8 Nervous system | 9 Organs of special sense | 10 Alimentary tract and appendages | 11 The body-cavities, mesenteries and septum transversum | 12 Later development of the vascular system | 13 Urinogenital system | 14 Skeleton | Appendix | Frank Lillie

Cite this page: Hill, M.A. (2024, April 17) Embryology Book - The development of the chick (1919) 14. Retrieved from

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