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

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.