Book - Introduction to Vertebrate Embryology 1935-1
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Shumway W. Introduction to Vertebrate Embryology. (1935) John Wiley & Sons, New York
- Shumway (1935): Preface - Contents | Part I. Introduction | Part II. Early Embryology | Part III. Organogeny | Part IV. Anatomy of Vertebrate Embryos | Part V. Embryological Technique
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Introduction to Vertebrate Embryology (1935)
Part I Introduction
Chapter I The Study Of Embryology
Embryology may be defined as that division of biological science which deals with the development of the individual organism. It is concerned with the orderly series of changes in form and function through which the initial germ of the new individual is transformed into a sexually mature adult. Among vertebrate animals, at least, the germ with which development commences is normally an egg that has been fertilized by a sperm. The sexually mature adult is an individual which has developed to a point where it can produce mature eggs if a female, or sperms if a male. Sometimes the word ontogeny is used as a synonym for embryology, but more often it is defined to include the entire life history of an individual from its origin to its death.
Early embryologists. — The earliest treatise on embryology which has been preserved is that of Aristotle (3884-322 B.c.) entitled ‘‘ De Generatione Animalium,” — concerning the generation of animals. This work describes the reproduction and development of many kinds of animals. It contains the first account of the development of the hen’s egg, day by day, so far as it could be seen with the naked eye. Comparing the different types of reproduction, Aristotle placed the mammals first, for, being unable to discover the egg, he thought that their young arose from a mixture of male and female fluids and were ‘“ born alive.” Sharks, on the other hand, arose from eggs which were retained within the body of the mother and so were also born alive. Next he placed the type of reproduction shown by reptiles and birds in which the egg is “‘ complete,” that is to say, furnished with albumen and a shell. Lowest among the vertebrates were the amphibians and bony fish with “ incomplete” eggs. His account of development showed ‘great powers of observation, skill in comparison, and imagination in interpretation. Notable among his speculations is one which has been given the name of “ epigenesis.” From his observations on the development of the hen’s egg he concluded that development always proceeds from a simple formless beginning to the complex organization of the adult.
Another famous name in embryology is that of William Harvey (1578-1657). His book (‘ Exercitationes de Generatione Animalium ’’) is largely based on the development of the chick, which he described in great detail, although he too was limited by the fact that the microscope had not yet come into general use. One of his contributions was a careful study of the development of the deer, which he compared with that of the chick. From purely theoretical considerations he came to the conclusion that mammals also formed eggs, and is responsible for the dictum “ Ex ovo omnia ”’ — all animals arise from eggs.
After the invention of the microscope, Marcello Malpighi (1628-1694) published an account of the development of the hen’s egg (‘‘ De Ovo Incubato ”’), illustrated with excellent figures of development from the 24-hour stage of incubation on. His work was responsible for a theory of “ preformation ” as opposed to Aristotle’s ‘ epigenesis.”” On theoretical grounds, he held that the various parts of the embryo were contained in the egg and became visible as they increased in size. The enthusiasm resulting from the remarkable discoveries made with the newly invented microscope led to many later and wholly imaginative accounts of homunculi — miniature adults — in eggs or sperms, respectively.
Caspar Friedrich Wolff (1733-1794), in a highly theoretical treatise (“‘ Theoria Gencrationis ’’), attacked the theory of preformation on logical grounds. A more important contribution on the development of the intestine in the chick demonstrated that the tubular intestine arose from the folding of a flat layer in an earlier stage of incubation. This was a direct refutation of the preformationist idea that the intestine was tubular from the beginning.
Comparative embryology. — Karl Ernst von Baer (1792-1876) is known as the “ father of modern embryology.”’ He discovered the egg of mammals in 1827 and published a book on animal development (1828 and 1837) in which he compared in detail the development of different animals. From these he drew four important conclusions, known as von Baer’s laws.
- The more general characteristics of any large group of animals appear in the embryo earlier than the more special characteristics.
- After the more general characteristics those that are less general arise and so on until the most special characteristics appear.
- The embryo of any particular kind of animal grows more unlike the forms of other species instead of passing through them.
- The embryo of a higher species may resemble the embryo of a lower species but never resembles the adult form of that species.
From the time of von Baer up to the present the history of embryology has been marked by increasing specialization. Thus there is a comparative embryology of the vertebrates and a comparative embryology of the invertebrates. There are also other divisions of embryology which will be indicated briefly in the following paragraphs.
Cellular embryology. — Soon after the first volume of von Baer’s treatise appeared, Schleiden and Schwann (1838, 1839) announced the cell theory, namely that all living things are composed of, and arise from, living units known as cells. This resulted in an intensive study, commencing in the latter part of the nineteenth century, of the germ cells, their origin and fertilization, which led Sutton in 1901 to the chromosomal theory of inheritance. In 1878 Charles Otis Whitman (1842-1910) traced for the first time the detailed history of the cells formed by the dividing egg (in the leech, Clepsine), thereby initiating the study of cell lineage. Cellular embryology is a subject which unites embryology with cytology, the study of the cell and its activities.
Genetics and embryology. — In 1866, Gregor Mendel (18221884) first carried on successfully experiments in breeding plants to discover the laws by which individual characteristics are inherited from one generation to another. His conclusions, now known as Mendel’s laws, will be discussed in a later chapter. His contributions were long unrecognized, but in 1900 they were 6 THE STUDY OF EMBRYOLOGY
rediscovered and in the following year Sutton first suggested that the behavior of the chromosomes afforded a mechanical explanation of these laws. This has led to the theory of the gene, a name proposed for the unit of heredity by Johannsen (1911). This theory in the hands of T. H. Morgan has assumed great importance to the embryologist, for, to quote from Brachet, ‘‘ Embryology is fundamentally the study of heredity in action.”
Phylogeny and embryology. — In 1866, Ernst Haeckel (1834— 1919) published a theory which he believed supported Darwin’s theory of evolution and which he called the ‘“‘ fundamental biogenetic law.”’ It is more often known as the recapitulation theory. This theory states that ontogeny is a brief and incomplete recapitulation of phylogeny, or that an animal passes through stages in its development comparable to those through which its ancestors passed in their evolution. So far as the vertebrates are concerned, this would mean that a mammalian embryo should pass through stages which are definitely fish-like and later through stages which are essentially reptilian. The fact is that, although there are individual characteristics which at times are reminiscent of fish-like or reptilian ancestors, there is never a time in the development of a mammal when it could be mistaken for a fish or a reptile. There are evidences that the vertebrates do retain in development certain features which also appeared in the development of their ancestors. For example, clefts appear in the pharynx of the embryos of birds and mammals, opening to the exterior just as they do in the embryos of fish. In the adult fish these clefts contain the gills, but this is not true of adult reptiles or birds. It has been found very difficult, if not impossible, to draw up a genealogical tree of the vertebrates based solely on embryological data, and the recapitulation theory is not so widely accepted as in former times.!
Experimental embryology. — Among Haeckel’s contemporary opponents was Wilhelm His (1831-1904), who directed attention to the physiology of the embryo. Denying the theory of recapitulation, he called attention to the mechanical processes by which the various structures of the embryo arise from particular regions of the germ. Later, Wilhelm Roux (1850-1924) put the study of experimental embryology on a firm basis when he pub 1 Shumway. 1982. ‘“ The Recapitulation Theory,” Quart. Rev. Biol. 7:93-99. CHEMICAL EMBRYOLOGY 7
lished a program for the new science which he called “ the mechanics of development.” This has led to an intensive attack upon the problems of development from the physico-chemical side which is carried on actively at the present time. Weismann (1834-1913), a leader in theoretical embryology, suggested a theory of chromosomal inheritance which came very close to the mark. Jacques Loeb (1859-1924) discovered a method of inducing development in unfertilized eggs (artificial parthenogenesis) which has led to extensive research on the nature of fertilization.
|Embryology in the classic period|
|4th century B.C.||Aristotle|
|Embryology in the Renaissance period|
|(Before the general use of the microscope)|
|(After the general use of the microscope)|
|Embryology in modern times|
|1839||von Baer||Comparative embryology|
|1839||(Schleiden and Schwann announced cell theory)|
|1859||(Darwin announced theory of natural selection)|
|1866||(Mendel announced laws of inheritance)|
|(Microscopic technique being developed)|
|1883||Roux||Mechanics of development|
|1891||Weismann||Theory of the germplasm|
|1900||(Rediscovery of Mendel’s laws)|
Chemical embryology. — No attempt is made to mention the names of men still alive who have contributed to our knowledge of embryology, for the roll of distinguished zodélogists here and abroad would have to be called. Yet it may be admissible to comment on the recent appearance of a monumental work in three volumes by Joseph Needham, entitled "Chemical Embryology," which seems to chart the course for still a new subscience in embryology.
The value of embryology. — To the student who specializes in zodlogy, embryology has a particular importance because it deals with the origin and development of the adult body. There is a fascination in tracing out the history of the different anatomical structures as they take form, grow, and gradually assume the appearance familiar to us in the mature animal. And in the history of the different organs are found clues to their relationships and functions. Iiveryone knows, for example, that the adrenal gland secretes a hormone, epinephrin, which, circulating in the blood, rouses the autonomic nervous system to greater activity. But in embryology the student learns that the part of the adrenal gland which secretes epinephrin is derived from those same ganglia which give rise to the autonomic nerves.
He also finds clues to ancestral relationships. Even though the recapitulation theory has been abandoned as an explanation of development, embryologists recognize that there are structures in the body which correspond to similar parts used for the same or different purposes in the bodies of some distant ancestor. The “ retention theory ” has been proposed by de Beer as an explanation. Thus the vestigial tail of the human embryo arises in the same place and manner as the tails of other vertebrates, and we have no doubt but that some remote prehuman ancestor sported and made use of a tail. The embryo retains this tail, not as a recapitulation of ancestral history, but because it inherits the genes which initiate the development of a tail. So the student of comparative anatomy often turns to embryology hoping to find homologies in the mode of origin and manner of development of the adult organs in which he is interested.
The modern student of embryology is concerned mainly with the dynamics of development. He examines the protoplasmic organization of the egg and the sperm, their genetic constitution, and the nature of the process in which the sperm initiates development in the egg. He traces the history of the different cells into which the egg divides and tries to learn the way in which that differentiation takes place. He is interested in the mechanics of the processes by which these cells arrange themselves into the different germ layers, and how the different organs arise.
To these problems he brings the methods of descriptive embryology: the delicate technique of preparing embryological material, the skilled use of the microscope and its accessories, the interpretation and reconstruction of his prepared material. He also uses the methods of experimental embryology: the alteration of the normal conditions of development; new genetic complexes; altered environmental conditions at different stages of development; the development of individual cells or parts of the embryo in isolation or transplanted into new positions or different hosts.
Embryology is not an casy subject. It requires a high type of visual imagination. The student must bear in mind that he is dealing with living objects, three-dimensional and continually changing in volume, shape, and constitution. Much of his attention must be given to the cells of the embryo, as they multiply, migrate, take on different appearances, and carry on different functions. But he must always remember that the embryo has a life of its own to lead. All the different cells and cell groups in the embryonic body work in harmony if the development of the embryo is normal. He must not lose sight of the embryo-as-awhole.
The student preparing for medicine has a professional interest in embryology. Teachers of human anatomy have long since agreed that a knowledge of embryological relationships is the best possible preparation for the study of human anatomy. A good working acquaintance with the outlines of human embryology is prerequisite to the study of obstetrics. And the practitioner of medicine must be prepared to answer all sorts of questions about human development.
There are two different ways of approaching the subject of vertebrate embryology, when more than one type of development is to be studied. By the first method the different types of development are taken up one after another, e.g., amphioxus, frog, chick, man. The second method consists of discussing the different topics of embryology in turn and comparing the conditions found in each of the types. In this book, the second, or comparative, method is employed. But before taking up the first topic in comparative embryology, it is helpful to examine, very briefly, the life history of each of the types to be used in the later discussion. This will serve to introduce the main stages of embryology, and to point out the different conditions under which development takes place.
The history of embryology has passed through three phases. First came the period of fact-finding or description. The first name associated with this period is that of Aristotle. Before the invention of the microscope, Harvey, and after its invention, Malpighi, made careful studies of the development of the hen’s egg.
The second period is that of comparative embryology commencing with von Baer. Comparative embryology has been influenced in the past by Haeckel’s theory of recapitulation, which was supposed to support the Darwinian theory. With this period we associate also the subject of cellular embryology growing out of Schleiden and Schwann’s cell theory. This subject is now closely linked with genetics, for the gene, or unit of genetics, is located in the nucleus of the cell.
The present period may be called that of experimental embryology, foreshadowed by His and put on a firm basis by Roux.
The study of embryology is of value in understanding the relationships of the parts of the adult body, and the homologies of adult organs in different groups of animals. But its immediate aim is to discover the nature of developmental processes. Its methods are observational and experimental. It is concerned both with the behavior of the cells of the embryo and with the activities of the embryo as a whole.
Historical. Locy, W. A. 1915. Biology and Its Makers, 3rd Ed. .
Needham, J. 1931. Chemical Embryology, Vol. 1. —— 1934. History of Embryology.
Nordenskiold, E. 1928. The History of Biology. Russell, E. S. 1916. Form and Function.
See also references, Chap. II. ~.McEwen, R.S. 1931. Vertebrate Embryology, 2nd Ed.
Richards, A. 1931. Outline of Comparative Embryology.
Wieman, H. L. 1930. An Introduction to Vertebrate Embryology.
Comparative vertebrate embryology. Brachet, A. 1921. Traité d’embryologie des vertébrés.
Hertwig, O. (ed.) 1906. Handbuch der vergleichenden und experimentallen Entwickelungslehre der Wirbelticre. 6 volumes.
Jenkinson, J. W. 1913. Vertebrate Embryology.
Kellicott, W. E. 1913. Chordate Development.
Kerr, J. G. 1919. ‘Textbook of Embrvology, Vol. 2., Vertebrates exclusive of Mammals.
Comparative invertebrate embryology.
Dawydoff, C. 1928. Traité d’embryologie comparée des invertébrés.
Korschelt, E., and Heider, K. 1902-1910. Lehrbuch der vergleichenden Entwicklungsgeschichte der wirbellosen Tiere.
MacBride, E. W. 1914. Textbook of Embryology, Vol. 1., Invertebrates.
Cellular embryology (and cytology).
Cowdry, K. V. (ed.) 1924. General Cytology.
Sharp, L. W. 1934. Introduction to Cytology, 3rd Ed.
Wilson, KE. B. 1925. The Cell in Development and Heredity, 3rd Ed.
Experimental embryology. See references, Chap. VII.
Atlases. Duval, M. 1884. Atlas d’embryologiec.
Goette, A. 1874. Atlas zur Entwickelungsgeschichte der Unke.
Keibel, F. (ed.) 1897-1923. Normentafeln zur Intwicklungsgeschichte der Wirbelticre. Kohlmann, J. 1907. Handatlas der Entwickelungsgeschichte des Menschen.
See also bibliographies in references cited above.
Biological Abstracts, commencing with literature of 1926.
Concilium Bibliographicum, card index, commencing with literature of 1896.
Minot, C. S. 1893. A Bibliography of Vertebrate Embryology. Mem. Boston Soc. Nat. Hist., 4:487-614.
Monographs, embryological series. Carnegie Institution of Washington. Contributions to Embryology.
Chapter II Vertebrate Life Histories
It is obvious that in an introductory text it is impossible to: describe the development of an animal representing each vertebrate group. There are, however, four vertebrates whose embryology has been studied more intensively than any others. These are the amphioxus, the frog, the chick, and man. But before continuing with a brief account of the life history of these vertebrates it is advisable for the student to recall the list of terms which will be used in the descriptions following.
|(Synonyms in parentheses)|
|Anterior (cephalic, cranial, rostral) — head end.|
|Posterior (caudal) — tail end.|
|Dorsal — back side.|
|Ventral — belly side.|
|Lateral — either right (dextral) side, or left (sinistral) side.|
|Mesial (median, medial) — middle.|
|Proximal — nearer the point of reference.|
|Distal — further from the point of reference.|
|Transverse (horizontal) — a plane intersecting the antero-posterior axis at right angles, dividing anterior portion from posterior.|
|Sagittal — the mesial plane of the body or any plane parallel to it, dividing right portion from left.|
|Frontal (coronal) — any plane at right angles to both transverse and mesial planes dividing dorsal portion from ventral.|
|Primordium (anlage, Germ.; ébauche, Fr.) — the first recognizable stage in the development of any new part of the embryo.|
|Invagination — the growth of a surface in (toward the point of reference).|
|Evagination — the growth of a surface out (away from the point of reference).|
The amphioxus (Branchiostoma lanceolatum) is not really a vertebrate, .for it lacks a skull and vertebral column. But because it has a notochord and other chordate structures it is a relative of the vertebrates, a protochordate. Bygsome it is be
ture, the blastopore, which later narrows as the gastrula increases in length (Fig. 11).
The germ layers. — The outer layer of the gastrula is known as the ectoderm; the inner one is called the endoderm. It really includes not only the endoderm proper, which is to become the lining of the digestive tube, but also the middle germ layer or chorda-mesoderm, which now occupies the roof of the gastrocoel.
The roof of the gastrocoel soon, 11 or 12 hours after fertilization, develops three longitudinal grooves. The middle one of these folds is to become the notochord; the others give rise each to a series of pouches or enterocoels (Fig. 1J), from which the mesoderm is formed.
The ectoderm immediately over the roof of the gastrocoel is called the neural plate. About 15 hours after fertilization, ectoderm from the ventral side grows up over the blastopore to cover the neural plate (Fig. 1J).
Hatching. — The embryo escapes from its egg envelopes at this time, if not indeed a little earlier. It is now cylindrical in form, flattened on the dorsal surface, its length about twice its diameter. It appears to be about twice the volume of the original egg, owing to the large digestive cavity arising from the gastrocoel. The blastopore is covered by ectoderm from the ventral side, but this opens to the exterior by means of the anterior neuropore (Fig. 1K).
The larva. — After hatching, the embryo still subsists on the remainder of its yolk until the mouth opens, about the fourth day after fertilization. It is then about 1 mm. in length, very slender, and probably of no greater volume than the original egg (Fig. 1L). So soon as the mouth opens and the embryo is able to ingest food from external sources it is called a larva. By now all the organ systems except those connected with reproduction are functioning. For about three months the larva leads a free-swimming existence, making its way to deeper waters (Fig. 1M).
Metamorphosis. — At the end of three months, roughly speaking, the larva has increased in length to an average of 3.5 mm. It now gives up its free-swimming life to burrow in the sands and slowly assume its adult characteristics (Fig. 1N). The ability to produce mature germ cells is first manifested when the animal is about 200 mm. long.
B. The Frog
The frog (Rana pipiens) is one of the anuran amphibia. It is selected as a type of ichthyopsid (fish and amphibia) or anamniote (developing without an amnion). It has been a favorite object of embryological observations and experiments for centuries, and its development is better known than that of any other vertebrate except the chick.
Spawning. — The breeding season of the frog is in the early sprgng, soon after the ice is off the ponds. The males, emerging first from hibernation, make their way to the breeding grounds, where they congregate and sing in chorus while awaiting the coming of the females. On arrival, each female is seized by a male who grasps her for long periods (amplexus). In the early morning both individuals discharge their germ cells, so that fertilization is external. The egg, about 1.7 mm. in diameter (Fig. 2A), is surrounded with a layer of albumen which swells rapidly, causing the eggs, in masses of 3500 to 4500 (Wright), to adhere to vegetation or to rest on the bottom in shallow water. The yolk, present in the form of platelets, is concentrated in the lower hemisphere of the egg.
Fertilization. — Fertilization is external, but the close contact of the individuals during amplexus ensures that the sperm enters the egg before the swelling of the egg jelly prevents it. The first polar body is formed before fertilization, the second afterwards.
Cleavage. — The rate of cleavage depends upon the temperature, but the first division (Fig. 2B) may occur from one to two hours after fertilization, earlier at high temperatures, later at low ones. Cleavage divides the egg completely, but the third cleavage is unequal so that the four 3-blastomeres of the animal hemisphere are markedly smaller than the four of the vegetal hemisphere (Fig. 2C). After the third cleavage, the pattern becomes more irregular.
Blastula. — The presence of the large yolk-laden blastomeres in the vegetal hemisphere results in an eccentrically placed blastocoel. Furthermore, cleavage planes tangential to the surface of the blastula produce a layer of blastomeres several cells in thickness.
Gastrula. — The presence of great amounts of yolk prevents any invagination, and gastrulation takes place by overgrowth instead. Commencing from a shallow groove just below the equator (Fig. 2D), the smaller cells grow down over the larger ones. The down-growing cells form a two-layered fold because the cells at the margin are turned in as the fold grows down. As this overgrowth and tucking-in continues, the fold extends at its two extremities to become crescent-shaped (Fig. 2E). Finally the two ends of the crescent meet to form a circle which rapidly diminishes in circumference until finally only a small plug of the larger yolk-laden cells protrudes (Fig. 2F). The circle is known as the blastopore, and the groove with which it commenced is known as the dorsal lip of the blastopore. A gastrocoel is formed between the large yolk-laden cells and the smaller cells turned in at the lips of the blastopore.
Fig. 2. — Development of the frog. A, fertilized egg, from side, X8. B, first cleavage, from posterior side, X15. C, third cleavage, from left side, 15. D, early gastrula, (dorsal lip stage). I, middle gastrula, (lateral lips). F, late gastrula, (yolk plug stage). G, neural folds. (D-G, from posterior side, semidiagrammatic, approx. X15.) H, neural tube closed, 2.4 mm. I, embryo of 3mm. J,embryoof6mm. K,embryoof9mm. IL, embryo of 11mm. (H-L, from left side, measured alive, drawn after preservation X10.) M, full grown tadpole. N, after metamorphosis. (M and N, from left side, X1, after Wright, 1914.)
The germ layers. — The cells which were left on the exterior of the gastrula make up the ectoderm, while the inturned cells form an inner layer which includes both the endoderm and the chorda-mesoderm. The roof of the gastrocoel, therefore, is made up of two layers. The lower layer is the endoderm; the upper layer, lying beneath the ectoderm, is the chorda-mesoderm. It separates into three longitudinal strips, of which the middle one becomes the notochord. The others give rise to the mesoderm, which grows down between ectoderm and endoderm. No enterocoels are formed, but the mesoderm breaks up into a series of block-like somites on either side of the notochord.
The neurula.— The neural plate lies over the roof of the gastrocoel. It forms around its margin neural folds (Fig. 2G) which will later grow together to produce the neural tube. At this time the frog embryo is called a neurula. While the neural tube is being formed the embryo increases in length to about 2mm. This length is attained, ordinarily, on the second day after fertilization, although at room temperature development proceeds more rapidly.
Hatching. — During the first 13 to 20 days the embryo increases rapidly in length and in the development of its organ systems and finally, when it attains the length of 6 mm. (Fig. 2J), it wriggles out of its jelly. At room temperature this may take place within 5 days of fertilization and when the embryo is only 3 mm. in length (Fig. 21). The embryo as yet has no mouth or external gills but is provided with a sucker by which it attaches and activities quite unlike those of the adult. This larval period is terminated by a sudden metamorphosis associated with a change to terrestrial conditions.
The egg of the chick is enormous because of the great amount of yolk and the albumen enclosed within the shell. Fertilization is internal and prior to the formation of the albumen and shell. Development is very rapid and accompanied by the development of an amnion or water bath, and an allantois which serves as an extra-embryonic bladder, lung, and albumen sac. These features are correlated with the terrestrial environment of the developing egg. Eggs of this type are termed “ cleidoic ” (Needham).
The human egg is very small owing to the small amount of contained yolk. Fertilization is internal, and the developing egg soon implants itself in the wall of the uterus where its ten months of development proceed. The early stages of development are passed through very rapidly, and the blastula and gastrula are quite unlike any seen in other classes of vertebrates. An amnion is formed around the developing embryo, and this structure is concerned in the formation of an umbilical cord connecting the embryo to the placenta, a disc-shaped organ of maternal and fetal origin. The placenta serves as an organ of interchange between mother and young up to the time of birth. Development continues long after this event.
Conklin, E. G. 1932. The Embryology of Amphioxus. Jour. Morphol. 54:69151.
— 1933. The Development of Isolated and Partially Separated Blastomeres of Amphioxus. Jour. Exptl. Zool. 64:303-375.
Kerr, J.G. 1919. Textbook of Embryology, II, Chap. 1.
MacBride, E. W. 1915. Textbook of Embryology, I, Chap. 17.
Willey, A. 1894. Amphioxus and the Ancestry of the Vertebrates.
Huxley, J.S., and de Beer, G. R. 1934. The Elements of Experimental Embryology, Chap. 2.
Marshall, A.M. 1893. Vertebrate Embryology.
Morgan, T. H. 1897. The Development of the Frog’s Egg.
Noble, J. K. 1931. The Biology of the Amphibia.
Wright, A.H. 1914. North American Anura.
Ziegler, H. E. 1902. Lehrbuch der vergleichenden Entwickelungsgeschichte der niederen Wirbeltiere.
Duval, M. 1889. Atlas d’embryologie.
Lillic, F. R. 1919. The Development of the Chick, 2nd Ed.
Patten, B. M. 1929. The Early Embryology of the Chick, 3rd Ed.
Man. Arey, L. B. 1934. Developmental Anatomy, 3rd Ed. Keibel, F., and Mall, F. P. 1910. Human Embryology. Kollmann, J. 1907. Handatlas der Entwickclungsgeschichte des Menschen.
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