Book - Comparative Embryology of the Vertebrates 4-14

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

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Part IV - Histogenesis and Morphogenesis of the Organ Systems

Part IV - Histogenesis and Morphogenesis of the Organ Systems: 12. Structure and Development of the Integumentary System | 13. Structure and Development of the Digestive System | 14. Development of the Respiratory-buoyancy System | 15. The Skeletal System | 16. The Muscular System | 17. The Circulatory System | 18. The Excretory and Reproductive System | 19. The Nervous System | 20. The Development of Coelomic Cavities | 21. The Developing Endocrine Glands and Their Possible Relation to Definitive Body Formation and the Differentiation of Sex

Respiratory and Buoyancy Systems

A. Introduction

1. External and Internal Respiration

Respiration consists of two phases: (1) external and (2) internal. External respiration enables the organism to acquire oxygen from its external environment and to discharge carbon dioxide into this environment. Internal respiration is the utilization of oxygen and the elimination of carbon dioxide by the cells and tissues of the organism. The formation of the structural mechanisms related to external respiration, in many vertebrates, is associated intimately with buoyancy functions. The development of external respiratory and buoyancy mechanisms is discussed in this chapter.

2. Basic Structural Relationships Involved in External Respiration

a. Cellular Relationships

In effecting external respiration, it is necessary for blood capillaries to come into a close relationship with a moist or watery medium containing sufficient amounts of oxygen and a lowered content of carbon dioxide. The mechanisms permitting this relationship vary in different vertebrates. In lower vertebrates, blood capillaries in the gills or in the skin are brought near the watery medium containing oxygen, while, in higher vertebrates, lungs are used for this purpose. In lower vertebrates, an epithelial layer of cells is always interposed between the blood stream and the oxygen-containing fluid. Small amounts of mesenchyme or connective tissue may interpose also (fig. 299B & C). However, in the air capillaries of the lungs of birds (fig. 307C) and in the air cells (alveoli) of mammalian lungs (figs. 299 A; 309G), the surrounding blood capillaries may be exposed intimately to the air-fluid mixture containing oxygen, and the barrier of epithelium between the blood capillaries and the air mixture may be greatly reduced if not entirely absent.

b. Sites or Areas Where External Respiration Is Accomplished

External respiration is achieved in various areas in the embryos and adults of different vertebrate species. In the early shark embryo, external gill filaments, attached to the pharyngeal area, serve as a mechanism for effecting external respiration (fig. 299D), whereas, in the chick and reptile embryo, allantoic contacts with surface membranes of the egg are important (fig. 299E) . In the frog tadpole, the flattened tail region is a factor, as well as the presence of gills and lungs associated with the pharyngeal area. The embryos of higher mammals utilize allantoic-placental relationships for this phase of respiration (see Chap. 22). Similarly, in adult vertebrate species, various areas of the body are used as respiratory mechanisms, such as a moist skin (fig. 299B), gills, lungs, vascular villosities, or papillae (fig. 299F). The skin is most important in the amphibian group as a respiratory mechanism (Noble, ’31, pp. 162, 174-175). However, considering the vertebrate group in its entirety, the branchial or pharyngeal area is the particular part of the developing body devoted to the formation of adult respiratory mechanisms.

c. Main Types of Organs Used for Respiration

Two main types of respiratory organs are developed in the vertebrate group:

  1. branchial organs or gills in water-living forms and
  2. pulmonary organs or lungs in land-frequenting species.

Both of these organs represent pharyngeal modifications.

B. Development of Branchial or Gill Respiratory Organs

As observed in the previous chapter, p. 618, the invaginating branchial grooves and the outpocketing branchial pouches come together in apposition in the early embryos of all vertebrate species, and, in water-living forms, varying numbers of these pouch-groove relationships perforate to form the gill slits. In cyclostomatous fishes (fig. 301 A, B), the number of perforations is six or more pairs; in elasmobranch and teleost fishes, there are five or six pairs (fig. 301C, D); and in amphibia, two or three pairs become perforated. In general, the first pair of branchial-pouch-groove areas is concerned with the formation of the spiracular openings or with the auditory mechanisms. However, in some species it may be vestigial. In water-inhabiting species, the succeeding pairs of pouch-groove areas and their accompanying visceral arches may develop gill structures. (See p. 669, visceral skeleton.)

Two types of gill mechanisms are developed in the vertebrate group:

  1. internal gills in fishes and
  2. external gills in amphibia and in lung fishes.

in all cases, gill development involves a modification of visceral-arch structure. This modification involves the external surface membranes and blood vessels of the arches. The first two pairs of visceral arches, the hyoid and mandibular, are utilized generally throughout the vertebrate series in jaw and tongue formation (sec Chap. 13). On the other hand, the third and succeeding pairs of visceral arches are potentially branchial or gill-bearing arches in water-living forms. In reptiles, birds, and mammals, the potency for gill formation by these arches ostensibly is lost.

Fig. 299. Structural relationships of respiratory surfaces. (A after Clements, ’38; B after Noble, ’31; H after Patten: Am. Scientist, vol. 39, ’51; F and G after Noble, ’25; C and D original.) (A) Respiratory surface in air sac of pig, 18 hrs. after birth. Capillaries are exposed to air surface. (B) Section through epidermis of respiratory, integumentary folds along the sides of the body of Cryptobranchiis aileganiensis. (C) Transverse section of external gill filament of Rami pipiens. (D) External gill filaments of Squalus acanthias. (E) The allantoic-egg-surface relationship of the developing chick embryo. (F) Respiratory villosities or “hair” of Astylosternus robustus, the hairy frog. (G) vSection through skin of vascular villosity shown in (F).

Fig. 300. Respiratory surface relationships in fishes. (AC original; D and E after Romer: The Vertebrate Body, 1949, Philadelphia, Saunders.) (A-C) External gill filaments and developing gill lamellae on gill arch of shark embryo, Squalus acanthias. (D) Section of gill arch of a shark. (E) Section of gill arch of a teleost fish.

1. Development of Gills in Fishes

a. Development of Gills in Squalus acanthias

As the developing gill arch of Squalus acanthias enlarges, the lateral portion extends outward as a flattened membrane, the gill septum (fig. 300A). On the posterior surface of the early gill arch, the covering epithelium produces elongated structures, the external gill filaments. Each gill filament contains a capillary loop which connects with the afferent and efferent branchial arteries (see Chap. 17). These filaments are numerous and give the branchial area a bushy appearance when viewed externally (fig. 300B). The epithelial covering on the anterior face of the gill arch, in the meantime, produces elongated, lamella-like folds, the gill lamellae or gill plates (fig. 300C). During later embryonic life, the external gill filaments are retracted and resorbcd as gill lamellae are developed at the basal area of the filaments. The gill arch thus comes to have a scries of gill lamellae or plates developed on anterior and posterior surfaces, i.e., the surfaces facing the gill-slit passageway. The gill plates on each surface of the gill arch form a demibranch, and the two demibranchs constitute a holobranch or complete gill.

Meanwhile, internal changes occur within the branchial arch. The original aortal (vascular) arch becomes divided into efferent and afferent aortal arteries, with capillaries interposed between the two (fig. 341 A-D). Afferent capillaries bring blood from the afferent portion of the aortal arch to the gill lamellae, while efferent capillaries return the blood to the efferent segment of the aortal arch. Associated with these changes, a skeletal support for the gill arch and gill septum is formed (fig. 315C and D). It is to be observed that the branchial or gill rays extend outward between the lamellae and thus form a series of supports for the gill septum and lamellae. Musculature is developed also in relation to each gill arch (fig. 327B).

b. Gills of Teleost Fishes

Gill development in teleost fishes is similar to that of Squalus acanthias, but the gill septum is reduced, more in some species than in others (fig. 300D, E). An operculum or external covering of the gills, supported by a bony skeleton, also is developed. The operculum forms an armor-like, protective door, hinged anteriorly, which may be opened and closed by opercular muscles (fig. 301D).

c. External Gills

Aside from the formation of external gill filaments as mentioned above (fig. 300B), true external gills, resembling those of Amphibia, occur in most of the dipnoan (lung) fishes and Polypterus in the larval stages (fig. 302A).

2. Development of Gills in Amphibia a. General Features

The gills of Amphibia occur only in the larval condition and in some adults which retain a complete aquatic existence, such as the mud puppy, Necturus maculosus, and the axolotl, Ambystoma rnexicanum. In other adult amphibia which have not renounced a continuous watery existence, such as Amphiuma and Cryptobranchus, the larval gills also are lost. Cryptobranchus relies largely upon the skin as a respiratory mechanism (fig. 299B). External gills are formed in the larval stage of all amphibia, and, in some, they present a bizarre appearance (Noble, ’31, Chaps. Ill and VII). In the frog tadpole, external gills are formed first, to be superseded later by an internal variety.

The amphibian external gill is a pharyngeal respiratory device which differs considerably from that found in most fishes. In many species, the gill is a columnar musculo-connective tissue structure with side branches, projecting outward from a restricted area of the branchial arch (fig. 302B). Gill filaments or cutaneous vascular villosities extend outward from the tree-like branches of the central column. The exact pattern differs with the species. In some amphibian larvae, the gill is a voluminous sac-like affair (sec Noble, ’31, p. 61).

Fig. 301. Gill arrangement in various fishes. (After Dean: Fishes, Living and Fossil, 1895, New York and London, Macmillan and Co.) (A) Polistotrema (Bdellostoma). (B) Hagfish, Myxine. (C) Shark. (D) Teleost.

Fig, 302. External gills. (A after Kerr: Chap. 9, Entwicklungsgeschichte tier Wirbeltiere, by Keibel, Jena, G. Fischer; B from Noble, ’31; C-E original.) (A) Larval form of Lepidosiren paradoxa. (B) Larval form of Pseudohranchus striatus. (C, D) Early developmental stages of Necturus maculosus. (E) Gill filaments on gill of adult Necturus.

As observed in the previous chapter, there are five pairs of branchial-pouchgroove relationships in frogs and salamanders, although six may occur in the Gymnophiona (Noble, ’31, p. 159). In the Gymnophiona, also, the first pair of branchial pouches perforates to the exterior for a while during embryonic life and each perforation forms a spiracle similar to that of the sharks and certain other fish. Later it degenerates. In other Amphibia, the first pair of branchial pouches never perforates to the exterior. It is concerned with the formation of the Eustachian tubes, as in most frogs and toads, or it degenerates and eventually disappears. The second, third, fourth, and fifth pairs of branchial pouches perforate variously in different Amphibia. In the frog, Rana pipiens, the second, third, and fourth branchial-pouch-groove relationships generally perforate, and sometimes the fifth does also. In Necturus maculosus, the third and fourth pairs normally perforate.

b. Development of Gills in Necturus maculosus

The gills of Necturus arise at about the 10- to 14-mm. stage as fleshy columnar outgrowths from a limited region of the third, fourth, and fifth visceral arches (i.e., the first, second, and third branchial bars or gill arches). (See fig. 302C.) These outgrowths are at first conical in shape (fig. 227) but later become compressed laterally. Epidermal outgrowths or gill filaments arise from the sides of these outgrowing gill columns (fig. 302C, D). (See Eycleshymer, ’06.) As the larva grows and matures, the development of gill filaments from the sides of the gill columns becomes profuse (fig. 302E). During the elaboration of the gill column and gill filaments, the original aortal (vascular) arch becomes separated into two main components, the afferent artery from the ventral aorta to the gill column and an efferent artery from the gill column to the dorsal aorta (Chap. 17).

c. Development of Gills in the iMrva of the Frog, Rana pipiens

1) Development of External Gills. As stated on p. 639, two types of gills are developed in the frog larva, external and internal. The external gills are developed as follows: At about the 5-mm. stage, the gill-plate area on either side of the embryo begins to be divided into ridges by vertical furrows (fig. 303A). Eventually, three ridges appear. These ridges represent the third, fourth, and fifth visceral arches (i.e., the first, second, and third branchial arches). From the upper external edges of these arches, a conical protuberance begins to grow outward, beginning first on the first branchial arch. Ultimately, three pairs of these fleshy columns are formed (fig. 3()3B). From these gill columns, finger-like outgrowths, the gill filaments, arise. An abortive type of gill may form also in relation to the fourth branchial arch. The gill column and the filaments possess the ability to expand and contract.

2) Formation of the Operculum. At approximately the 9- to 10-mm. stage, an oro-pharyngeal opening is formed by rupture of the pharyngeal membrane. At this time, also, the opercular membranes arise. Each operculum arises as a fold of tissue along the caudal edge of the hyoid or second visceral arch. This opercular fold on either side grows backward over the gill area. Eventually, the two opercula fuse ventrally and laterally with the body wall to form a gill chamber for the gills (fig. 303C). On the right side the fusion of the operculum with the body wall is complete. However, on the left side the fusion of the operculum in the mid-lateral area of the body wall is incomplete and a small opening remains as the opercular opening (fig. 257B') 3) Internal Gills. During the above period of opercular development, the external gills become transformed into internal gills, and branchial clefts form between the gill arches. In doing so, the external gill columns gradually shrink, and small, delicate, gill filaments sprout from the outer edges of the gill arches (fig. 303D). External respiration is achieved now not by a movement of the gill in the external medium, as previously, but by the passage of water into the mouth, through the gill slit, over the gill filament, and, from thence, through the opercular opening to the exterior. Both types of gill filaments, external and internal, fundamentally are similar.

4) Resorption and Obliteration of Gills. The resorption of gills is a phenomenon associated with metamorphosis in dipnoan fishes and in Amphibia, although certain species of Amphibia, as indicated on p. 639, retain certain larval characteristics in the adult condition. Most species metamorphose into an adult form which necessitates many changes in body structure (Noble, ’31, p. 102). This transformation has been related to the thyroid hormone (Chap. 21 ). In frogs, toads, and salamanders, the thyroid hormone produces degeneration and resorption of gills, the branchial clefts fuse, and the larval branchial skeleton is changed into the adult form (fig. 317).

An interesting feature of gill resorption in the anuran tadpole is that the degenerating gills produce a cytolytic substance which brings about the formation of the hole in the operculum through which the foreleg protrudes during metamorphosis (Helff, ’24; Noble, ’31, p. 103).

C. Development of Lungs and Buoyancy Structures

1. General Relationship Between Lungs and Air Bladders

The functions of buoyancy and external respiration are related closely. Lungs and air bladders (sacs) constitute a series of pharyngeal diverticula associated with these functions (fig. 304A-F). (For an historical approach to the work on developing lungs, see Flint, ’06; for studies on air bladders, consult Goodrich, ’30.) Air bladders (sacs) arc a characteristic feature of most teleost and ganoid fishes. In elasmobranch and cyclostomatous fishes, the air bladder is absent. Two main types of air bladders are found:

  1. a physoclistous type (fig. 304G), in which a direct connection with the pharyngeal area is lost (e.g., the toadfish, Opsanus tan), and
  2. a more primitive physostomous variety (fig. 304A-E), retaining a pharyngeal or pneumatic duct (e.g., the common pike or pickerel, Esox Indus).

Fig. 303. Gill development in the tadpole of Rana pipiens. (All drawings are original.) (A) Five- to six-mm. tadpole. (B) Frontal section of 7-mm. tadpole. (C) External, ventral view of 10-mm. tadpole, showing opercular fold covering gill area. (D) Gill bar, internal and external giil filaments of 10- to 11 -mm. stage.

Fig. 304. Swim-bladder and lung relationships. (A-F slightly modified from Dean: Fishes, Living and Fossil, 1895, New York and London, Macmillan and Co.; G after Goodrich, ’30.) (A E) Sagittal and transverse sections of swim-bladder relationships. (F) Lung relationship of Dipnoi and Tetrapoda. (G) Diagram of physoclistous swim bladder of teleost fish.

One function of the air bladder presumably is to alter the density of the fish in such a way as to keep its density as a whole equal to the surrounding water at various levels (Goodrich, ’30, p. 586). Buoyancy, therefore, is one of the main functions of the air bladder.

The air bladders of fishes, in some cases at least, have both respiratory or lung and buoyancy functions (Goodrich, ’30, pp. 578-593). In the bony ganoid fishes, Amia calva and Lepisosteus osseus (fig. 304B), the air bladder apparently has a primary function of external respiration and, therefore, may be regarded as a lung which secondarily is associated with the function of buoyancy. The latter condition is found also in the Dipnoi (lungfishes) .

The lung of the mud puppy, Necturus maculosus, is capable of considerable extension, particularly in the antero-posterior direction, is devoid of air cells within, and, hence, probably serves the buoyancy function as much or more than that of respiration. The lungs of sea turtles are capable of great distension and aid the animal in maintaining a position near the surface of the water. In the bird group, air sacs are united directly to the lungs, as sac-like extensions of the latter.

Thus, the formation of structures which assume the responsibility for the functions of buoyancy and respiration is a characteristic feature of pharyngeal development in most vertebrate species.

2. Development of Lungs

a. Development of Lungs in the Frog and Other Amphibia

In the 5- to 6-mm. embryo of Rana pipiens, the lungs arise as a solid evagination of the midventral area of the pharynx at the level of the fifth branchial pouches and over the developing heart. At the 7-mm. stage from this evagination, two lung rudiments begin to extend caudally below the developing esophagus (fig. 305). In the 10-mm. embryo, the lungs extend backward from a common tracheal area above the heart and liver area (fig. 258D). At this time, the entodermal lung buds are surrounded by a mass of mesenchyme and coelomic epithelium. The entodermal lining eventually becomes folded to form larger and smaller air chambers.

In Necturus, the development of lungs is similar to that of the frog, but the inner surface of the lungs remains quite smooth. The tracheal area of the frog and Necturus shows little differentiation and represents a comparatively short chamber from the lungs to the glottis. In some urodeles, the trachea is well differentiated, possessing cartilaginous, supporting structures (e.g., Amphiuma, Siren ) .

Fig. 305. Lung rudiment of 7-mm. of frog tadpole. (Cf. fig. 258.)

Fig. 306. Lung development in the chick. (All figures, with the exception of A, were redrawn from Locy and Larsell: ’16, Am. J. Anat., vols. 19, 20; A original.) (A) External view of lung rudiment during third day of incubation. (B) Transverse section through pharynx and lung pouches of embryo of 52 to 53 hrs. of incubation. (C) Section slightly anterior to (B), showing laryngotracheal groove. (D) Lateral view of lung outgrowth of chick at close of fourth day of incubation. (E) Diagram of dissection, exposing left lung of 9-day embryo. Air sacs are now evident; observe relation of heart to lungs. (F) Ventral view of lungs and air sacs of 12-day embryo. (G) Diagram of lateral view of bronchi of 9-day embryo. Four ectobronchi, from which parabronchi are arising, are shown at right of figure.

b. Lung Development in the Chick

1) General Features of Lung Development. The development of lungs in the chick differs greatly from that in the Amphibia and other vertebrates. (For a thorough description of the developing lung of the chick, reference should be made to Locy and Larsell, ’16, a and b.)

Lung development begins during the first part of the third day of incubation in the form oFventro-lateraT, ridp^-like enlargements of the pharynx, immediately posterior to the fourth pair of branchial (visceral) pouches. These evaginations arise from a ventral, groove-like trough of the pharyngeal floor (fig. 306A). The entire area of the pliaryngeal floor, where the lung rudiments begin to develop, gradually sinks below the pharyngeal-esophageal level, and its remaining connection with the pharynx proper is the laryngotracheal groove in the floor of the pharynx (fig. 306B, C).

After the lung and tracheal rudiments arc formed, they extend backward rapidly into the surrounding mesenchyme and they soon project dorsaJ]yj._as indicated in figure 306D. The latter figure presents the developmental condition of the lung rudiments late on the fourth day of incubation. Two areas of the lung rudiment are evident, namely, the tracheal and lung rudiments proper. The external appearance of the developing lungs on the ninth day of incubation is shown in figure 306E, while that of the twelfth day with the forming air sacs is shown in figure 306F.

2) Formation of Air Sacs. The air sacs arise as extensions from the main bronchi during the sixth to seventh day of incubation. During the ninth day,^ they are present as well-developed structures (fig. 306E). The abdominal air sac appears as a posterior continuation of the mesobronchus or primary bronchus of the lung, while the cervical air sac arises from the anterior entobronchus, an outgrowth of the mesobronchus at the anterior extremity of the lung. The anterior intermediate, posterior intermediate, and the interclavicular air sacs take their origins from the ventral surface of the lungs and represent outgrowths from the entobronchi (figs. 306G, 307A). The interclavicular air sac arises from the fusion of four moieties, two from each lung. The air sacs lie among the viscera and send out slender diverticula, some of which may enter certain bones (fig. 308B).

Fig. 307. Lung development in the chick. (All figures, after Locy and Larsell: ’16, Am. J. Anat., vols. 19, 20.) (A) Diagram of dissection of lung of 9.5-day embryo, designed to show entobronchi and air-sac connections with bronchial tree. (B) Diagram of mesial aspect of adult lung, showing parabronchial connections between entobronchi and ectobronchi. Dorsal and lateral bronchi are not shown. (C) Simplified diagram to show air capillaries in relation to infundibula and parabronchus. (Blood capillaries added to one sector of figure represent a modification of the original figure.) (D) Diagram of lateral surface of right lung of 15-day embryo, showing recurrent bronchi of abdominal and posterior intermediate air sacs. Anastomoses of recurrent bronchi are also shown.

Fig. 308. Respiratory structures in adult birds. (A after Kingsley, ’12, Comparative Anatomy of Vertebrates, Philadelphia, P. Blakiston’s Son & Co.; B slightly modified from Goodrich, ’30.) (A) Syrinx or voice box of canvasback, Aythya. (B) Diagram of left side view of lungs and air sacs of an adult bird.

3) Formation of the Bronchi and Respiratory Areas of the Chick’s Lung.

Internally, the primary bronchial division of each lung passes into the lung’s substance where it continues as the niesobronchus. The mesobronchus thus represents a continuation of the main or primary bronchial stem of the lung and is a part of the original entodermal outpushing from the pharynx. From the niesobronchus, the ectobronchi and entobronchi arise as diverticula (fig. 307A, B ). The parabronchi or lung pipes develop as connections between the ectobronchi and entobronchi (fig. 307B). The parabronchi constitute the respiratory areas of the lung, for the parabronchi send off from their walls elongated diverticula, the infundibula or vestibules. The vestibules are branched distally (fig. 307C) and anastomose with each other to form the air capillaries. The blood capillaries (fig. 307C) ramify profusely between the air capillaries. It is not clear that the air capillaries possess definite cellular walls throughout.

As indicated in figure 307D, other or recurrent bronchi are formed as air passages which arise from the air sacs and grow back into the lungs, where they establish secondary connections with the other bronchi. The air sacs thus represent expanded parts of the bronchial circuits of the lungs which not only provide buoyancy but effect a more thorough utilization of the available air by the respiratory areas of the lungs. That is, all the air passing through the respiratory parts of the lung is active, moving air. (See Locy and Larsell, 16b, pp. 42-43; Goodrich, ’30, pp. 600-607.)

Fig. 309. Lung development in the mammal. (A-F modified from Flint, ’06; G modified from Maximow and Bloom, ’42, A Textbook of Histology, Philadelphia, Saunders.) (A-F) Development of the bronchial tree in the pig. (G) Terminal respiratory relationships in the human lung. Respiratory bronchioles arise from terminal divisions of the terminal bronchiole; from the respiratory bronchiole arise the alveolar ducts which may terminate in spaces, the atria; from the atrium the alveolar sacs arise; and the side walls of each alveolar sac contain the terminal air sacs or alveoli.

4) Trachea, Voice Box, and Ultimate Position of the Bird’s Lung in the Body. The trachea of the bird’s lung is an elongated structure, reinforced by cartilage rings or plates in the tracheal wall. The voice box of the bird is developed at the base of the trachea in the area of the tracheal division into the two major bronchi. It is an elaborate structure, consisting of a number of folds of the mucous membrane together with an enlargement of this particular area. This structure is known as the syrinx (fig. 308A). The morphological structure of the syrinx varies from species to species. The ultimate position of the bird’s lung in the body is shown in figure 308B.

5) Basic Cellular Composition of the Trachea, Lungs, and Air Sacs. It is obvious from the description above that the entire lining tissue and the respiratory membrane of the bird’s respiratory and air-sac system are derived from the original entodermal evagination, whereas the muscle, connective, and other tissues are formed from the surrounding mesenchyme.

c. Development of Lungs in the Mammal

1) Origin of the Lung Rudiment. The first indication of the appearance of the lungs in the pig and human embryo is the formation of a midventral trough or furrow in the entoderm of the pharynx, the laryngotracheal groove. This groove forms immediately posterior to the fourth branchial (visceral) pouch, approximately at the stage of 3 to 4 mm. in both pig and human. In the human, about the fourth week, and 3-mm. pig, the laryngotracheal groove deepens, and its posterior end gradually forms a blind, finger-like pouch which creeps posteriorly below the esophageal area as a separate structure (fig. 309A). Thus, the original laryngotracheal groove is restricted to the cephalic end of the developing lung rudiment, where it forms a slit-like orifice in the midventral floor of the pharynx at about the level of the fifth visceral (i.e., third branchial) arch.

2) Formation of the Bronchi. As the caudal end of the original lung rudiment grows caudad, it soon bifurcates into left and right bronchial stems as shown in figure 309B. Each primary or stem bronchus is slightly enlarged at the distal end. As the stem bronchi of the right and left lung buds continue to grow distally, evaginations or secondary bronchi arise progressively from the primary bronchi as indicated in figure 309C-E. While this statement holds true for the human embryo, the apical bronchus (i.e., eparterial bronchus because this lobe of the lung comes to lie anterior to the pulmonary artery) in the pig arises directly from the trachea as shown in figure 309D. Each of these secondary bronchi forms the main bronchus for the upper and middle lobes of the lungs (fig. 309D, E). From each lobular bronchus, other bronchial buds arise progressively and dichotomously, with the result that the bronchial system within each lobe of the lung becomes complex, simulating the branches upon the limb of a tree. Considerable variation may exist in the formation of the various bronchi in different individuals.

3) Formation of the Respiratory Area of the Lung. This growth of bronchial buds of the pulmonary tree continues during fetal life and for a considerable time after birth. The large bronchi give rise to smaller bronchi, and, from the latter, bronchioles of several orders originate. Finally, the terminal bronchioles arise. Fifty to eighty terminal bronchioles have been estimated to be present for each lobule of the human lung (Maximow and Bloom, ’42, p. 465). From each of the terminal bronchioles, a varying number of respiratory bronchioles arise, which in turn give origin to the alveolar ducts, and, from the latter, arise the alveolar sacs and alveoli. Each alveolus represents a thin-walled compartment of the alveolar sac (fig. 309G). The exact cellular structure of the terminal air compartments or alveoli is not clear. In the frog lung, a layer of flattened epithelium is present. However, in the lung of the bird and the mammal, this epithelial lining may not be complete, and the wall of the alveolus may be formed, in part at least, by the endothelial cells of the surrounding capillaries (fig. 299A; Palmer, ’36; Clements, ’38).

4) Development of the Epiglottis and Voice Box. The epiglottis is the structure which folds over the glottis and thus covers it during deglutition. The glottis is the opening of the trachea into the pharynx. An epiglottis is found only in mammals. It arises as a fold in the pharyngeal floor in the area between the third and fourth visceral arches. It grows upward and backward in front of the developing glottis (fig. 310A~C) . In the meantime, the arytenoid swellings or ridges appear on either side of the glottis.

The larynx or voice box is an oval-shaped compartment at the anterior end of the trachea in mammals. It is supported by cartilages derived from the visceral arches (Chap. 15). The vocal cords arise as transverse folds along the lateral sides of the laryngeal wall.

5) Cellular Composition. The epithelial lining of the larynx, trachea, bronchi, etc., is derived from the entodermal outpushing, whereas the surrounding mesenchyme gives origin to the cartilage, muscle, and connective tissue present in these structures.

Fig. 310. Development of the epiglottis and entrance into the larynx in the human embryo. (Consult also fig. 285.) (All figures slightly modified from Keibel and Mall: Manual of Human Embryology, vol. II, ’12, Philadelphia, Lippincott.) (A) About 16-mm., crown-rump length, 7 to 8 weeks. (B) About 40-mm., crown-rump length, 9 to 10 weeks. (C) Late fetal condition.

6) Ultimate Position of the Mammalian Lung in the Body. See Chapter 20.

3. Development of Air Bladders

It is difficult to draw a clear distinction between air bladders of Pisces and the lungs of Tetrapoda. Air bladders and gills appear to be the standard arrangement for most fishes. It is probable, therefore, that the function of external respiration rests mainly upon the branchiae or gills in all fishes other than the Dipnoi, while the function of buoyancy is the responsibility of the air bladder. In some fishes (Dipnoi and ganoids), the functions of buoyancy and respiration converge into one structure, the air bladder or lung, as they do in many Tetrapoda.

In development, air bladders, like the lungs of all Tetrapoda, arise as diverticula of the posterior pharyngeal area. In most cases, the air bladder arises as a dorsal diverticulum (fig. 304A, B), while, in other instances, its origin appears to be from the lateral wall (fig, 304C). In Salmonidae, Siluridae, etc., for example, it arises from the right wall, while in Cyprinidae, Characinidae, etc., it takes its origin from the left wall. The air bladder generally is a single structure (fig. 304A, C, D), but in some cases it is double or bilobed (fig. 304E).

Generally speaking, the air bladder receives blood from the dorsal aorta or its immediate branches (fig. 304G), but in Dipnoi and Polypterus, the blood supply to the air bladder comes from the pulmonary arteries as it does in Tetrapoda.

4. Lunglessness

Many urodele amphibia have reduced or lost their lungs entirely. In many cases the reduced condition of the lungs or absence of lungs is compensated for by the development of buccopharyngeal respiration. The latter type of respiration depends upon an extreme vascularization of the pharyngeal and caudal mouth epithelium and rapid throat movements which suck the air in and then expel it. In Aneides (Autodax) liigubrus, a land form, these throat movements may reach 120 to 180 movements per minute (Ritter and Miller, 1899). Lungless aquatic salamanders also practice buccopharyngeal respiration, although, in Pseudotriton ruber, cutaneous respiration evidently is resorted to (Noble, ’25).


Clements, L. P. 1938. Embryonic develop- Eycleshymer, A. C. 1906. The growth and ment of the respiratory portion of the regeneration of the gills in the young pig’s lung. Anat. Rec. 70:575. ‘ Necturus. Biol. Bull. X: 171.

Flint, J. M. 1906. The development of the lungs. Am. J. Anat. 6:1.

Goodrich, E. S. 1930. Studies on the Structure and Development of Vertebrates. Macmillan and Co., London.

HelflF, O. M. 1924. Factors involved in the formation of the opercular leg perforation in anuran larvae during metamorphosis. Anat. Rec. 29:102.

Locy, W. A. and Larscll, O. 1916a. The embryology of the bird’s lung. Based on observations of the domestic fowl. Part 1. Am. J. Anat. 19:447.

and . 1916b. The embryology of the bird’s lung. Based on observations of the domestic fowl. Part II. Am. J. Anat. 20: 1.

Maximow, A. A. and Bloom, W. 1942. A Textbook of Histology. W. B. Saunders Co., Philadelphia.

Noble, G. K. 1925. The integumentary, pulmonary and cardiac modifications correlated with increased cutaneous respiration in the Amphibia; a solution to the “hairy frog’’ problem. J. Morphol. & Physiol. 40:341.

. 1931. The Biology of the Amphibia. McGraw-Hill Book Co., Inc., New York.


Palmer, D. W. 1936. The lung of a human foetus of 170 mm. C. R. length. Am. J. Anat. 58:59.

Ritter, W. E. and Miller, L. 1899. A contribution to the life history of Autodax lupubris Hallow., a Californian salamander. Am. Nat. 33:691.

Cite this page: Hill, M.A. (2019, May 24) Embryology Book - Comparative Embryology of the Vertebrates 4-14. Retrieved from

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