Development, structure and function of a novel organ, the lung-air sac system of birds: To go where no vertebrate has gone

School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown 2193, Johannesburg, South Africa.
Biological Reviews (Impact Factor: 9.67). 12/2006; 81(4):545-79. DOI: 10.1017/S1464793106007111
Source: PubMed


Among the air-breathing vertebrates, the avian respiratory apparatus, the lung-air sac system, is the most structurally complex and functionally efficient. After intricate morphogenesis, elaborate pulmonary vascular and airway (bronchial) architectures are formed. The crosscurrent, countercurrent, and multicapillary serial arterialization systems represent outstanding operational designs. The arrangement between the conduits of air and blood allows the respiratory media to be transported optimally in adequate measures and rates and to be exposed to each other over an extensive respiratory surface while separated by an extremely thin blood-gas barrier. As a consequence, the diffusing capacity (conductance) of the avian lung for oxygen is remarkably efficient. The foremost adaptive refinements are: (1) rigidity of the lung which allows intense subdivision of the exchange tissue (parenchyma) leading to formation of very small terminal respiratory units and consequently a vast respiratory surface; (2) a thin blood-gas barrier enabled by confinement of the pneumocytes (especially the type II cells) and the connective tissue elements to the atria and infundibulae, i.e. away from the respiratory surface of the air capillaries; (3) physical separation (uncoupling) of the lung (the gas exchanger) from the air sacs (the mechanical ventilators), permitting continuous and unidirectional ventilation of the lung. Among others, these features have created an incredibly efficient gas exchanger that supports the highly aerobic lifestyles and great metabolic capacities characteristic of birds. Interestingly, despite remarkable morphological heterogeneity in the gas exchangers of extant vertebrates at maturity, the processes involved in their formation and development are very similar. Transformation of one lung type to another is clearly conceivable, especially at lower levels of specialization. The crocodilian (reptilian) multicameral lung type represents a Bauplan from which the respiratory organs of nonavian theropod dinosaurs and the lung-air sac system of birds appear to have evolved. However, many fundamental aspects of the evolution, development, and even the structure and function of the avian respiratory system still remain uncertain.

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    • "Infundibula from the floor of the atria open into the air capillaries , which are the gas exchanger . Atria , infundibula , and air capillaries are lined with the parabronchial epithelium that contains of granular cells , squamous atrial cells , and squamous respiratory cells ( reviewed in Maina , 2006b ) . The mor - phological similarity between the granular atrial cells in bird species with type II pneumocytes of the mam - malian lung has been reported ( Klika et al . "
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    ABSTRACT: The purpose of this study is to determine the possible changes in the localization of the four Epidermal Growth Factor Receptors and three ligands in quail lungs from the first day of hatching until the 125th after hatching using immunohistochemical methods. Immunohistochemical results demonstrated that four EGFRs and their ligands are chiefly located in the cytoplasm of cells. Additionally, ErbB4, AREG, and NRG1 are localized to the nucleus and nucleolus, but EGF is present in the nucleolus. ErbB2 was also found in the cell membrane. In the epithelium of secondary bronchi, the goblet cells only exhibited ErbB1 and ErbB2, whereas the basal and ciliated cells exhibited EGFRs and ligands immunoreactivity. The atrial granular cells displayed moderate levels of ErbB1-ErbB3 and EGF and strong levels of ErbB4, AREG, and NRG1 immunoreactivity. While the squamous atrial cells and squamous respiratory cells of air capillaries and endothelial cells of blood capillaries exhibited moderate to strong ErbB2, ErbB4, AREG, and NRG1 immunoreactivity, they had negative or weak ErbB1, ErbB3, and EGF immunoreactivity. The expression levels of ErbB2-ErbB4, EGF, AREG, and NRG1 were also detected in fibroblasts. Although ErbB2 was highly expressed in the bronchial and vascular smooth muscle cells, weak expression of ErbB1, ErbB3, AREG and EGF and moderate expression of ErbB4 and NRG1 were observed. Macrophages were only negative for ErbB1. In conclusion, these data indicate that the EGFR-system is functionally active at hatching, which supports the hypothesis that the members of EGFR-system play several cell-specific roles in quail lung growth after hatching. Microsc. Res. Tech., 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
    Microscopy Research and Technique 07/2015; 78(9). DOI:10.1002/jemt.22544 · 1.15 Impact Factor
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    • "Generally, the interatrial septa are inconspicuous and the atria are very shallow in small and metabolically highly active species of birds (Duncker 1974; Maina et al. 1982a) (Fig. 36) and in the ostrich (Maina and Nathaniel 2001). The atria project from the parabronchial lumen into the gas exchange tissue (Figs. 34–37) and give rise to 3 to 8 narrower passages, the infundibulae (McLelland 1989; Maina 2005). In the pigeon and mallard, the infundibulae are 25 to 40 lm wide and about 100 to 150 lm long (West et al. 1977). "
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    ABSTRACT: The avian respiratory apparatus is separated into a gas exchanger (the lung) and ventilators (the air sacs). Synchronized bellows-like movements of the cranial and caudal air sacs ventilate the lung continuously and unidirectionally in a caudocranial direction. With the lungs practically rigid, after their insertion into the ribs and the vertebrae and on attaching to the membranous horizontal septum, surface tension is not a constraining factor to the intensity that the gas exchange tissue can subdivide. Delicate, transparent, capacious and avascular, the air sacs are not directly involved in gas exchange. The airway system comprises of a three-tiered system of passageways, namely a primary bronchus, the secondary bronchi and the tertiary bronchi (parabronchi). The crosscurrent system is formed by the perpendicular arrangement between the mass (convective) air flow in the parabronchial lumen and the centripetal (inward) flow of the venous blood in the exchange tissue; the countercurrent system consists of the centrifugal (outward) flow of air from the parabronchial lumen into the air capillaries and the centripetal (inward) flow of blood in the blood capillaries, and; the multicapillary serial arterialization system is formed by the blood capillaries and the air capillaries where venous blood is oxygenated in succession at the infinite number of points where the respiratory units contact exchange tissue. Together with the aforementioned systems, features like large capillary blood volume, extensive respiratory surface area and thin bloodgas barrier accord high pulmonary diffusing capacity of O2 that supports the high metabolic capacities and energetic lifestyles of birds. Keywords Birds � Lung � Air sacs � Respiration �Development � Flight � Oxygen
    Journal of Ornithology 07/2015; DOI:10.1007/s10336-015-1263-9 · 1.71 Impact Factor
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    • "To gain insight into basal archosaur pulmonary anatomy, and to elucidate how and why the lungs of birds and those of the American alligator diverged, requires the careful study of a range of crocodilian and avian species. Whereas numerous studies are available for both anatomical and physiological aspects of avian lungs (Duncker, 1971; Brackenbury, 1972; Maina & Nathaniel, 2001; Maina, 2006; Farmer & Sanders, 2010), there are few studies of the crocodilian respiratory system, particularly studies that combine physiological and anatomical measurements. The clade Crocodylia is composed of at least two major lineages: Alligatoroidea, which includes the two extant alligator species and seven extant caiman species and Crocodyloidea, which includes the 13+ extant species of crocodiles. "
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    ABSTRACT: THIS PAPER IS FREE ONLINE- GO TO THE WEBSITE TO GET IT! The lungs of birds have long been known to move air in only one direction during both inspiration and expiration through most of the tubular gas-exchanging bronchi (parabronchi). Recently a similar pattern of airflow has been observed in American alligators, a sister taxon to birds. The pattern of flow appears to be due to the arrangement of the primary and secondary bronchi, which, via their branching angles, generate inspiratory and expiratory aerodynamic valves. Both the anatomical similarity of the avian and alligator lung and the similarity in the patterns of airflow raise the possibility that these features are plesiomorphic for Archosauria and therefore did not evolve in response to selection for flapping flight or an endothermic metabolism, as has been generally assumed. To further test the hypothesis that unidirectional airflow is ancestral for Archosauria, we measured airflow in the lungs of the Nile crocodile (Crocodylus niloticus). As in birds and alligators, air flows cranially to caudally in the cervical ventral bronchus, and caudally to cranially in the dorsobronchi in the lungs of Nile crocodiles. We also visualized the gross anatomy of the primary, secondary and tertiary pulmonary bronchi of C. niloticus using computed tomography (CT) and microCT. The cervical ventral bronchus, cranial dorsobronchi and cranial medial bronchi display similar characteristics to their proposed homologues in the alligator, while there is considerable variation in the tertiary and caudal group bronchi. Our data indicate that the aspects of the crocodilian bronchial tree that maintain the aerodynamic valves and thus generate unidirectional airflow, are ancestral for Archosauria.
    PeerJ 03/2013; 1(2):e60. DOI:10.7717/peerj.60 · 2.11 Impact Factor
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