Book - The development of the chick (1919) 1

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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 I The Early Development to the End of the Third Day

Chapter I The Egg

The parts of a newly laid hen's egg are the shell, shell-membrane, albumen, uDd yolk. In an egg that has been undisturbed for a short time the yolk floats in the albumen with a whitish disc, the blastoderm about 4 mm. in diameter, on its upper surface. If the yolk be rotated, it will return to its former position in a few minutes, owing to the slightly lower specific gravity of the hemisphere containing the blastoderm. The blastoderm is the living part of the egg, from which the embrj^o and all its membranes are derived. It is already in a fairly advanced stage of development when the egg is laid. The yolk and blastoderm are enclosed within a delicate transparent membrane (vitelline membrane) which holds the fluid yolk-mass together. We may now consider some details of the structure and composition of the parts of the egg.

The shell is composed of three layers: (1) the inner or mammillary layer, (2) the intermediate spongy layer, and (3) the surface cuticle. The mammillary layer consists of minute calcareous particles about 0.01-0.015 mm. in diameter welded together, with conical faces impinging on the shell-membrane; the minute air-spaces between the conical inner ends of the mammillae communicate with the meshes of the spongy layer, which is several times as thick, and which is bounded externally by the extremely delicate shell cuticle. The spongy layer consists of matted calcareous strands. The shell cuticle is porous, but apparently quite structureless otherwise. The cuticular pores communicate with the mesh-work of the spongy layer; thus the entire shell is permeable to gases, and permits of embryonic respiration, and evaporation of water.

The shell-membrane consists of two layers, a thick outer layer next to the shell and a thinner one next the albumen. Both are composed of matted organic fibers (more delicate in the inner than in the outer layer), crossing one another in all directions. At the blunt end of the egg the two layers are separated and form a chamber containing air that enters after the egg is laid (Fig. 2).

Fig. 2. — Diagram of the hen's egg in section to show relations of the parts. A. C, Air chamber. Alb., Albumen. Bl., Blastoderm. Chal., Chalaza. I. S. M., Inner layer of the shell membrane. L., Latebra. N. L., Neck of Latebra. N. P., Nucleus of Pander. O. S. M., Outer shell membrane, p' v. s., Perivitelline space. S., Shell. V. M., Vitelline membrane. W. Y., White yolk. Y. Y., Yellow yolk.

The physical characteristics of the albumen are too well known to require description. A dense layer immediately next to the vitelline membrane is prolonged in the form of two spirally coiled opalescent cords towards the blunt and narrow ends of the egg respectively; these are the chalazse, so called from a fanciful resemblance to hail stones. The two chalazse are twisted in opposite directions. In a hard-boiled egg it is possible to strip off the albumen in concentric spiral layers from left to right from the broad to the small end of the egg.

The yolk and blastoderm are enclosed within the delicate vitelline membrane; the yolk is a highly nutritious food destined to be gradually digested and absorbed by the living cells of the blastoderm and used for the growth of the embryo. It is not of uniform composition throughout, but consists of two main ingredients known as the yellow and the white yolk. The yellow yolk makes up the greater part of the yolk-sphere; the main part of the white yolk is a flask-shaped mass, the bulb of which, known as the latebra, is situated near the center of the whole yolk, the neck rising towards the surface and expanding in the form of a disc (nucleus of Pander) situated immediately beneath the blastoderm (Fig. 2) ; at its margin this disc is continuous with a thin peripheral layer of white yolk that surrounds the entire mass. In addition there are several thin layers of white yolk concentric to the inner bulbshaped mass.i If an egg be opened, a dehcate hair inserted in the blastoderm to mark its position, and then boiled hard, a section through the hair and center of the yolk will show the above relations quite clearly. The white yolk does not coagulate so readily as the yellow yolk, and it may be distinguished by this property as well as by its Hghter color.

Both kinds of yolk are made up of innumerable spheres which are, however, quite different in each (Fig. 3). Those of the yellow yolk are on the whole larger than those of the white yolk (about 0.025-0.100 mm. in diameter) with extremely fine granular contents. There is no ^P fluid between the spheres. Those of the white yolk are smaller and more variable in size, ranging from the finest granules up to

1 The assertion that the thin layers that define the concentric stratification of the yellow yolk are of the nature of white yolk is traceable to Meckel V. Hemsbach, Leuckart, and Allen Thomson. His was not able to satisfy himself that the characteristic elements of the white yolk occur within these thin concentric lamellse (Untersuchungen ueber die erste Anlage des Wirbeltierleibes, p. 2).

Fig. 3. — Yolksphere s of the hen's egg; highly magnified. (After Foster and Balfour.)

A. Varieties of white yolk-spheres.

B. Yellow yolk

about 0.07 mm. The larger spheres of the white yolk contain several highly refractive granules of relatively considerable size as compared with those of the yellow spheres (Fig. 3), and such granules may have secondary inclusions. As we shall see later, the smaller granules of the white yolk extend into the germinal disc (forerunner of the blastoderm) and grade into minute yolkgranules contained within the living protoplasm.

The earlier investigators from the time of Schwann regarded the white yolk-spheres as actual cells (Schwann, Reichert, Coste, His). His especially laid great stress on this interpretation; he believed that they were derived from the cells of the ovarian follicle which migrated into the ovum in the course of ovogenesis, that they multiplied like other cells, and took part in the formation of certain embryonic tissues. Subsequently he abandoned this position as untenable. The white yolk spheres are now universally regarded as food matters of a particular sort.

The yolk and albumen are complex mixtures of many different substances, organic and inorganic, containing all the elements necessary for the growth of the embryo. Very little is known concerning the series of chemical changes that go on in them during incubation.

Chemical Composition of the Hen's Egg. — The following data on the chemical composition of the hen's egg are taken from Simon's Physiological Chemistry. For details and literature the student is referred to the standard text-books of physiological chemistry.



Water 47.19-5L49

Solids 48.51-42.81

Fats (olein, pahiiitin, and stearin) 21.30-22.84

Vitelline and other alhumens 15.63-15.76

Lecithin 8.43-10.72

Cholesterin 0.44- 1.75

Cerebrin 0.30

Mineral salts 3.33- 0.36

Coloring matters | q r -q Glucose J

Analysis of the Mineral Salts

Sodium (NaoO) 5.12- 6.57

Potassium (K/J) 8.05- 8.93

Calcium (CaO) 12.21-13.28



Magnesium (MgO) 2.07- 2.11

Iron (Fe203) 1.19- 1.45

Phosphoric acid, free (Pi'Og) 5.72

Phosphoric acid, combined 63.81-66.70

SiHcic acid 0.55- 1.40

Chlorine Traces.


Water 80.00-86.68

SoHds 13.22-20.00

Albumens 11.50-12.27

Extractives 0.38- 0.77

Glucose 0.10- 0.50

Fats and Soaps Traces

Mineral salts 0.30- 0.66

Lecithins and Cholesterin Traces.

Analysis of the Mineral Ash

Sodium (NaaO) 23.56-32.93

Potassium (KoO) 27.66-28.45

Calcium (CaO) 1.74- 2.90

Magnesium (MgO) 1.60- 3.17

Iron (Fe.Os) 0.44- 0.55

Chlorine (CI) 23.84-28.56

Phosphoric acid (P2O5) 3.16- 4.83

Carbonic acid (CO2) 9.67-11.60

Sulphuric acid (SO3) 1.32- 2.63

Silicic acid (SiO.O 0.28- 0.49

Fluorine (Fl) Traces.

The shell consists of an organic matrix of the nature of keratin impregnated with lime salts: calcium and magnesium carbonates about 97 %, calcium and magnesium phosphates about 1 %, keratin and water about 2 %, trace of iron.

The shell-membrane and the vitelline membrane are stated to consist of keratin or a closely allied substance.

Formation of the Egg. The organs of reproduction of the hen are the ovary and oviduct of the left side of the body. Although the right ovary and oviduct are formed in the embryo at the same time as those of the left side, they degenerate more or less completely in the course of development (see Chap. XIII), so that only functionless rudiments remain. This would appear to be correlated with the large size of the egg and the delicate nature of the shell, as there is not room for two eggs side by side in the lower part of the body-cavity.

Fig. 4. — Reproductive organs of the hen. (After Duval, based on a figure by Coste.) The figure is diagrammatic in one respect, namely, that two

The ovary lies at the anterior end of the kidney attached by a fold of the peritoneum (mesovarium) to the dorsal wall of the body-cavity. In a laying hen ova of all sizes are found from microscopic up to the fully formed ovum ready to escape from the follicle. Such an ovary is shown in Figure 4; the gradation in size of the ova will be noticed up to the one fully formed and ready to burst from its capsule. At 5 in this figure is shown a ruptured follicle, and the ovum which has escaped from this follicle is shown in the oviduct at 8. It will be seen that the part of the definitive hen's egg produced in the ovary is the so-called yolk. The blood-supply of the very vascular ovary is derived from the dorsal aorta, and the veins open into the vena cava inferior.

The oviduct is a large coiled tube (Fig. 4) which begins in a wide mouth with fringed borders, the ostium tuhce ahdominale (funnel or infundibulum) opening into the body-cavity near the ovary. It is attached by a special mesentery to the dorsal wall of the body-cavity, and opens into the cloaca. The following divisions are usually distinguished: (1) the funnel or infundibulum, (2) the albumen secreting portion, (3) the isthmus, (4) the uterus or shell-gland, (5) the vagina (Fig. 4). The albumen secreting portion includes all of the coiled tube; the isthmus is a short section next to the dilated uterus, and the vagina is the short terminal portion opening into the cloaca (Figs. 4 and 5).

The formation of an egg takes place as follows: the yolk, or ovum proper, escapes by rupture of the follicle along a preformed band, the stigma (Fig. 4-4), into the infundibulum, which swallows it, so to speak, and it is passed down by peristaltic contractions

ova are shown in the oviduct at different levels; normally but one ovum

is found in the oviduct at a time.

1, Ovary, region of young follicles. 2 and 3, Successively larger follicles. 4, Stigmata, or non-vascular areas, along which the rupture of the follicle takes place. 5, Empty follicle. 6, Cephalic lip of ostium. 7, Funnel of oviduct (ostium tubse ahdominale). 8, Ovum in the upper part of the ovidiic't. 9, Region of the oviduct in which the albumen is secreted. 10, Albumen surrounding an ovum. 11, Ovum. 12, Germinal disc. 13, Lower segment of albumen-secreting portion. 14, Lower part of the oviduct (uterus," shell-gland). 15, Rectum. 16, Reflected wall of the abdomen. 17, Anus, or external opening of cloaca.

of the oviduct. The escape of the ovum from the follicle is known as the process of ovulation. During its passage down the oviduct it becomes surrounded by layers of albumen secreted by the oviducal glands. The shellmembrane is secreted in the isthmus and the shell in the uterus (Fig. 5). The ovum is fertilized in the uppermost part of the oviduct and the cleavage and early stages of formation of the germ-layers take place before the egg is laid. The time occupied by the o\auii in traversing the various sections of the oviduct is as follows: Glandular portion of the oviduct three hours, isthmus one hour, uterus and laying sixteen to seventeen hours (combined observations of Patterson, and Pearl and Curtis). If the hen be disturbed eggs may be retained long after they are ready to be layed.

Some of the details of these remarkable processes deserve attention: the observations of several naturalists demonstrate that the ripe follicle is em

FiG. 5. — Uterus (shell-gland) of the hen cut open to show the fully formed egg. (After Duval.) 1, Cut surface of oviduct, region of

isthmus. 2 Reflected flap of uterus. ^j,^^^^j ^ ^j^^ ^^^^^^^ of the ovi 3, Egg ready to be laid. 4, Lower ^

extremity, or vaginal portion, of the duct before its rupture SO that

oviduct 5, Rectum. 6, Opeiiing of ^^^ ^^^^^^^ ^|^^g ^^^ ^^ ^^^^^

the oviduct into the cloaca. /, Open- , , ^

ing of the rectum into the cloaca. 8, the body-cavity, but into the

^^°^^^- oviduct itself. Coste describes

the process in the following way: In hens killed seventeen to twenty hours after laying I have observed all the stages of this remarkable process. In some the follicle, still intact and enclosing its egg, had already been swallowed, and the mouth of the oviduct, contracted around the stalk of the capsule, seemed to exert some pressure on it, in other cases the ruptured capsule still partly enclosed the egg which projected from the opening; in others finally the empty capsule had just deposited the egg in the entrance of the oviduct." According to Patterson the funnel of the oviduct becomes inactive as soon as an egg is received, but about the time of laying it becomes highly active and again clasps an egg follicle.

The existence of double-yolked eggs renders it probable that the oviduct can pick up eggs that have escaped into the bodycavity. But in some cases ova that escape into the body-cavity undergo resorption there.

Immediately after the ovum is received by the oviduct a special layer of albumen is secreted which adheres closely to the vitelline membrane and is prolonged in two strands, one extending up and the other down the oviduct ; these strands become the chalazse; the layer to which they are attached may, therefore, be called the chalaziferous layer (Coste) of the albumen. The Une joining the attachments of the chalazse is at right angles to the main axis of the ovum (that passing through the germinal disc) ; it is obvious, therefore, that there must be some antecedent condition that determines the position of the ovum in the oviduct; this is probably the position of the ovum in the folhcle, i.e., the relation of the germinal disc to the stigma, for the follicular orientation is apparently preserved in the oviduct. The question is of considerable importance because, as we shall see, the axis of the embryo is later bisected by a plane passing through the chalazse, and is therefore certainly determined at the time that the chalazffi are formed, and Bartelmez even traces it back to the earliest stages of the ovocyte.

After formation of the chalazse the ovum passes down the oviduct, rotating on the chalazal axis, and thus describing a spiral path; the albumen which is secreted abundantly in advance of the ovum is therefore wrapped around the chalaziferous layer and chalazse in successive spiral layers and the chalazse are revolved in spiral turns.

Only about 50 % of the white of the egg is formed by the albumen secreting portion of the oviduct; this is in the form of a dense layer formed of matted fibers; the shell membrane is deposited directly on this; and the more fluid portion of the albumen constituting 50% or more of its entire bulk enters through the shell membrane while the egg is in the isthmus and uterus (Pearl and Curtis, 1912).

Abnormal eggs are of two main kinds: those with more than one 3^olk, and enclosed eggs (ovum in ovo). Double-yolked eggs are obviously due to the simultaneous, or almost simultaneous, liberation of two yolks, and their incorporation in a single set of egg-membranes. The two yolks are usually separate in such cases and are derived, presumably, from separate follicles. But two yolks within a single vitelline membrane have been observed; such are in all probability products of a single follicle. Cases of three yolks within a single shell are extremely rare. The class of enclosed eggs includes those in which there are two shells, one within the other. In some cases the contents of the enclosed and the enclosing eggs are substantially normal, though of course the enclosing shell is abnormally large; in others the enclosed egg may be abnormal as to size (small yolk), or contents (no yolk). In all cases described, the enclosing egg possesses a yolk (Parker). Abnormal eggs of these three classes are of either ovarian or oviducal origin; doubled-yolked eggs and eggs with abnormal yolks are due to abnormal ovarian conditions; enclosed eggs to abnormal oviducal conditions, or to both ovarian and oviducal abnormalities. Assuming the normal peristalsis of the oviduct to be reversed when a fully formed egg is present, the egg would be carried up the oviduct a greater or less distance and might there meet a second yolk. If the peristalsis became normal again, both would be carried to the uterus and enclosed in a common shell. (For a fuller discussion of double eggs see G. H. Parker.)

Ovogenesis. The ovogenesis, or development of ova, may be divided into three very distinct stages. The first stage, or period of multiplication, is embryonic and ends about the time of hatching (in the chick) ; it is characterized by the small size of the ova and their rapid multiplication by division. The multiph'ing primitive ova are known as ovogonia. At the end of this period multiplication ceases and the period of growth begins. The ova, known as ovocytes of the first order, become enclosed in follicles; the size of the ovum constantly increases and the yolk is formed. The third period, known as the period of maturation, is characterized by two successive exceedingly unequal divisions of the egg-cell, producing two minute cells, the polar globules, that take no part in the formation of the embryo, but die and degenerate. The process of maturation begins in the fully ripe follicle and is completed after ovulation in the oviduct, while the ovum is being fertilized.

The origin of the primitive ova, their multiplication and the formation of the primordial follicles is described in Chapter XIII. In the young chick all the cell cords and cell nests (described in Chapter XIII) become converted into primordial follicles. During the egg-laying period there is a continuous process of growth and ripening of the primordial follicles, which takes place successively; the immense majority at any given period remain latent, but all stages of growth of egg follicles may be found in a laying hen.

A primordial follicle consists of the ovum surrounded by a single layer of cubical epithelial cells (granulosa or follicle cells); the fibers of the adjacent stroma have a concentric arrangement around the follicle forming the theca folhculi (Fig. 6 Str.). The ovum itself is a rounded cell with a large nucleus placed excentrically so as to define a primary axis of the ovum. In the protoplasm on one side of the nucleus is a concentrated mass of protoplasm, the yolk-nucleus, from w^hich rays extend, and minute fatty granules.

HoU derives the follicular cells in birds from the stroma, but on insufficient grounds. According to D'Hollander, they are derived, like the primitive ova, from the germinal epithelium, in which he agrees with the majority of his predecessors. He states that the period of multiplication of the ovogonia ends about the time of hatching; that the period of growth of the ovocytes begins at about the fourteenth da}- of incubation (seven days before hatching), and before the formation of the primordial follicle, which begins on the fourth day after hatching. Thus the periods of multipHcation and gro\\i^h overlap.

Although the nucleus (germinal vesicle of authors) is strongly excentric in position in the youngest ovocytes, it occupies a more nearly central position in those slightly older. When the ovum is about 0.66 mm. in diameter, it moves to the surface along the shortest radius and comes to lie almost in contact with the vitelline membrane (Fig. 7). It becomes elliptical, and later the outer surface is flattened against the vitelline membrane, the inner surface remaining convex (Fig. 8). The point on the surface to which the germinal vesicle migrates is situated away from the surface of the ovary, and thus in the position of the pedicle of

FiG. 6. — Primordial follicle from the ovary of the hen. (After Holl.)

Gr., Granulosa. N., Nucleus. Str., Stroma. Y. N., Yolk nucleus.

Fig. 7. — Section of an ovarian ovum of the pigeon; drawn from a preparation of Mr. J. T. Patterson. The actual dimensions of the ovum are 1.44 X 1.25 mm.

f. s., Stalk of follicle. G. V., Germinal vesicle. Gr., Granulosa. L., Latebra. p. P., Peripheral protoplasm, pr. f., Primordial folhcles. Th. ex., Theca externa. Th. int., Theca interna. Y. Y., Yellow yolk. Z. r., Zona radiata.

the follicle, when the latter projects from the surface of the ovary (Fig. 7). This determines the position of the future germ disc. The nucleus increases in size with the growth of the ovum; in the youngest ovocytes its diameter is about 9 /x; in the ripe ovum it is flattened and may measure 455 ju in diameter by 72 ^ in thickness.


While the nucleus is still near the center of the egg a very dense deposit of extremely fine granules is formed around it, and gradually extends out towards the periphery of the cell, but does not involve the peripheral layer of protoplasm. This central aggregation of yolk-granules represents the primordium of the latebra or central mass of the white yolk.

The ovum grows very slowly up to a diameter of about 6 millimeters, and all of the yolk found during this period belongs to the category of white yolk. Certain of these ova, but only a few at any one time, then suddenly begin to grow at an enormously increased rate, adding about 4 mm. to their diameter every twenty-four hours until the full size of al)out 40 mm. in diameter is attained. It is during this period that the concentric layers of yellow and white yolk are laid down in the periphery.

Riddle has studied this period by the ingenious method of feeding the stain Sudan III, which has an especial affinity for fat, to laying hens at definite time intervals. The stain attaches itself to fatty acids of the food which are taken up unchanged by the egg. The consequence is that during any period of Sudan III feeding a red stained layer of yolk is formed; so that it is possible by regulating the dose and interrupting the feedings to obtain ova with alternate bands of stained and unstained yolk. In this way he was able to show that a layer of yellow and of white yolk about 2 mm. in combined thickness on the average is laid down each twenty-four hours.

In a previous study the same author had shown that there is a daily rhythm of nutrition, associated with high and low blood pressure, which is responsible for the formation of the alternate fault-bars and fundamental bars of birds' feathers. It is this same claih^ rhythm that determines the concentric stratification of the yolk, yellow yolk being formed during the longer period of high blood pressure, and white yolk during the briefer nocturnal period of low pressure.

"The layer of white yolk of the hen's egg is then a growthmark left at the ever changing boundary of the ovum ; it represents the result of yolk formation under sub-optimal conditions." (Riddle.)

The germinal vesicle lies in a thickening of the peripheral layer of protoplasm known as the germinal disc, which is continuous, like the remainder of the peripheral protoplasm, in early


stages with the protoplasmic reticulum that forms the walls of the yolk- vacuoles. The germinal disc increases in extent and thickness, and the peripheral protoplasm disappears over most of the yolk. An inflow of the peripheral protoplasm into the disc appears very probable by analogy with the bony fishes where this process can be studied with great ease.

The method of formation of the neck of the latebra and the so-called nucleus of Pander, or peripheral expansion of the neck, follows more or less directly from the preceding account: As the circumference of the ovum enlarges, the germinal disc is carried out and leaves behind it a trail in which yellow yolk is not formed. When the ovum is fully grown, the exact boundaries between the protoplasmic germinal disc and the yolk are not determinable. The disc itself is charged with small yolk-granules which grade off very gradually into the white yolk lying around and beneath the disc.

The mode of nutrition of the ovum and the formation of the vitelhne membrane remain to be considered. The nutrition is conveyed from the highly vascular theca follicuh by way of the follicular cells, or membrana granulosa, to the ovum. The nutriment enters by diffusion; at no stage is there any evidence of immigration of sohd food particles, let alone entire cells, into the growing ovum. At an early stage a definite membrane is formed between the ovum and the folhcular cells, the zona radiata or primordium of the vitelhne membrane (Fig. 7). This is pierced by innumerable extremely minute pores which become narrow canals as the zona radiata increases in thickness. The •follicular cells and the peripheral layer of protoplasm of the ovum are connected by extremely dehcate strands of protoplasm that pass through the pores (Holl). In some way the nutriment of the ovum is conveyed through these strands.

The discussion as to whether the zona radiata is a product of the ovum itself or of the follicular cells seems to me to be largely academic and wih not be summarized here. There seems to be sufficient evidence of a primary true vitelline membrane secreted by the ovum itself, though this may not represent the entire zona radiata of older ova.

The third phase of ovogenesis, maturation or formation of the polar globules, is transferred to the next chapter, because it is overlapped by the process of fertihzation. It is not definitely known if maturation in birds may be completed without fertilization, but it seems probable that, as in many other animals, the completion of maturation is dependent on the stimulus of fertihzation. It is, however, essentially a process absolutely distinct from fertilization, and in some animals {e.g., echinids) is completed without fertilization.

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) 1. Retrieved from

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