Bronchial Airway System

While the molecular and genetic controls of the development of the tracheal system of insects (e.g. Sutherland et al. 1996; Jarecki et al. 1999; Sato and Kornberg 2002) and the BALu have now been well documented (e.g. Cardoso 2000, 2001; Hislop 2002; Xiao et al. 2003), little is known about the processes that occur in the avian respiratory system. In the domestic fowl, the embryonic lungs first become perceptible from day 3.5 (about stage 26; Hamburger and Hamilton 1951) of embryogenesis (e.g. Duncker 1978; Maina 2003a,b). They appear like small, ridge-like outgrowths (Fig. 4A). Between days 3.5 and 5.5, the swellings approximate (Fig. 4B) and fuse on the ventral midline. Thereafter, they divide into left and right primordial lung buds (Fig. 4C,D). The lung buds form by multiplication and projection of the epithelial (endodermal) cells (that initially lined the primitive foregut) into the surrounding mes-enchyme (Fig. 5A,B). The buds are covered by a somatopleural mesothelium (Fig. 5B). As they progressively advance into the coelomic cavity, the developing lungs diverge towards the respective lateral aspects of the body wall (Fig. 4D), reaching their definitive topographical locations on the dorsolateral aspect of the coelomic cavity at about day 8 (Fig. 6A). At that stage, the lung buds have enlarged and transformed from a saccular to a rather wedge shape

Bronchial Buds

Fig. 4. A Lung buds (arrowheads) developing on the ventral aspect of the floor of the primitive pharynx. Arrow Gastrointestinal system. Day 3. B Lung buds approximating on the ventral midline (arrowheads). Arrows Gastrointestinal system. Day 4. C Saccular lungs (arrowheads) diverging and advancing towards the dorsolateral aspects of the coelomic cavity. Stars Branchial arches. Day 5. D Close-up of the lungs (arrowheads). Arrow Gastrointestinal system; asterisk trachea. Day 5. The knobbed arrow shows the cranial-caudal orientation of the specimen. Figures 4-20 and 22-36 are preparations from the domestic fowl, Gallus gallus variant domesticus. (Maina 2003b)

Fig. 4. A Lung buds (arrowheads) developing on the ventral aspect of the floor of the primitive pharynx. Arrow Gastrointestinal system. Day 3. B Lung buds approximating on the ventral midline (arrowheads). Arrows Gastrointestinal system. Day 4. C Saccular lungs (arrowheads) diverging and advancing towards the dorsolateral aspects of the coelomic cavity. Stars Branchial arches. Day 5. D Close-up of the lungs (arrowheads). Arrow Gastrointestinal system; asterisk trachea. Day 5. The knobbed arrow shows the cranial-caudal orientation of the specimen. Figures 4-20 and 22-36 are preparations from the domestic fowl, Gallus gallus variant domesticus. (Maina 2003b)

(Fig. 6A). Next, the lungs rotate along longitudinal and transverse axes and start to engage and insert into the underlying ribs. From the end of day 9, they are firmly affixed to the ribs and the hilus lies on the craniomedial aspect. Costal impressions (sulci) are conspicuous on the dorsolateral aspect of the lung (Fig. 6B-D).

Forming as an extension of the trachea and the extrapulmonary primary bronchus (EPPB), the intrapulmonary primary bronchus (IPPB) is the first airway to form (Fig. 7A). It runs from the hilus to the caudal edge of the devel-

Trachea And Lung Bud

Fig. 5. A Lung bud (dashed oval enclosure) developing on the ventrolateral aspect of the foregut. Dashed arrow Endothelial cells extending into the underlying mesenchymal cells (MC). Day 3. B Close-up of the developing lung (after the fusion of the right and left lung buds) showing the trachea lined by an epithelium with conspicuously large epithelial cells (arrows). EC Endothelial cells; dashed area mesenchymal cells (MC); arrowhead mesothe-lial cells covering the formative lung. Day 5. (Maina 2003a)

Fig. 5. A Lung bud (dashed oval enclosure) developing on the ventrolateral aspect of the foregut. Dashed arrow Endothelial cells extending into the underlying mesenchymal cells (MC). Day 3. B Close-up of the developing lung (after the fusion of the right and left lung buds) showing the trachea lined by an epithelium with conspicuously large epithelial cells (arrows). EC Endothelial cells; dashed area mesenchymal cells (MC); arrowhead mesothe-lial cells covering the formative lung. Day 5. (Maina 2003a)

Avian Lung

Fig. 6. A Lungs (Lu) starting to insert into the ribs (arrowheads). Day 6. B Longitudinal section of the lung showing costal sulci (dashed circles). Arrows Developing parabronchi; arrowheads secondary bronchi. Day 9. C Lateral surface of the lung showing anastomosing parabronchi (arrows). Arrowheads Costal sulci. Day 10. D Lateral surface of the lung showing well-developed parabronchi (arrows) and costal sulci (arrowheads). Day 13. (Maina 2003b)

Fig. 6. A Lungs (Lu) starting to insert into the ribs (arrowheads). Day 6. B Longitudinal section of the lung showing costal sulci (dashed circles). Arrows Developing parabronchi; arrowheads secondary bronchi. Day 9. C Lateral surface of the lung showing anastomosing parabronchi (arrows). Arrowheads Costal sulci. Day 10. D Lateral surface of the lung showing well-developed parabronchi (arrows) and costal sulci (arrowheads). Day 13. (Maina 2003b)

oping lung. From day 9, secondary bronchi (SB) progressively sprout from the various aspects of the luminal (circumferential) surface of the IPPB and radiate outwards (Figs. 7B-D and 8A-F). The IPPB terminates in the formative abdominal air sac (AAS; Fig. 8D,F-H). Inaugurating as solid cords of epithelial cells (Fig. 9A), parabronchi (PR; tertiary bronchi) form. As the PR lengthen, they develop a lumen that is encircled by epithelial cells (Fig. 9B,C). External to the developing PR are cy to architecturally heterogeneous mesenchymal cells (Mc, Fig. 9D). Successively, the PR grow and anastomose pro-

Primary Bronchus
Fig. 7A-D. Embryonic avian lungs grown on matrigel rafts at day 7 of development (stage 28). PB Primary bronchus; SB secondary bronchus; GIT gastrointestinal system. Scale bars 0.1 mm. J.N. (Maina and B.K. Kramer, unpubl. observ.)

fusely as they interconnect the SB (Figs. 10 and 11), ultimately forming the bulk of the lung. Initially, columnar epithelial cells line the parabronchial lumina (PRL, Fig. 12A-C). The cells attach onto a basement lamina (BL, Fig. 12B,C). Mesenchymal cells affix onto the outer surface of the BL (Fig. 12B,C). In due course, epithelial cells transform and organize into cords that delineate the atria (Fig. 11D), out pocketings from the luminal surface of the PR (Figs. 11D and 12D). Initially,the epithelial cells that line the PRL join across laterally located bridge-like extensions (Fig. 13A), large intercellular spaces exist between the epithelial cells that project prominently into the PRL (13A,B). As the atria form, they give rise to a variable number of infundibulae (Figs. 14 and 15).The atria are conspicuous on day 15, the infundibulae on day

Avian Lung

Fig. 8A-H. Embryonic avian lungs grown on matrigel rafts at day 10 showing a primary bronchus (PB) giving rise to secondary bronchi (SB). The expansions at the ends of the primary bronchus (arrows) may give rise to air sacs. Ep Epithelium. Scale bars 0.5 mm. J.N. (Maina and B.K. Kramer, unpubl. observ.)

Fig. 8A-H. Embryonic avian lungs grown on matrigel rafts at day 10 showing a primary bronchus (PB) giving rise to secondary bronchi (SB). The expansions at the ends of the primary bronchus (arrows) may give rise to air sacs. Ep Epithelium. Scale bars 0.5 mm. J.N. (Maina and B.K. Kramer, unpubl. observ.)

Avian Lungs

Fig. 9. A Cluster of epithelial cells (Ec) surrounded by mesenchymal cells (Mc). Day 9. B Parabronchi (arrows) with a formed lumen. Mc Mesenchymal cells. Day 11. C Close-up of a developing parabronchus (Pr) surrounded by a columnar epithelium (Ec). Mc Mesenchymal cells. Day 15. D Mesenchymal cells of the stroma of the developing avian lung showing interconnections by thin cytoplasmic extensions (arrows). Day 16. (Maina 2003b)

Fig. 9. A Cluster of epithelial cells (Ec) surrounded by mesenchymal cells (Mc). Day 9. B Parabronchi (arrows) with a formed lumen. Mc Mesenchymal cells. Day 11. C Close-up of a developing parabronchus (Pr) surrounded by a columnar epithelium (Ec). Mc Mesenchymal cells. Day 15. D Mesenchymal cells of the stroma of the developing avian lung showing interconnections by thin cytoplasmic extensions (arrows). Day 16. (Maina 2003b)

16, and the AC and the blood capillaries (BC) on day 18 (Figs. 16-18). The atria, infundibulae, and AC form by massive remodeling of the mesenchymal cell stroma of the 'undifferentiated' exchange tissue (ET, parenchyma) of the developing lung (Figs. 14-18). In the rat lung, the canaliculi enlarge with condensation of the mesenchyme, a process brought about by programmed cell death (apoptosis; Stiles et al. 2001). Progressively, in the lung of the domestic fowl, the AC approximate the BC, as the thickness of the BGB attenuates. By time of hatching (day 21), the AC and BC have lavishly intertwined with each other and the BGB is remarkably thin (Fig. 18C,D).

Fig. 10. A Parabronchi (Pb) extending (arrows) into the surrounding mesenchymal cells (MC). Day 15. B Parabronchi (Pb) at the periphery of the lung budding (arrowheads) and projecting inwards (arrows). MC Mesenchymal cells. Day 16. C A parabronchus (Pb) branching (arrows) and extending into the mesenchymal cells (MC). Day 16. D Close-up of secondary bronchus (SB) from which parabronchi (arrows) are sprouting. MC Mesenchymal cells; arrow heads developing blood vessels. Day 10. (Maina 2003a)

Fig. 10. A Parabronchi (Pb) extending (arrows) into the surrounding mesenchymal cells (MC). Day 15. B Parabronchi (Pb) at the periphery of the lung budding (arrowheads) and projecting inwards (arrows). MC Mesenchymal cells. Day 16. C A parabronchus (Pb) branching (arrows) and extending into the mesenchymal cells (MC). Day 16. D Close-up of secondary bronchus (SB) from which parabronchi (arrows) are sprouting. MC Mesenchymal cells; arrow heads developing blood vessels. Day 10. (Maina 2003a)

Starting with a narrow lumina and proportionately thick ET (Fig. 19A,C), gradually, the PRL enlarge at the expense of the gas ET (Fig. 19D). In birds like the domestic fowl (galliforms), interparabronchial septa (IPRS), bands of connective tissue that separate PR, form (Fig. 19C). The paleopulmonary parabronchi (PPPR) and the neopulmonary parabronchi (NPPR; Chap. 3.6) are well formed and have intensely anastomosed by day 14 (Fig. 20). The PPPR are hoop-like in orientation and are located dorsal to the primary bronchus (PB), while the NPPR are generally located ventral to the PB and anastomose more profusely (Fig. 20C). Where they exist, the IPRS bestow a rather hexagonal (geodesic) shape to the PR (Fig. 19D). The shape may optimize the packaging of the PR in the lung. In the avian lung, a large number of PR gives a higher volume of ET that in turn should confer more extensive RSA. In human engineering (e.g. French 1988), geodesic design is known to

Secondary Bronchus Section

Fig. 11. A Cross section of the primary bronchus (Pb) giving rise to secondary bronchi (arrowheads) that in turn give rise to parabronchi (arrows). Day 15. B A primary bronchus (Pb) giving rise to secondary bronchi (arrowheads) that in turn give rise to parabronchi (arrows). Day 16. C Parabronchi (Pr). Dashed area Anastomosing parabronchi; Ex exchange tissue. Day 16. D Longitudinal view of a parabronchus showing atria (At) that are separated by atrial muscles (arrowheads). Ex Exchange tissue. Day 18. (Maina 2003b)

Fig. 11. A Cross section of the primary bronchus (Pb) giving rise to secondary bronchi (arrowheads) that in turn give rise to parabronchi (arrows). Day 15. B A primary bronchus (Pb) giving rise to secondary bronchi (arrowheads) that in turn give rise to parabronchi (arrows). Day 16. C Parabronchi (Pr). Dashed area Anastomosing parabronchi; Ex exchange tissue. Day 16. D Longitudinal view of a parabronchus showing atria (At) that are separated by atrial muscles (arrowheads). Ex Exchange tissue. Day 18. (Maina 2003b)

impart stronger construction. The cells of the bee's wax are perhaps the best known example of exploitation of geodesic design in nature. The avian lung is reported to be very strong: compression of the lung does not cause significant collapse of the AC (Macklem et al. 1979). In species of birds where IPRS are well formed, the AC and BC of adjacent PR do not communicate. The granular pneumocytes (type II cells) are conspicuous from day 17 of development (Figs. 15B-D and 16B). Thereafter, the surfactant should appear on the respiratory surface.

Fig. 12. A Parabronchus (Pr) lined by an epithelium (Ec) that comprises of columnar cells. Ms Mesenchymal cells. Day 12. B, C Parabronchi (Pr) surrounded by an epithelium (Ec) that comprises simple columnar cells. Arrowheads Basement lamina; Ms mesenchymal cells. Day 13. D Cross section of a parabronchus (dashed circle) showing developing atria between atrial muscles (arrows). Arrowhead The parabronchial epithelial lining from which the atrial muscles develop; dashed lines radiating from the dashed circle positions of the inter-parabronchial septa that separate adjacent parabronchi. Day 14. (Maina 2003b)

Fig. 12. A Parabronchus (Pr) lined by an epithelium (Ec) that comprises of columnar cells. Ms Mesenchymal cells. Day 12. B, C Parabronchi (Pr) surrounded by an epithelium (Ec) that comprises simple columnar cells. Arrowheads Basement lamina; Ms mesenchymal cells. Day 13. D Cross section of a parabronchus (dashed circle) showing developing atria between atrial muscles (arrows). Arrowhead The parabronchial epithelial lining from which the atrial muscles develop; dashed lines radiating from the dashed circle positions of the inter-parabronchial septa that separate adjacent parabronchi. Day 14. (Maina 2003b)

In the BALu substantial development, growth, and remodeling of the terminal airways and alveoli occur postnatally, with the BGB thinning and the RSA extending at the end of the embryonic life and for a certain time post-natally (e.g. Burri and Weibel 1977; Schittny and Burri 2004). Moreover, the degree of lung development at birth varies greatly among mammalian species. The marsupial quokka wallaby, Setonix brachyurus, e.g., is born with the lung at the canalicular stage of development (Makanya et al. 2001) and the highly neotenic naked mole rat, Heterocephalus glaber, carries a rela-

Avian Lung

Fig. 13. A Epithelial cells (EC) lining the lumen of a developing parabronchus. The apical aspects (arrowheads) project deeply into the parabronchial lumen (PL). The cells are interconnected through laterally located intercellular junctions (arrows). Stars Intercellular spaces; BL basement lamina; MC mesenchymal cells. Day 15. B Close-up of the apical aspects of the epithelial cells (EC) extending into the parabronchial lumen (PL). Arrowheads Microvilli; arrows intercellular spaces. Day 16. (Maina 2003a)

Fig. 13. A Epithelial cells (EC) lining the lumen of a developing parabronchus. The apical aspects (arrowheads) project deeply into the parabronchial lumen (PL). The cells are interconnected through laterally located intercellular junctions (arrows). Stars Intercellular spaces; BL basement lamina; MC mesenchymal cells. Day 15. B Close-up of the apical aspects of the epithelial cells (EC) extending into the parabronchial lumen (PL). Arrowheads Microvilli; arrows intercellular spaces. Day 16. (Maina 2003a)

Cross Section Microvilli

Fig. 14. A Cross section of a developing parabronchus (Pr) in which atria (arrowheads) have formed. Arrows Infundibulae; Mc mesenchymal cells. Day 15. B Atria (Af) separated by atrial muscles (arrows) giving rise to infundibulae (If). Ex Exchange tissue; arrowheads developing air capillaries. Day 16. C Infundibulae (If) giving rise to air capillaries (arrows). Ex Exchange tissue; Af, atria. Day 17. D Atria (Af) forming infundibulae (If) that in turn give rise to air capillaries (arrows). Arrowheads Strut-like muscular structures that may support the developing atria; circle, a site where adjacent atria anastomose. Day 19. (Maina 2003b)

Fig. 14. A Cross section of a developing parabronchus (Pr) in which atria (arrowheads) have formed. Arrows Infundibulae; Mc mesenchymal cells. Day 15. B Atria (Af) separated by atrial muscles (arrows) giving rise to infundibulae (If). Ex Exchange tissue; arrowheads developing air capillaries. Day 16. C Infundibulae (If) giving rise to air capillaries (arrows). Ex Exchange tissue; Af, atria. Day 17. D Atria (Af) forming infundibulae (If) that in turn give rise to air capillaries (arrows). Arrowheads Strut-like muscular structures that may support the developing atria; circle, a site where adjacent atria anastomose. Day 19. (Maina 2003b)

tively immature lung to adulthood (Maina et al. 1992). In sensorial mammals such as mice and rats, pups are born with lungs at the saccular stage, in humans they are at the early alveolar stage, and in precocial mammals such as sheep they are at the late alveolar stage (Schittny and Burri 2004). On the whole, the PRLu is well developed and functionally competent at the end of the incubation period (Duncker 1978; Maina 2003a,b). The structural components, especially the AC and the BC, are well formed and reach their greatest number and size, while the BGB is noticeably thin. Thereafter, only streamlining and consolidation of the constitutive components occur: no

Fig. 15. A A developing parabronchus showing a lumen (asterisk) surrounded by atrial muscles (AM). Arrows Communication between the atria and infundibulae with the parabronchial lumen; arrowheads, atria. Day 15. B Parabronchial lumen (asterisk) surrounded by atrial muscles (AM). Arrow Connection between an atrium and parabronchial lumen; stars sites where atrial muscles interconnect. At Atria; arrowheads putative type II (granular) pneumocytes. Day 17. C Exchange tissue of a parabronchus showing the parabronchial lumen (asterisk) and forming atria (arrows) leading into the infundibulae (If). Star Site atrial muscles connect; arrowheads developing air capillaries; IPS inter-parabronchial septum. Day 17. D Close-up of the exchange tissue showing infundibulae (If) giving rise to air capillaries (arrowheads). AM Atrial muscles; arrows red blood cells contained in blood capillaries. Day 17. (Maina 2003a)

Fig. 15. A A developing parabronchus showing a lumen (asterisk) surrounded by atrial muscles (AM). Arrows Communication between the atria and infundibulae with the parabronchial lumen; arrowheads, atria. Day 15. B Parabronchial lumen (asterisk) surrounded by atrial muscles (AM). Arrow Connection between an atrium and parabronchial lumen; stars sites where atrial muscles interconnect. At Atria; arrowheads putative type II (granular) pneumocytes. Day 17. C Exchange tissue of a parabronchus showing the parabronchial lumen (asterisk) and forming atria (arrows) leading into the infundibulae (If). Star Site atrial muscles connect; arrowheads developing air capillaries; IPS inter-parabronchial septum. Day 17. D Close-up of the exchange tissue showing infundibulae (If) giving rise to air capillaries (arrowheads). AM Atrial muscles; arrows red blood cells contained in blood capillaries. Day 17. (Maina 2003a)

important new structures appear after hatching. The final remodeling of the parenchyma occurs through extensive apoptosis, especially during the last 3 days of development. In the mammalian (rat) lung, apoptosis occurs towards the third postnatal week of development (Schittny et al. 1998; Bruce et al. 1999). Duncker (1978) attributed the accelerated embryonic development of

Avian Lung

Fig. 16. A A formative infundibulum (If) giving rise to air capillaries (AC). EC Epithelial cells; stars red blood cells. Day 16. B Close-up of an infundibulum (If) with type II (granular) pneumocytes (GP) in the surrounding epithelium. Arrowheads Osmiophilic lamellated bodies; stars red blood cells. Day 17. C Exchange tissue showing blood capillaries containing red blood cells (stars) surrounded by developing air capillaries (AC). Arrowheads Conspicuously thick blood-gas barrier (BGB). Day 18. D Exchange tissue at the periphery of a parabronchus showing blood capillaries containing red blood cells (stars) surrounded by air capillaries (AC). The blood-gas barrier (arrowheads) is much thinner. IPS Inter-parabronchial septum. Day 20. (Maina 2003a)

Fig. 16. A A formative infundibulum (If) giving rise to air capillaries (AC). EC Epithelial cells; stars red blood cells. Day 16. B Close-up of an infundibulum (If) with type II (granular) pneumocytes (GP) in the surrounding epithelium. Arrowheads Osmiophilic lamellated bodies; stars red blood cells. Day 17. C Exchange tissue showing blood capillaries containing red blood cells (stars) surrounded by developing air capillaries (AC). Arrowheads Conspicuously thick blood-gas barrier (BGB). Day 18. D Exchange tissue at the periphery of a parabronchus showing blood capillaries containing red blood cells (stars) surrounded by air capillaries (AC). The blood-gas barrier (arrowheads) is much thinner. IPS Inter-parabronchial septum. Day 20. (Maina 2003a)

the PRLu, particularly during the final days, to mechanical ventilation of the lung, a process that is reported to occur before hatching (e.g. Visschedijk 1968).

Among birds, evident differences exist in the degrees of lung development between altricial and precocial birds (Duncker 1978). In the latter, e.g., the domestic fowl and the herring gull, Larus argentatus, of which the chicks receive little or no parental care and the chicks are able to walk and feed soon after hatching, the atria and the gas ET are well developed at hatching. In altri-

Air Capillary Avian Lung

Fig. 17. A Air capillaries (AC) surrounded by developing blood capillaries that contain red blood cells (stars). Arrows Nuclei of forming endothelial cells; IPS interparabronchial septum. Day 17. B Developing blood capillaries that contain red blood cells (stars) extending and surrounding the air capillaries (AC). Arrowheads Cells and connective tissue elements breaking down and leading to interconnection of the blood capillaries; EC endothelial cells. Day 17. C Close-up of developing air capillaries (AC) and blood capillaries containing red blood cells (stars). Arrows Sites where connective tissues and cells have broken down to allow connection between the developing blood capillaries; dashed area a site where cells are breaking down to lead to an air capillary being totally surrounded by a blood capillary; arrowhead formative BGB. Day 18. D Air capillaries (AC) and developing blood capillaries containing red blood cells (stars). Arrows Disintegrating mesenchymal cells; arrowheads, extension of and formation of vascular spaces. Day 19. (Maina 2003a)

Fig. 17. A Air capillaries (AC) surrounded by developing blood capillaries that contain red blood cells (stars). Arrows Nuclei of forming endothelial cells; IPS interparabronchial septum. Day 17. B Developing blood capillaries that contain red blood cells (stars) extending and surrounding the air capillaries (AC). Arrowheads Cells and connective tissue elements breaking down and leading to interconnection of the blood capillaries; EC endothelial cells. Day 17. C Close-up of developing air capillaries (AC) and blood capillaries containing red blood cells (stars). Arrows Sites where connective tissues and cells have broken down to allow connection between the developing blood capillaries; dashed area a site where cells are breaking down to lead to an air capillary being totally surrounded by a blood capillary; arrowhead formative BGB. Day 18. D Air capillaries (AC) and developing blood capillaries containing red blood cells (stars). Arrows Disintegrating mesenchymal cells; arrowheads, extension of and formation of vascular spaces. Day 19. (Maina 2003a)

Fig. 18. A Developing blood capillaries (BC) with some of them containing red blood cells (stars). AC Air capillaries; arrows formative endothelial cells; arrowheads BGB. Day 18. B Thin BGB (arrowheads) between air capillaries (AC) and developing blood capillaries some of which contain red blood cells (stars). Arrows Formative endothelial cells or disintegrating mesenchymal cells. Day 19. C Air capillaries (AC) and blood capillaries containing red blood cells (stars). Arrowheads Thick parts of the BGB. Day 21. D Air capillaries (AC) and blood capillaries containing red blood cells (stars). Arrowheads Thin BGB. Day 26. (Maina 2003a)

Fig. 18. A Developing blood capillaries (BC) with some of them containing red blood cells (stars). AC Air capillaries; arrows formative endothelial cells; arrowheads BGB. Day 18. B Thin BGB (arrowheads) between air capillaries (AC) and developing blood capillaries some of which contain red blood cells (stars). Arrows Formative endothelial cells or disintegrating mesenchymal cells. Day 19. C Air capillaries (AC) and blood capillaries containing red blood cells (stars). Arrowheads Thick parts of the BGB. Day 21. D Air capillaries (AC) and blood capillaries containing red blood cells (stars). Arrowheads Thin BGB. Day 26. (Maina 2003a)

cial birds, where the chicks are helpless and unable to feed themselves, e.g., the pigeon, Columba livia, the PR are small, the atria shallow, and the gasexchange mantle is thin. While some growth of the PR continues after hatching in both the precocial and altricial birds, the process is more marked in later taxon where the development of the PR is completed just before the birds start to fly. With minimal or no parental care, adequately efficient lungs are essential for the survival of chicks of precocial birds to enable them to run and/or fly in order to escape from predators and procure food.

Fig. 19. A Stacks of parabronchi (arrows). Arrowhead Costal sulcus. Day 15. B Developing parabronchi (arrows) separated by interparabronchial septa (arrowheads).Ex Exchange tissue. Day 16. C Parabrochi (Pr) with parabronchial lumina surrounded by relatively thick exchange tissue mantle (Ex). Arrowheads Interparabronchial septa. Day 18. D Parabronchi (Pr) with wide parabronchial lumina and thin gas exchange tissue (Ex). Day 26. (Maina 2003a)

Fig. 19. A Stacks of parabronchi (arrows). Arrowhead Costal sulcus. Day 15. B Developing parabronchi (arrows) separated by interparabronchial septa (arrowheads).Ex Exchange tissue. Day 16. C Parabrochi (Pr) with parabronchial lumina surrounded by relatively thick exchange tissue mantle (Ex). Arrowheads Interparabronchial septa. Day 18. D Parabronchi (Pr) with wide parabronchial lumina and thin gas exchange tissue (Ex). Day 26. (Maina 2003a)

On the whole, in the avian lung, a 'tree-like' arrangement where arteries and veins strictly track the airways, as occurs in the mammalian lung (Fig. 21), does not form (e.g.Abdalla 1989). The PR anastomose and interconnect the SB, establishing continuity of the air conduits: there are no cul-de-sacs (blind-ends) in the PRLu. While in the BALu the airway system forms by regular dichotomous bifurcation, with branches following predictable dorsoventral, mediolateral, and proximal-distal trajectories (e.g. Adamson 1997; Cardoso 2001; Schittny and Burri 2004; Fig. 21A,C), in the PRLu the

Fig. 20. A Parabronchi (arrows) on the craniomedial aspect of the lung. Arrowhead First medioventral secondary bronchus. Day 13. B Transverse section of the lung showing a primary bronchus (arrowhead) giving rise to secondary bronchi (arrows). Pr Parabronchi. Day 15. C Longitudinal section of the lung showing a primary bronchus (Pb) giving rise to secondary bronchi (arrows). The dashed line separates the paleopulmonic region of the lung (above) and the neopulmonic one (below). Pr Parabronchi; arrowheads costal sulci. Day 15. D Craniodorsal aspect of the lung showing deep costal impressions (arrowheads) and paleopulmonic parabronchi (Pr) separated by the costal sulci. Day 16. (Maina 2003a)

Fig. 20. A Parabronchi (arrows) on the craniomedial aspect of the lung. Arrowhead First medioventral secondary bronchus. Day 13. B Transverse section of the lung showing a primary bronchus (arrowhead) giving rise to secondary bronchi (arrows). Pr Parabronchi. Day 15. C Longitudinal section of the lung showing a primary bronchus (Pb) giving rise to secondary bronchi (arrows). The dashed line separates the paleopulmonic region of the lung (above) and the neopulmonic one (below). Pr Parabronchi; arrowheads costal sulci. Day 15. D Craniodorsal aspect of the lung showing deep costal impressions (arrowheads) and paleopulmonic parabronchi (Pr) separated by the costal sulci. Day 16. (Maina 2003a)

IPPB runs through the lung (Figs. 7 and 8), giving rise to SB and PR that interconnect the SB (Figs. 9 and 20): a continuous loop of the airway system exists. This design is fundamental to the back-to-front through-flow of air (continuous and unidirectional ventilation) in the avian lung that is effected by the concerted action of the air sacs (e.g. Fedde 1980) and an inherent aerodynamic valving mechanism (Chaps. 3.9 and 3.11).

Bronchial Cast

Fig. 21A-C. Triple latex cast preparations of the lung of the pig, Sus sucrofa, showing that the bronchial system (B), the arterial system (A), and the venous systems (V) pattern each other. Respectively, B, C, and D show the venous, bronchial, and arterial systems. Scale bars 1 cm. (Maina and van Gils 200l)

Fig. 21A-C. Triple latex cast preparations of the lung of the pig, Sus sucrofa, showing that the bronchial system (B), the arterial system (A), and the venous systems (V) pattern each other. Respectively, B, C, and D show the venous, bronchial, and arterial systems. Scale bars 1 cm. (Maina and van Gils 200l)

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