Book - Comparative Embryology of the Vertebrates 5

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Nelsen OE. Comparative embryology of the vertebrates (1953) Mcgraw-Hill Book Company, New York.

1953 Comparative Vertebrate Embryology: 1. The Period of Preparation | 2. The Period of Fertilization | 3. The Development of Primitive Embryonic Form | 4. Histogenesis and Morphogenesis of the Organ Systems | 5. The Care of the Developing Embryo | Figures

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Part V - The Care of the Developing Embryo

The care of the developing embryo necessitates the formation of various types of embryonic membranes, and in many species, the retention of the developing embryo within either maternal or paternal body structures (Chap. 22).

A. Introduction

1. Care in Relation to the Number of Young Produced

In this chapter, we shall consider the methods by which developing embryos of different vertebrate species are cared for and nourished during development. The amount of care given to the developing egg varies greatly. However, one primary rule appears to govern the reproductive habits of the species, namely, the species must survive. This survival is accomplished by two principal methods:

  1. by the production of enormous numbers of developing young, given no protective care, with the result that few survive to the adult or reproductive stage, and
  2. by the formation of fewer developing individuals with greater amounts of protective care.

Generally speaking, the fewer the individual embryos produced, the greater the care.

Examples of the method of species survival without parental care are evident in the codfish, Gadus, which spawns about 8 to 10 millions of eggs during a particular breeding period or in the ling, Molva, which discharges from 14 to 60 millions of eggs at one time. In these instances, the species survive by the sheer number of developing young produced. On the other hand, the shark, bird, and mammal substitute an extreme care of the developing egg. With the result that the number of eggs produced at each breeding period is reduced enormously, compared with that of the cod or ling.

2. General Environmental Conditions Necessary for Development

Regardless of whether or not there is specialized care of the developing young, the following conditions, concerned with the nutrition and care of the young, are necessary in the development of all vertebrate embryos:

(a) All embryos develop within a fluid or "embryonic lake" made possible by the presence of certain, enveloping membranes;

(b) a favorable temperature is required, particularly in warm-blooded species;

(c) food material including water must be supplied;

(d) oxygen is necessary to the developing embryo, and

(e) the removal of carbon dioxide and other wastes is imperative.

3. Types of Enveloping or Protective Membranes

Many types of protective membranes are produced in the vertebrate group for the purpose of caring for the developing young. These membranous and other types of protective envelopes may be classified as follows:

a. Egg membranes.

b. Extra-embryonic membranes.

c. The uterine portion of the oviduct.

d. Uncommon or specialized structures.

The egg membranes are those membranes produced around the egg during its formation in the ovary or during the journey down the oviduct. They are classified generally into three categories:

  1. Primary egg membranes are the membranes which are produced by the surface layer of the egg as it develops in the ovary, e.g., the vitelline membrane;
  2. secondary egg membranes are the membranes contributed to the egg by the activities of the surrounding follicle cells of the ovary, e.g., the zona pellucida of mammals, possibly also the chorion of some fish eggs; and
  3. tertiary egg membranes are the membranes contributed to the egg as it passes down the oviduct, such as the albuminous layers of frog and chicken eggs.

The extra-embryonic membranes are those membranes constructed of embryonic tissues which extend out of and beyond the strict confines of the embryonic body. As such they represent specialized embryonic tissues adapted to fulfill certain definite functions necessary to the embryo. The extra-embryonic membranes are:

  1. The yolk sac, found in most species. The yolk sac is developed as an extension of the primitive gut.
  2. The amnion, representing a sac-like structure which surrounds the embryo. It is found only in the that is^ the reptiles, birds, and mammals.
  3. The allantois. This structure arises as an outpushing from the midventral area of the hindgut, and is found only in reptiles, birds, and mammals.
  4. Pharyngeal diverticula. The pharyngeal diverticula are found in certain species of fish and in amphibians. The external gill filaments of the shark embryo mentioned in Chapter 14 are an example of this type of extra-embryonic membrane. Also in certain species of Amphibia elaborate pharyngeal placentae are evolved which function in a respiratory capacity.

The uterine portion of the oviduct functions, of course, as a capsule to protect the developing egg in all ovoviviparous and viviparous species.

Uncommon, specialized structures for the protection of the developing embryo are formed in many species of fishes and Amphibia. These structures are described more explicitly on p. 915.

4. Types of Food Sources

There are two main types of food sources for vertebrate embryos, namely, endogenous and exogenous sources. The endogenous form of food supply is found in all amphibian species, in the lung-fishes, Amphioxus, etc., where nourishment necessary for development is incorporated directly within the developing embryonic cells from the beginning cleavages of the egg. On the other hand, in the exogenous type of food supply the nourishment necessary for development lies outside of the developing embryonic tissues. This type of food storage is found in elasmobranch and teleost fishes, reptiles, birds, and mammals. Two categories are to be observed, as follows:

(1) In the majority of fishes, and in all reptiles, birds, and prototherian mammals, the food is stored within the egg. The developing embryo which lies upon this food source utilizes a specialized type of extraembryonic tissue to digest and assimilate the food materials.

(2) In some fishes and in the metatherian and eutherian mammals, most, or practically all, of the food elements come directly from the maternal (and, in some instances in fishes, from paternal) tissues as the embryo develops. Here also, a specialization of extra-embryonic tissue is necessary to tap the supply of food.

5. Mechanisms for Oxygen Supply and Carbon Dioxide Removal

Two types of oxygen supply and carbon dioxide removal mechanisms are encountered. In the majority of fishes and in the larger number of Amphibia, the surface of the developing egg functions as a respiratory membrane. In some fishes, and in rare instances in the Amphibia, special diverticula of the pharyngeal area are developed to care for this function. On the other hand, in all reptiles, birds, and mammals, the allantoic diverticulum from the hindgut assumes respiratory responsibilities.

6. Oviparity, Ovoviviparity, and Viviparity

The word oviparous is derived from two Latin words, namely, ovum, egg, and parere, to bring forth. Oviparous animals thus produce eggs from which the young are hatched after the egg is laid or spawned. Among the vertebrates, oviparous species include most of the fishes, amphibia, reptiles, birds, and prototherian mammals. Ovoviviparity is a condition in which the egg is retained within the confines of the reproductive duct or other specialized areas where it hatches, and the young are brought forth or born alive. The greater portion of the embryo's nourishment is derived from the nutritive materials within the egg, while oxygen uptake, together with fluid substances and the elimination of carbon dioxide, is effected through the oviducal wall and its blood vessels. Ovoviviparous species include certain sharks, teleosts, certain urodele and anuran amphibia, and various reptiles. In viviparity (Latin, vivus, alive) the new individual is brought forth alive. In viviparity the developing embryo obtains some or all of its nourishment through the wall of the uterus or other specialized structure. Viviparous forms are found among the sharks, teleosts, and reptiles, together with all species of metatherian and eutherian mammals.

B. Formation and Importance of the Protective Embryonic Membranes

1. The Egg Membranes

a. Primary and Secondary Egg Membranes

The formation of the primary and secondary egg membranes were described in Chapter 3. The importance of these membranes formed around the egg, while it develops in the ovary, is considerable. The so-called fertilization membrane, produced, for example, in Amphioxus, the zona radiata and chorion of fishes, the vitelline membrane of amphibians, reptiles, and birds, or the zona pellucida of mammals are important structures. All these membranes form the first or primary protective coating around the embryo. Between the embryo and this primary embryonic membrane is a fluid-filled area, the perivitelline space. The perivitelline fluid is favorable to the embryo. Thus, the surrounding fertilization, vitelline, or zona membranes act as an insulating wall between the outside environment and this early perivitelline pond of the embryo. All vertebrate embryos, from the fishes to the mammals, are protected normally by the primary embryonic membrane during the period of cleavage, and, in many fishes and amphibians this membrane functions until the time when the embryo hatches and assumes a free-living existence.

b. Tertiary Egg Membranes

1) Mammals. The lengths of the Fallopian tubes of different mammalian species vary considerably. In the mouse, rabbit, human, and sow, the Fallopian tubes vary in length, not only from species to species but also from individual to individual within the species. Yet, the time of passage of the egg through this region of the reproductive duct approximately, for all four species, is from 3 to Wi days. On the other hand, the length of the uterine tube of the opossum may be from 5 to 10 times that of the mouse, yet the time consumed in egg transport in the former species is about 19 to 24 hours. Moreover, in the sow and mouse, evidence has been accumulated which tends to show that egg transport through the middle portion of the uterine tube is slower than that of the portion near the infundibulum or of the part near the uterus (Anderson, '27; Lewis and Wright, '35). In the Monotremata, Flynn and Hill ('39, p. 540) conclude that "passage through the tube must be fairly rapid." In all these instances, the rate of egg travel through the uterine tube appears to be dependent upon necessary developmental changes within the cleaving egg and functional changes within the uterus and the uterine tube. In other words, the rate of egg propulsion through the Fallopian tube varies with the species. The time consumed in transit is not related to the length of the tube, but is correlated with changes in the uterus, preparatory to receiving the egg at a proper developmental stage.

The deposition of protective enveloping coats around the egg during egg passage through the Fallopian tube is encountered in certain mammals. In the monotremes, a rather dense, albuminous coat is deposited around the egg in the upper two thirds of the Fallopian tube, and a clearer, more fluid secretion is deposited around the egg by the glandular cells in the posterior third of the tube (Flynn and Hill, '39). A leathery shell is formed around the egg and these albuminous coats in the posterior segment or uterus. In the opossum, a dense albuminous coating forms around the egg during its passage down the upper part of the Fallopian tube, while a thin much tougher membrane is added around the outside of the albuminous material in the tube's lower part. In the rabbit, a thick albuminous coating is deposited around the egg as it passes downward within the Fallopian (uterine) tube. Therefore, formation of protective egg envelopes may be regarded as a specific function of the Fallopian tube during egg passage in some mammals.

The reactions of the developing egg within the uterine portion (uterus) of the reproductive duct in the higher mammals are dramatic events in which the embryo develops special contacts with the uterine wall. In some cases, the embryo becomes entirely enclosed within the tissues of the uterus. These phenomena are considered on pages 914, 920.

2) Birds. The passage of the hen's egg down the oviduct has been studied at various times from the time of Aristotle to the present. In its transportation, the "naked yellow" or ovum becomes surrounded by an intricate association of fibers, albuminous substance, membranes, and calcareous shell which form a system of protective envelopes. As the egg of the hen passes posteriad in the oviduct, it rotates slowly under the influence of muscular contractions and the spiral arrangement of longitudinal folds of the mucous membrane lining the oviduct. This rotation aids in the deposition of the membranes and albuminous layers.

a) Formation of the Chalaziferous Layer. The first coating of albumen is deposited around the egg as it passes through the posterior portion of the infundibulum (fig. 157). It is in the form of a sheet of mucin-like fibers in the meshes of which is a dense albuminous substance. This capsule of albumen is applied closely to the vitelline membrane of the ovum, and it represents the membrana chalazifera, or chalaziferous layer (fig. 369A). (See Romanoff and Romanoff, '49, pp. 137, 219.)

b) Deposition of the Middle Dense Layer of Albumen. The egg soon leaves the infundibular area of the oviduct and enters the albumen.secreting region where a dense layer of albuminous material, the albuminous sac, is deposited together with mucin fibers, the albumen being enmeshed in the latter (fig. 369A).

c) Formation of the Inner Liquid Layer of Albuminous Material and the Chalazae. As the egg continues its journey posteriad, it is rotated upon the spirally arranged folds of the oviduct. This rotation twists the mucinlike fibers in the inner portion of the dense albuminous layer, and it is believed that this twisting motion squeezes the more fluid albumen out of the mucin meshwork where it becomes deposited immediately around the chalaziferous layer to form the inner liquid layer of albumen. At the same time, some of the mucin fibers become twisted in opposite directions at the upper and lower ends of the egg as the latter is rotated along the spiral folds of the oviduct. These twisted fibers form a bundle at the anterior and posterior ends of the egg and become attached firmly to the chalaziferous layer, reaching outward into the dense albumen. These two bundles of twisted mucin fibers form the chalazae, one chalaza being tied to the chalaziferous layer at the lower end of the egg (i.e., the end occupying the more posterior position in the oviduct) and the other lying attached to the chalaziferous layer at the upper end of the egg (fig. 369A),

d) Deposition of the Outer Liquid Albuminous Layer. As a result of the resection experiments of Asmundson and Burmester ('36), one is led to conclude that a considerable amount of the outer, watery, albuminous layer which comes to surround the middle dense layer of albumen is deposited in the anterior part (i.e., the ovarian end) of the albumen-secreting portion of the oviduct (figs. 157; 369A). Some of the watery material is added in the isthmus and in the uterus (Romanoff and Romanoff, '49, p. 220).

e) Formation of the Egg Membranes and Egg Shell. As the egg reaches the isthmus, the shell membranes are formed around the albuminous material. In the upper part of the isthmus, the thin inner membrane is formed, while the thick, coarse, outer membrane is deposited in the posterior parts of the isthmus. These two membranes of the egg expand considerably coincident with the passage of a watery albuminous material through their meshwork into the outer, liquid, albuminous layer while the egg passes through the lower part of the isthmus, and also during the first part of the egg's occupancy of the uterus. As a result, the volume of the albumen is increased rapidly and considerably in this general area.

During the latter part of the period of the egg's residence within the uterus, calcareous concretions or mammillae are deposited upon the external face of the coarse, outer, egg membrane (fig. 369B). Each conical concretion or mammilla is embedded in the outer egg membrane. The broader distal end of the mammila faces outward while the pointed proximal end is attached to the egg membrane (fig. 369B). Small pores appear between the various mammillae. External to the mammillary layer, a spongy layer of collagenous fibers is formed. This spongy layer gradually becomes impregnated with calcium salts which lie within the spaces between the spongy fibers and between the mammillary and spongy layers. The calcified spongy layer and associated mammillary concretions form the egg shell. The calcium probably is secreted in the form of bicarbonate which later changes to calcium carbonate. Some calcium chloride and phosphate, together with a calcium-protein substance also are formed. The colored pigments of the egg shell in colored eggs are ooporphyrin pigments, derived probably from the hemoglobin of worn-out red blood cells. A thin cuticle or protective film is applied to the surface of the calcified spongy layer just before the egg is laid (fig. 369B).

Fig. 369. Structure of the hen's egg. (A and B redrawn from Romanoff and Romanoff, 1949. Wiley & Sons, Inc., N. Y.) (A) General structure of newly laid hen's egg (after Romanoff). (B) Detailed structure of egg shell (after von Nathusius).

The rate of transport of the egg through the oviduct of the hen is interesting. Once the egg has entered the infundibulum, it takes but 20 minutes to complete its passage through this area. The infundibular region constitutes five per cent of the length of the oviduct. In the albumen-secreting region where it accumulates most of its albumen, the egg spends about four hours. This segment forms about 60 per cent of the total oviducal length. The passage through the isthmus requires approximately one hour. This region forms 15 per cent of the total length of the oviduct. The last or uterine segment is about the same length as that of the isthmus, but the egg spends about 80 per cent of its passage time or about 19 hours in this portion. The rate of passage, therefore, in the more anterior portion of the oviduct is rapid, somewhat slower in the isthmus, and very slow in the uterus (Romanoff and Romanoff, '49).

3) Reptiles. Egg passage through the oviduct and deposition of the tertiary egg membranes in reptiles probably resembles very closely that of the bird with the exception that in a considerable number of reptiles the young develop in the uterus and are discharged in a free-living condition (see p. 83). Also, the eggs of modern reptiles have a thick leathery shell instead of the brittle calcareous shell of bird's eggs.

4) Amphibians. In the frog, egg transport down the glandular portion of the oviduct appears to be effected mainly by the propelling force of the beating cilia, possessed by certain of the cells lining the oviduct. This ciliary action possibly is aided by some peristaltic action of the oviducal musculature. The cilia are found on the cells which line the longitudinal ridges which run "more or less the length of the oviduct" (Noble, '31, p. 282). As the egg moves downward (posteriad), it is covered by mucus or similar gelatinous material. In the common frog, Rana pipiens, three gelatinous layers are deposited around the egg during its oviducal passage.

Passage of the egg through the oviduct in other Amphibia probably resembles that of the frog.

In many Amphibia (e.g., frogs), the caudal portion of the oviduct is expanded to form a special compartment, called the uterus, where the eggs remain for a period before discharge to the outside. In some urodeles, the eggs are retained in the oviduct, and the young are born in the larval or fully metamorphosed state (see p. 189).

5) Fishes. Internal egg transport in fishes presents a variety of conditions. In many teleosts, the ovary, when egg formation is completed, becomes a large egg sac, directly connected with the short oviduct. At the time of spawning, a general contraction of the ovarian tissues occurs, and the eggs are expelled into the oviduct and from there to the outside. The contraction of the ovarian tissues, together with a peristaltic behavior of the oviducal musculature, affords the mechanism necessary to transport the eggs to the external environment. Egg membranes are not deposited around the egg as it passes through the oviduct in teleost fishes.

In the elasmobranch fishes, however, glandular and uterine portions of the oviduct are present, and the large egg is transported through the upper glandular region of the oviduct in a manner similar, presumably, to that in the hen. Surrounding membranes of albuminous materials, and an outer chitinoid "shell" are produced in the glandular area. These membranes vary with the species and some are complicated as indicated in figure 380A. In many elasmobranch fishes and also in the so-called viviparous teleost fishes, the egg is retained in the uterine portion of the oviduct. Here the young develop and, when discharged to the outside, are able to fend for themselves. In these forms, the uterus is adapted to the function of providing the embryo with an environment suitable for its development.

In the cyclostomatous fishes, an oviduct is not present, and egg transport resolves itself into a discharge of eggs into the coelomic cavity from which the eggs pass through openings into the cavity of the urogenital sinus. Ovarian membranes only are present around the cyclostome egg. These membranes may be complex as in the hagfish, Polistotrema (Bdellostoma), (fig. 162).

2. The Extra-embryonic Membranes

The extra-embryonic membranes as indicated previously are those membranes produced from the embryonic tissues. These membranes are the yolk sac, amnion, chorion (serosa) and allantois. In a strict sense, the periderm (see Chapter 12) probably should be included as an extra-embryonic membrane for it is elaborated at the surface area of the epidermis and functions to protect and presumably to regulate the possible entrance of substances from the surrounding environment.

a. Yolk Sac

A yolk sac is present in all reptiles, in birds and mammals, and in those fishes which have megalecithal eggs, that is, having a large amount of yolk substance stored within the egg. Two types of yolk sacs are found among the vertebrates, viz.:

  1. a yolk sac whose walls are composed of entoderm, mesoderm and ectoderm in the form of closely associated layers. This type of yolk sac is found in the embryos of the hagfishes, Polistotrema (Bdellostoma) stouti and Myxine glutinosa, in most elasmobranch fishes, and in teleosts (fig. 370A). Some of the amphibia with a large quantity of yolk in the egg such as Necturus maculosus, also approach this condition.
  2. a second type of yolk sac is found in reptiles, birds and mammals. In these instances the wall of the yolk sac is composed mainly of entoderm and mesoderm, i.e., the splanchnopleure, as the extra-embryonic coelom tends to separate the splanchnopleure from the somatopleure in these forms (fig. 370B).

Fig. 370. Diagrams of extra-embryonic membranes. (A) Transverse section of yolk sac and developing body in teleost and elasmobranch fishes showing relation of body layers to the yolk mass. (B) Transverse section of yolk sac and forming serosa (chorion) in reptiles, birds, and prototherian mammals. (C-E) Diagrams showing extra-embryonic membranes in the pig. (C) Conditions in 16-17 somite pig, age approximately 16 days. The ends of the diagram have been omitted in part, because of length of embryonic vesicle. (D) Conditions in embryo of 5 mm. or about 17-18 days of age. (E) The extraembryonic membranes in embryo of about 4-5 weeks of age.

b. Amnion

The amnion is a specialized sac which comes to encompass the embryo in reptiles, birds and mammals (fig. 370B-E). Because of its restriction to these vertebrates, the reptiles, birds and mammals are grouped together as the Amniota, the fishes and amphibia being designated as the Anamniota.

Eggs which are spawned into the surrounding water, as in fishes and amphibia, are cradled or cushioned by the surrounding fluid, and the embryo is free to develop without undue pressure from any side. In the Amniota, however, this watery environment must be established artificially and hence the amnion is formed to accommodate and enclose the fluid of this individualized embryonic “swimming" pool.

The amnion arises generally in two ways, as follows, although intermediate forms are found among certain mammals (see Mossman, '37).

  1. By a dorsal folding of the somatopleure, in which anterior, lateral, and posterior amnionic folds project dorsad and fuse (see figures 238B; 242C and G; 370B-E). This method is found in reptiles, birds, prototherian mammals, the opossum, pig, rabbit, etc.
  2. The second main method is by cavitation, i.e., a cavity develops within the cells forming the inner cell mass of the early embryo (fig. 3 72 A and B). Found in human, mouse, rat, etc. In the monkey, the formation of the amnion is somewhat intermediate between the folding and cavitation methods.

c. Chorion (Serosa)

The formation of the amnion by the folding method also results in the development of the chorion or serosa, in that it separates the somatopleure from the splanchnopleure of the yolk sac (fig. 370B and C). However, in those forms which utilize the hollowing out or cavitation method of amnion formation as in the human, the chorion forms directly by the attachment of extraembryonic mesoderm to the inner aspect of the trophectoderm (fig. 372 A and B),

d. Allantois

In most fishes and amphibia, external respiration of the developing embryo is possible by a direct interchange of oxygen and carbon dioxide across the perivitelline fluid and primary embryonic membranes into the surrounding watery medium. However, in eggs which are deposited on dry land, such as those of birds, reptiles, and prototherian mammals, a specialized embryonic structure, the allantois, is formed to permit external respiration to occur. The allantoic diverticulum arises as a mid-ventral outpushing of the caudal end of the hindgut (fig. 370C). The allantois is a hollow, sac-like structure composed of entoderm on the inside and splanchnopleuric mesoderm externally. As it extends outward, blood vessels develop in the mesoderm. It eventually comes in contact with the chorion with which it fuses to form the chorioallantoic membrane (fig. 370D and E). The chorio-allantoic membrane in reptiles and birds contacts the surface membranes of the shell (fig. 299E).

In the higher mammals an allantoic diverticulum also is formed. In this group of vertebrates, the allantois not only serves the function of external respiration but also is the main instrument in nutrition. In the human embryo, the entodermal evagination from the hindgut forming the allantoic diverticulum is small, and blood vessels develop precociously within the mesoderm of the body stalk (see figure 372B). These blood vessels course distad to the developing chorion and its villi where external respiration is accomplished.

However, in the pig and many other mammals, the allantoic diverticulum is a large, spacious structure (see figure 370D and E).

Respiratory devices thus arise as diverticula from two general areas of the vertebrate body, viz.:

  1. the pharyngeal area (see Chapter 14) and
  2. the hindgut area.

e. Yolk Stalk, Allantoic Stalk, Belly Stalk, and Umbilical Cord

As the embryo increases in size (see figures 370C-E; 372B-D), the yolksac connection with the mid-gut area of the embryo becomes relatively smaller. The constricted area of entoderm and mesoderm which connects the yolk sac with the midgut is called the vitelline duct or yolk stalk. Similarly, the constricted area of the allantois which connects the allantoic diverticulum with the hindgut area is called the allantoic stalk. As the embryo continues to enlarge, the yolk stalk and allantoic stalk are brought closer together and their mesoderms fuse. The closely associated yolk and allantoic stalks form the belly stalk in the area where they attach to the belly (ventral) wall of the embryo (fig. 370E). The narrowing ring-like area between the ventral body wall of the embryo and the yolk and allantoic stalk tissues is a passageway for blood vessels to and from the yolk and allantoic stalk tissues. It is called the umbilical ring, umbilicus or omphalos. As the embryo continues to enlarge, the amnion in the mid-ventral area of the embryo is reflected downward from the umbilical ring or umbilicus over the yolk-stalk and allantoic-stalk tissues and thus eventually encloses the yolk and allantoic stalks (figs. 370E; 372C and D). This entire structural complex composed of amnionic tissue, together with enteric and allantoic diverticula and splanchnopleuric mesoderm, is called the umbilical cord (fig. 372D).

Fig. 371. Brood compartments for care of young. (A) Pregnant female of the lizard, Chalcides tridactylus (Seps chalcides), showing uterine compartments containing developing eggs. (Redrawn from Needham, 1942, Biochemistry and Morphogenesis, Cambridge University Press, London.) (B) Dorsal brood pouch in the anuran, Gastrotheca pygmaea. (C) Dorsal brood pouch in Gastrotheca marsupiata. Observe small dorsal opening of pouch. (D) Dissection of vocal (brood) pouch in male of Rhinoderma darwinii. (B-D, redrawn from Noble, 1931, The Biology of the Amphibia, McGrawHill, N. Y.)

Fig. 372. Extra-embryonic membranes in human embryo. (A) Diagrammatic representation of extra-embryonic membranes in embryo of about 12 days of age, shortly after enclosure within uterine endometrium. (Redrawn and modified from Hertig and Rock, 1941, Carnegie Contr. to Embryology, vol. 29.) (B) Extra-embryonic membranes in embryo of about 16 days. (C) Extra-embryonic membranes in embryo of about 28 days. (D) Extra-embryonic membranes in embryo of about 12 weeks.

In the human embryo, that portion of the mesoderm which connects the forming allantoic diverticulum with the chorionic mesoderm is called the body stalk (fig. 372B).

3. The Reproductive Duct as a Protective Embryonic Membrane

The developing egg is retained within the oviduct in all metatherian and eutherian mammals and in various species in the other major vertebrate groups with the exception of the birds. Even in the birds (fig. 157), a partial development of the egg normally occurs within the confines of the oviduct. Oviparity thus encroaches upon ovoviviparity in birds, and ovoviviparity infringes upon viviparity in certain sharks (Squalus acanthias), reptiles (various snakes and lizards), and prototherian mammals. However, oviparity has this feature which distinguishes it from ovoviviparity and viviparity, namely, the new individual always hatches or leaves the confinement of the egg membranes outside the protective environment of the reproductive duct (or other protective structures). On the other hand, ovoviviparous and viviparous forms are released from the egg membranes and thus "hatch out" within the oviduct or other covering structure. The more viviparous the particular species, the sooner the new individual hatches from its egg membranes. In most cases of ovoviviparity and viviparity, the reproductive duct (specifically, the uterine segment) acts as a protective embryonic membrane which surrounds the developing embryo or embryos. Thus, a definite area of the reproductive duct is temporarily allotted to the embryo. If several embryos are present, a particular segment of the uterus is assigned to the care and protection of each embryo (see TeWinkle, '41, '43, and '50) (fig. 371 A). For further description of the uterine portion of the oviduct as a protective mechanism see p. 919.

Fig. 373 - Continued

placenta is of the epitheliochorial variety, i.e., the epithelium of the chorionic tissue comes into contact with the epithelium of the uterus without erosion of either. (C) Placental relationships in the dog. This figure represents a small area at the edge of the zonary placenta shown in fig. 378D, as indicated. (Redrawn and modified from Mossman, 1937, Carnegie Institute Publications, vol. 26, Contributions to Embryology, No. 158.) This placenta is a dual type, in that the edge of the placenta resembles somewhat the hemochorial type, i.e., maternal blood in direct contact with the chorionic epithelium of the villus, while the center of the placental zone is of the endotheliochorial type of placentation, i.e., the epithelium of the chorionic villus is in contact with the endothelial lining of the maternal blood capillaries. (D) Placental relationship in human. (Redrawn and modified from Spanner, Zeitschrift fur Anatomic, vol. 105, Julius Springer, Berlin, Germany. ) The placenta is made up of many cotyledons, each cotyledon being composed of a main stem villus, which contains the larger fetal blood vessels, and from the large stem villus smaller branching villi extend out into the surrounding maternal blood. Imperfectly developed septa separate the various cotyledons. This type of placentation is of the hemochorial variety, i.e. the chorionic epithelium is in contact with the maternal blood. (E) Diagram illustrating the hemoendothelial type of placentation in the late gestation period of the rabbit. Here the chorionic epithelium is eroded and the capillaries of the chorionic villi lie within the maternal blood.

Fig. 374. Placentation in the mouse. (A) Blastocyst within fold of the uterine mucosa. (B) Longitudinal section of uterine site of placentation showing mesometrial and antimesometrial aspects. (C) Later stage of conditions shown in B. Observe that placentation of the embryo is in the antimesometrial side of the uterus. The placenta is probably of the hemochorial relationship at first becoming hemoendothelial later as in the rabbit. (See Mossman, '37.) (A-C, redrawn from Snell, 1941, The Early Embryology of the Mouse, Blakiston, Philadelphia.)

4. Uncommon or Specialized Structures as Protective Mechanisms

Many structures other than the oviduct are used by various vertebrate species to accommodate and protect the developing egg. In the teleost, Heterandria formosa, the eggs are retained within the ovary (Scrimshaw, '44). Although a typical, teleostean, oil droplet is present in the egg which measures 0.39 mm. in diameter, it is not utilized until late in development, and most of the nourishment is afforded by a vascular sac which partly encloses the embryo. In the teleost, Gamhusia affinis, the egg also develops in the ovarian follicle, but, in this case, most of the nourishment is derived from yolk which is contained within the egg. In the sea horses. Hippocampus, and in the pipefishes, Syngnathus, the eggs are transferred to a pouch, formed by folds of skin located in the ventral body wall of the male. Here the embryos develop (fig. 106). Many teleost fish are "mouth breeders," that is, they carry the eggs for various periods in the buccal cavity.

The amphibia show an array of protective devices for young. The marsupial frogs are most interesting. In Gastrotheca (Nototrema) pygmaea, the "maternal purse," formed by cutaneous folds, spreads over the dorsal area of the trunk, and an elongated opening in the middorsal line permits passage into the sac (fig. 371 B). In Gastrotheca rnarsupiata, the opening of the dorsal brood pouch is located in the sacral area (fig. 371C). The brood pouch of Gastrotheca ovifera is similar to that of G. rnarsupiata (Noble, '31, pp. 60, 510). In some forms, such as G. weinlandii, the skin of the back is covered by calcareous dermal plates and in such species Noble says the young are "enclosed within a veritable coat of mail" Lastly, mention may be made of the little Chilean frog, Rhinoderrna darwinii. In this instance the male frog carries the few eggs and young, through metamorphosis, in his vocal pouches (fig. 370D). (See Noble, '31, pp. 71 and 507.)

C. Special Adaptations of the Extra-embryonic Membranes for Uterine Existence

1. Implantation

a. Definition

Implantation is the process whereby the embryo becomes attached to a nutritional substrate. The term is applied generally to those embryos which become associated intimately with the uterine wall. This is the common usage of the term. However, it is well to point out that the embryos of teleost and elasmobranch fishes as well as those of reptiles, birds and prototherian mammals become attached to the yolk substrate of the egg. Moreover, this attachment entails the elaboration of an extra-blastular or extra-embryonic tissue (i.e., the periblast tissue) of a syncytial nature similar to that present where embryos attach intimately to the uterine wall in the higher mammals. Most vertebrate embryos thus rely upon a process of implantation for nutritional support.

b. Types of Implantation

When implantation occurs in such a way that the embryo remains within the lumen of the uterus while the extra-embryonic membranes make a superficial attachment to the uterine mucosa, it is called central or superficial implantation. This type of implantation is found in all cases of implantation in lower vertebrates. In the marsupial mammals it is present in Perarneles and Dasyurus, and among the eutherian mammals in the pig, cow, rabbit, sheep, dog, cat, etc. In the mouse and rat the early blastocyst comes to lie between the uterine epithelial folds in an antimesometrial position. These folds soon enclose the blastocyst almost completely (fig. 374A-C). This type of implantation is called ecceutric implantation and it borders upon the complete interstitial variety. In still other mammals, such as the guinea pig, man, chimpanzee, the embryo burrows into the uterine mucosa below the epithelium and in this way becomes surrounded completely by the endometrial tissue of the uterus. This condition is known as complete interstitial implantation (fig. 375A-C).

2. The Placenta and Placentation

a. Definition

The process of implantation implies an interaction and attachment between the extra-embryonic membranes and the uterine wall. This area of attachment between maternal and embryonic tissues is called the placenta, and the word placentation denotes the general process effecting this attachment. The word placenta is derived from the Greek and it means a flat cake. It received this name because the human placenta is a flat, rounded mass shaped more or less like a pancake. The placenta may be defined as the association between embryonic and uterine tissues for the purpose of physiological exchange of materials. It is evident that this is a restricted definition applicable only to uterine types of implantation.

b. Types of Embryonic Tissues Involved in Placentation ^

In all vertebrate embryos it is the extraembryonic somatopleure (extraembryonic ectoderm plus extraembryonic somatopleuric mesoderm) which contacts the uterine mucosa during placentation. In those species which possess a yolk-sac placenta, for example, in the dogfish, Mustelus laevis, the midgut extension of the splanchnopleure which surrounds the yolk unites with the extraembryonic somatopleure to form the embryonic contact (fig. 373A). On the other hand, in the chorio-allantoic placenta of the lizard, Chalcides tridactylus, and in the chorio-allantoic placenta of all eutherian mammals, it is the allantoic evagination of the hindgut which contacts the extraembryonic somatopleure (called the chorion in higher vertebrata) and unites with it to form the embryonic part of the placenta (fig. 373B). However, in all of these instances the epithelium of the extraembryonic somatopleure makes the direct contact with the maternal tissue. Certain exceptions to this general rule apparently exist, for in the rabbit during the later stages of gestation, the epithelium of the chorion may disappear in certain areas, permitting exposure of the fetal blood vessels to the maternal blood (fig. 373E).

c. Types of Placental Relationships in the Eutherian Mammals

1) Epitheliochorial Type. If the epithelium of the uterus is not destroyed, and the embryonic tissue merely forms an intimate contact with the uterine epithelium, the placenta is called an epitheliochorial placenta, e.g., pig (fig. 373B). Under these conditions the placental area is large and diffuse (see figure 378A). (The placenta of the dogfish, Mustelus laevis (fig. 373A) is essentially of this type.)

2) Endotheliochorial Variety. If the epithelium of the uterus is eroded, and the embryonic tissue (i.e., chorionic epithelium) comes in contact with the endothelium of the maternal blood vessels, the attachment is called an endotheliochorial placenta (e.g., dog, cat, and other Carnivora, figure 373C). As the placental attachment becomes more intimate the placental area becomes restricted. Compare figure 3 78 A and B with C, D and E.

3) Endotheliochorial Plus Syndesmochorial Placenta. In the Ungulata (cows, sheep, goats) the placenta is an extensive affair similar to that of the pig. However, the attachment between embryonic and maternal tissues occurs in certain areas known as cotyledons (fig. 378B). In parts of these cotyledons the association of maternal and embryonic tissue is of the endotheliochorial variety, but in other areas of the cotyledons only the epithelium of the uterus disappears, leaving the chorionic epithelium of the extra-embryonic tissue in contact with the connective tissue of the uterine wall. A condition where the chorionic epithelium makes contact with the connective tissues of the uterine wall is called a syndesmochorial relationship.

4) Hemochorial Placenta. In the rodents, primates (including man), shrews, moles, and bats the endothelium of the maternal blood vessels is destroyed by the erosive activity of the embryonic tissues, and the chorionic epithelium of the embryonic portion of the placenta comes directly in contact with the maternal blood (fig. 373D). This type of association is known as a hemochorial placenta.

5) Hemoendothelial Placenta. In the rabbit, the initial contact of the fetal tissues with the uterine epithelium forms an epitheliochorial relationship. Still later it becomes, after erosion of maternal tissue, a hemochorial condition, and finally, during the latter phases of pregnancy, even the chorionic epithelium disappears, leaving the endothelium of the embryonic blood vessels in contact with the maternal blood (fig. 373E). This type of association is the most intimate placental contact known and it is called a hemoendothelial relationship.

3. Implantation of the Human Embryo

a. Preparation for Implantation

In all cases of uterine care of the developing egg, the uterus must be prepared for the event. This preparation is induced by the activities of the ovarian hormones (see Chapter 2 and figures 53 and 59). Implantation of the embryo occurs in the early luteal phase of the reproductive cycle when the endometrial mucosa is in an optimum condition for the reception of the developing egg.

b. Implantation

As indicated above, p. 904, the process of egg transport down the Fallopian tube occurs at a rate which permits the developing egg (embryo) and the uterine tissue to prepare themselves for the implantation event. About three to three and one-half days elapse during the passage of the egg through the

Fig. 375. Implantation in human and monkey. Trophoblastic ectoderm shown in complete black in the following diagrams. (A) Human about 7Vi days. Blastocyst almost completely inside of the endometrium. (B) Human about 11 days. Blastocyst within endometrium. Trophoblast enlarging. (C) Human about 12 days. (D) Condition of human embryonic vesicle at about 13-15 days. Observe enormous thickening of trophoblast tissue, the presence of trophoblastic lacunae containing endometrial residues, and the formation of the secondary chorionic villi. (A-D, redrawn from Corner, 1944, Ourselves Unborn, Yale University Press, New Haven, Conn.) (E) Placental relationships at about 12 weeks. (Redrawn and modified from De Lee and Greenhill, 1943, The Principles and Practice of Obstetrics, Saunders, Philadelphia.) (F) Early stage in implantation of the monkey, Macaca mulatto, blastocyst about 9 days of age. (O) Monkey blastocyst about 10 days. (H) Monkey blastocyst about 10 days. (I) Monkey blastocyst 11 days. (J) Blastocyst of 13-day monkey embryo showing primary and secondary implantation sites. (F-J redrawn from Wislocki and Streeter, 1938, Carnegie Instit. Contributions to Embryology, Vol. 27, Contributions to Embryology, No. 160.) (K) Placentae of Lasiopyga callitrichus. Observe that umbilical cord and its blood vessels attach to the primary placental disc, while blood vessels are given off from the primary disc to the secondary disc. (Redrawn from Wislocki, 1929. Carnegie Contributions to Embryology, Vol. 20. Contributions to Embryology, No. 111.)

Fallopian tube. As a result, when the developing human egg reaches the uterus it is in the early blastula (blastocyst) condition (Chap. 6). The zona pellucida or secondary egg membrane is still intact. The blastocyst remains free within the uterus presumably for about four days. During this period, it becomes separated from the zona pellucida (i.e., it hatches) and the blastocoelic cavity of the blastocyst (blastula) subsequently enlarges greatly. The implantation site for man (and also monkeys) under normal conditions is the mid-dorsal or mid-ventral area of the uterus (Mossman, '37). The human embryo presumably begins to implant about 7 to 8 days after fertilization (Hertig and Rock, '45 ) . In doing so that pole of the blastocyst which contains the developing germ disc becomes attached to the uterine epithelium. As this occurs the uterine epithelium becomes eroded in the area of immediate contact with the blastocyst, and the epithelial cells of the trophoblast layer of the blastocyst increase in number. As a result, the trophoblast tissue enlarges greatly in the contact area (fig. 375A, F and G). During this process a change occurs in the trophoblast cells for the external cells fuse together to form a syncytium, the so-called syntrophoblast, while the inner trophoblast cells remain cellular and form the cytotrophoblast (fig. 376A). The syntrophoblast presumably acts as the invading tissue. {Note: the trophoblast tissue in figures 3 72 A and in 375 is shown in black.) As the syntrophoblast increases in quantity it comes to enclose irregular spaces, the trophoblastic lacunae (fig. 375B-D). Simultaneously localized areas of the syntrophoblast extend outward to form the primary villi (fig. 376A). These primary villi at first lack a mesenchymal core, but soon they become invaded by the mesoderm of the somatopleure to form the secondary villi (figs. 372B; 376B). At about 11 days, the developing human embryo is completely inside of the uterine wall (fig. 375B). At 12 to 15 days (fig. 375C and D), the syntrophoblast has expanded considerably and secondary villi begin to appear around the inner portions of the trophoblast (figs. 375D; 376B). Meanwhile (fig. 375D), some of the endometrial tissue close to the invading chorionic vesicle, including blood vessels, is broken down to form liquefied areas, the embryotroph. It is possible that this liquefied material is assimilated by the syntrophoblast and passed inward to the developing germ disc. If this histological material thus is utilized it forms a source of nutrition, and it may be called histotrophic nutrition.

c. Formation of the Placenta

As the developing chorionic vesicle grows within the endometrium of the uterus, the uterine mucosa expands over the growing vesicle (fig. 377 A and B). That part of the endometrial tissue overlying the chorionic vesicle is called the decidua capsularis (fig. 377A), and the portion of the endometrial lining of the uterus not concerned with the enclosure of the chorionic vesicle is called the decidua vera or decidua parietalis. The part of the endometrium lying between the muscle tissue of the uterine wall and the enlarging villi (fig. 372C and D) of the chorionic vesicle is the decidua basalis (fig. 377A).

At first chorionic villi are developed over the entire chorionic vesicle (fig. 372B), but as development goes on the villi in relation to the decidua parietalis are resorbed gradually to form a smooth area of the chorion, the chorion laeve (fig. 372D). Finally, only those villi in relation to the decidua basalis remain (fig. 372D). The villi within the decidua basalis enlarge and become the main villi for physiological interchange of materials between the embryo and the maternal tissues. This portion of the chorionic vesicle with the enlarged chorionic villi is known as the chorion frondosum (fig. 372D). The villi of the chorion frondosum and the tissue of the decidua basalis together form the placenta. The embryonic mesodermal tissues of the placenta are continuous with mesoderm of the umbilical cord, and the embryonic blood vessels of the placenta are directly continuous with the blood vessels of the umbilical cord (fig. 372D). The placental area thus is a dual structure composed of the decidua basalis or maternal placenta (placenta materna) and the chorion frondosum or fetal placenta (placenta fetalis) (fig. 375E). The placental area gradually expands during the early months of pregnancy until at about the fifth month when it reaches its greatest relative size or about one-half the internal aspect of the uterus.

Fig. 376. Structure of villi in human chorionic vesicle. (A) Primary villus. (B) Secondary villus. (C) Villus from chorion at about 4 weeks. Villus at about 14 weeks. Observe gradual disappearance of cytotrophoblast.

The early chorionic villi of about the fourth week of pregnancy are composed of four constituent parts, viz.:

  1. blood capillaries which course within
  2. the mesenchymal cells of the mesodermal core. Surrounding the internal core of mesenchyme is the trophectodermal layer composed of an inner
  3. cytotrophoblast, which is surrounded externally by the
  4. syntrophoblast (fig. 376C and D).

As development proceeds, the central core of mesenchyme with its blood capillaries increases in size, and the cytotrophoblast layer of the trophectoderm decreases in quantity, until, at about the fourth month, little remains of the cytotrophoblast layer with the exception of a few scattered cells below the syntrophoblast (fig. 376D).

The placental villi are grouped together into groups known as cotyledons. Between the cotyledons are the placental septa, which incompletely separate the various cotyledons from each other. The origin of the placental septa is uncertain, possibly being contributed to by both embryonic and maternal tissues. Surrounding the villi within each cotyledon is a pool of maternal blood which bathes the surfaces of the syntrophoblast of the villi. A hemochorial relationship is in this way established (fig. 373D).

4. Implantation in the Rhesus Monkey, Macaca mulatta

The various stages of implantation and placental formation of the rhesus monkey are shown in figure 375F-K. It is to be observed that the mbnkey develops a primary placenta (fig. 375H and I) which later is supplemented by another placenta, the secondary placenta, attached to the opposite uterine wall (fig. 375J and K). Also, the embryo of the rhesus monkey, unlike the human embrvdl does not bury itself within the uterine mucosa, and the chorionic vesicle remains Within the lumen of the uterus (see Wislocki and Streeter, '38).

Fig. 377. Human placentation. (A) Condition at about 4 weeks. (B) About six weeks. Villi disappearing on one side, while those of chorion frondosum are enlarging. (A and B redrawn from Corner, 1944, Ourselves Unborn, Yale University Press, New Haven, Conn.) (C) Placental relationships in dizygotic (i.e. two fertilized eggs) twins implanted close together. Observe two chorionic vesicles, and two placentae. (D) Placental relationships in monozygotic (one fertilized egg) twins. Observe one chorionic vesicle, two amnions, and one placenta. (C and D redrawn from Dodds, 1938, The Essentials of Human Embryology, John Wiley & Sons, New York.)

5. Implantation of the Pig Embryo

As in the human the passage of the cleaving egg of the pig through the Fallopian tube is slow, consuming about 3V^ days. When the egg reaches the uterus it still is surrounded by the zona pellucida and developmentally is in an advanced state of cleavage or early blastocyst formation (fig. 145H). It remains free in the uterine horn for about 6 to 7 days. During this period the blastocyst enlarges and elongates at a rapid pace, particularly during the sixth and seventh days of uterine existence (i.e., 9 and 10 days after copulation) (fig. 145I~L). The blastocyst eventually forms a much elongated attenuated structure about 1 meter long. During the earlier portion of the free uterine period the many blastocysts of the ordinary conceptual process in the sow become spaced within the horn of each uterus, an intriguing process which continues to remain baffling. From 10 to 13 days after copulation the blastocysts experience the gastrulation processes (see figure 145M-R; and figures 208 and 209); from days 13 to 15 body form is developed gradually (fig. 242 A-F) and the amnion and chorion are formed (fig. 242G).

From days 14 to 17 the allantoic diverticulum grows rapidly (figs. 242G; 370C--D). At this time the chorionic vesicle as a whole shortens and becomes much larger in transverse section. The yolk sac of the embryo of 16 to 17 days is greatly enlarged in relation to the size of the embryo, and the entoderm at its distal end lies closely apposed against the chorionic ectoderm (figs. 242F; 370C). As the allantoic cavity expands, the yolk sac, relatively speaking, contracts, and a relationship is established similar to that in figure 370D. As the allantois expands its mesoderm comes in contact with the mesoderm of the chorionic membrane and fuses with it (fig. 370E). This new layer forms the chorio-allantoic membrane. The chorio-allantoic membrane becomes folded into elongated folds which fit into similar folds of the uterine mucosa. A relationship thereby is formed as shown in figure 373B.

Fig. 378. External appearance of chorionic vesicles in various mammals. (A) Pig. This placental type is called diffuse. (A') Enlarged drawing of small cotyledon or areola. (B) Cow. Observe large cotyledons. This type of placenta is called cotyledonary. (C) Brown bear. Special zonary placenta. (D) Dog, etc. Zonary placenta. (E) Raccoon, incomplete zonary placenta. (A, B-E, redrawn and modified from Hamilton, Boyd and Mossman, 1947, Human Embryology, Williams and Wilkins, Baltimore.)

In certain areas of the chorion, specialized structures or areolae, containing small villi, appear to slightly invade the uterine glands (fig. 378A'). However, the epithelium is not destroyed, and at all times the maternal and fetal aspects of the greatly expanded placental area (see figure 378 A) may be separated without injury either to the chorionic or to the uterine epithelium.

6. Fate of the Embryonic Membranes

a. Yolk Sac

The yolk sac of teleost and elasmobranch fishes is withdrawn gradually toward the ventral body wall and intestine. The contribution of the yolk sac differs considerably in the two groups. In the teleost fishes, the somatopleuric portion of the yolk sac contributes much to the body wall while the splanchnopleuric tissues of the yolk sac form a considerable part of the latero-ventral region of the intestine. In the elasmobranch fishes, the somatopleuric layer of the yolk sac forms only a small area of the ventral body wall in the anterior trunk region, and the splanchnopleuric tissue of the yolk sac is withdrawn inward toward the duodenal area. This withdrawal of the splanchnopleuric tissue is a complex affair, for as the external yolk sac is withdrawn an internal yolk sac is developed as an evagination from the yolk stalk (vitelline duct) near the duodenum (fig. 296A). While the external yolk sac gets smaller the internal yolk sac increases in size, and after the external yolk sac has been entirely withdrawn a considerable part of the internal yolk sac remains. Ultimately the splanchnopleure of the internal yolk sac forms a small area of the duodenal wall.

In the chick the yolk sac is still large as hatching approaches. During the eighteenth and nineteenth days the yolk sac containing a considerable amount of yolk is withdrawn into the body cavity through the umbilicus. Here the yolk is absorbed rapidly and the yolk sac tissues are taken up into the wall of the intestine about 5 or 6 days after hatching.

The yolk sac of the higher mammals does not contain yolk substance. One of its main functions is the formation of the first blood cells (see Chapter 17). The yolk stalk and yolk sac increase somewhat in size during the early phases of development. Ultimately the yolk stalk becomes greatly elongated and separates from the yolk sac. The proximal portion of the yolk stalk is taken up into the wall of the intestine. In the human embryo, the area of yolk stalk inclusion into the intestinal wall is about 18 to 24 inches proximal to the ilio-caecal area.

b. Amnion and Allantois

The amnion and allantois of the Amniota function until birth. During parturition the amnion generally ruptures, but may remain intact around the offspring. For example, in a litter of six puppies, half of the amnions may be ruptured and half may be intact. The intact amnion must then be ruptured or the puppy will suffocate. In the human the after-birth consists of the following:

(a) the maternal membranes - decidua vera, decidua basalis, and decidua capsularis (vera), and

(b) the fetal membranes - chorion frondosum, chorion laeve, amnion, yolk sac, allantois, and umbilical cord.

D. Functions of the Placenta

The functions of the placenta are many, and the more intimate the contact with the maternal tissue the functions appear to increase. The various functions of the placenta may be listed as follows:

  1. Food materials pass from the maternal blood stream to the blood stream of the embryo.
  2. Waste materials pass from the embryo's circulatory system to the blood stream of the mother.
  3. Serves as the external respiratory mechanism for the embryo.
  4. It functions to elaborate two ovarian hormones, estrogen and progesterone (see Chapter 2) together with chorionic follicle-stimulating and luteinizing hormones. The production of estrogen and progesterone helps maintain pregnancy (see Chapter 2) and at the same time brings about the development of the mammary glands.
  5. The placenta and after-birth tissues form a source of nourishment to the female of many mammals, for it is generally eaten by the mother.

E. Tests for Pregnancy

The elaboration of chorionic follicle-stimulating and luteinizing hormones by the placenta in increasing amounts during the first part of pregnancy and their excretion by the kidneys makes possible certain tests for the detection of pregnancy (see Engle, '39).

1. Aschheim-Zondek Test

Aschheim and Zondek were the first investigators to detect gonad-stimulating principles in the urine of pregnant women. The excretion of these substances in pregnancy urine begins during the second week, about the fifteenth day, rises sharply to the thirtieth day and then gradually falls to the ninetieth day (Siegler and Fein, '39). This secretion probably is elaborated by the trophoblast of the developing chorion during the second week of pregnancy and later by the epithelium of the chorionic portion of the placenta. The presence of these gonad-stimulating substances in the urine provokes reproductive changes in the ovaries of common laboratory animals when injected with the urine. Aschheim and Zondek were the first to use this method for detecting pregnancy. The method consists of the injection of small amounts of pregnancy urine into mice and rats and, later, observing the appearance of hemorrhagic conditions of the follicles within the ovaries. A modification of the Aschheim-Zondek or A-Z test used by Kupperman, Greenblatt, and Noback, '43, consists of the injection of 1.5 cc. of a morning sample of urine into the lower portion of the abdomen of immature rats. The animal is killed with ether after two hours and pronounced hyperemic conditions of the ovary are observed as a positive test.

2. Friedman Modification of the Aschheim-Zondek Test

In this test 10 cc. of the suspected urine is injected into the marginal vein of the rabbit's ear. In about 1 2 to 24 hours a positive test is denoted by ovulation points (blood points) on the ovarian surface and by hemorrhagic conditions within the follicles. This test is as accurate as the original A-Z test and works in almost 98 to 99 per cent of the cases.

3. Toad Test

When the "clawed toad" of South Africa, Xenopus laevis, is injected with pregnancy urine, the animal ovulates within a few hours and the eggs are easily detected.

4. Frog Test

Wiltberger and Miller, '48, advocate the following test. Five cc. of a first morning (overnight) sample of urine is carefully injected subcutaneously into the dorsal or lateral lymph sacs of a male frog. Two or more frogs are used. Each frog is then placed in a clean, dry, glass jar with perforated lid. After 2 to 4 hours at ordinary room temperature, any urine that is voided by the frogs is examined microscopically. If urine is not present, the frog is seized by the hand while still in the jar. This treatment usually results in urination. Sperm in the urine denotes a positive test.

F. The Developing Circulatory System in Relation to Nutrition

All of the developing systems undergo gradual alterations which are integrated with, and contribute to, the ever-changing demands involved in the welfare of the embryo. However, the circulatory system is the one system which must assume the burden of transport of food materials, oxygen, and water to the developing systems. Synchronously it transports deleterious substances to the areas of elimination. While assuming this burden it also must evolve its own development to bring about the structure of the adult form of the circulatory system.

A striking example of the dual burden carried by the developing circulatory system is presented in the changes which go on a short time before and after birth (mammals) or hatching (reptiles and birds). The placental area in mammals and the chorio-allantoic structures in reptiles and birds act as respiratory

Fig. 379. Diagrams of probable fetal and postpartum circulations through the heart in the mammal. (A) Fetal circulation. Oxygenated blood passes through umbilical vein, to liver. Passing through the liver by means of the ductus venosus it gathers blood from the liver veins and empties into the inferior vena cava through the hepatic vein. Within the inferior vena cava it mixes with non-oxygenated blood from the posterior part of the body. Reaching the right atrium it passes across the atrium through the foramen ovale and into the left atrium and from thence into left ventricle. The blood from the superior vena cava crosses to one side of the blood current from the inferior vena cava in the right atrium on its way to right ventricle. Most of the blood from the right ventricle courses through the ductus arteriosus into the descending aorta. A small amount goes to the lungs via the pulmonary arteries. (B) Circulation after birth. Observe there is no passage of blood from the right atrium into the left atrium. The blood in the left atrium is returning oxygenated blood from the lungs. The ductus arteriosus has atrophied. (See text.) (A redrawn and modified from Windle, 1940, Physiology of the Fetus, Saunders, Philadelphia. B adapted from A.)

and excretory regions before birth and hatching. The circulatory system therefore must accommodate these areas in the fulfillment of the respiratory and excretory functions. However, at the same time the developing heart and immediate blood vessels in relation to the heart also must look forward, as it were, to the requirements of the period after birth (mammals) or after hatching (reptiles and birds). A diagram of the circulation of the blood through the heart previous to birth in the mammalian heart is shown in figure 379A, and figure 379B delineates the pathway of the blood after birth. Before birth the valve-like arrangement of the interatrial septa, I and II, permits the oxygenated blood from the placenta to flow from the right atrium into the left atrium. From the left atrium the blood passes into the left ventricle and from thence out through the aortic root to supply heart tissues, head region and systemic structures in general. On the other hand, the blood from the superior vena cava flows through the right atrium to the right ventricle, and from there it is propelled out into the proximal portion of the pulmonary artery, and through the ductus arteriosus (Botalli) (left sixth aortal arch) to the systemic aorta. The unaerated blood from the right ventricle in this way is mixed with aerated blood within the descending aorta. Some circulation to and from the capillary bed within the lungs also occurs at this period.

At birth and after, the change in the place of oxygenation of the blood from the placental area to the lungs with the stoppage of the blood flow through the umbilical vessels, necessitates the changes shown in figure 379B. The closure, normally, of the foramen ovale in interatrial septum II, together with the shrinkage of the ductus arteriosus to form the ligamentum arteriosum accommodates this change in direction of blood flow. The alterations which effect the stoppage of blood flow through the foramen ovale and ductus arteriosus are functional and they actually precede the morphological closure changes. The foramen ovale is functionally closed by the apposition of Septum I and Septum II. This apposition is effected by the equalization of the blood pressures in the right and left atria. However, the structural closure of the foramen ovale is produced by the growing together and gradual fusion of the two interatrial septa. The process is variable in different human individuals, and failure to attain complete structural closure of the foramen ovale occurs in about 20 to 25 per cent of the cases. Functionally, this failure to close may not be noticeable. On the other hand, in the heart of the kitten, failure to develop a complete morphological closure by 6 to 8 weeks after birth is rare.

The morphological closure of the ductus arteriosus also is gradual. This does not interfere with the relative normal functioning of the lungs for the opening up of the capillary bed within the lungs together with the concomitant voluminous flow of blood through the pulmonary arteries to the lungs, associated with the pressure exerted at the distal end of the ductus arteriosus by the blood within the descending aorta, aids the functional closure of the ductus arteriosus. In some individuals, the ductus arteriosus may remain open, to some degree, even in the adult.

G. Post-hatching and Post-partum Care of the Young

(fig. 380)

Although care of the young after hatching or after birth is beyond the province of this work, it should be observed that such care is characteristic of birds and mammals, and is present in certain instances in fishes and amphibia (fig. 3 SOB). In the marsupial mammals, the early post-partum care of the young in the marsupial pouch of the mother is closely related to the pre-hatching or pre-partum care of the young in other animal groups. In the opossum, for example (fig. 380D), the utterly helpless young are firmly attached to the nipples of the mother for about 50 days (McCrady, '38). This attachment in reality constitutes a kind of "oral placenta." From this viewpoint, the care of the developing embryo in marsupial mammals may be divided into two phases, namely, a uterine phase and an early post-partum phase. The first phase in the North American opossum consumes about 13 days, and the latter about 50 days. After the young become free from their nipple attachment they spend about 40 days in and out of the marsupium.


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1953 Comparative Vertebrate Embryology: 1. The Period of Preparation | 2. The Period of Fertilization | 3. The Development of Primitive Embryonic Form | 4. Histogenesis and Morphogenesis of the Organ Systems | 5. The Care of the Developing Embryo | Figures

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