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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: 9.79). 12/2006; 81(4):545-79. DOI: 10.1017/S1464793106007111
Source: PubMed

ABSTRACT 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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    • "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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    • "The air capillaries and blood capillaries form about 90% of the volume of the exchange tissue and intertwine closely. Three-dimensional computer reconstruction of serial sections (Woodward and Maina 2005) showed that the long-held notion that the air capillaries are straight "
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