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Unidirectional pulmonary airflow in vertebrates: a review of structure, function, and evolution

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Abstract

Mechanisms explaining unidirectional pulmonary airflow in birds, a condition where lung gases flow in a consistent direction during both inspiration and expiration in some parts of the lung, were suggested as early as the first part of the twentieth century and unidirectional pulmonary airflow has been discovered recently in crocodilians and squamates. Our knowledge of the functional anatomy, fluid dynamics, and significance of this trait is reviewed. The preponderance of the data indicates that unidirectional airflow is maintained by means of convective inertia in inspiratory and expiratory aerodynamic valves in birds. The study of flow patterns in non-avian reptiles is just beginning, but inspiratory aerodynamic valving likely also plays an important role in controlling flow direction in these lungs. Although highly efficient counter and cross-current blood–gas exchange arrangements are possible in lungs with unidirectional airflow, very few experiments have investigated blood–gas exchange mechanisms in the bird lung and blood–gas arrangements in the lungs of non-avian reptiles are completely unknown. The presence of unidirectional airflow in non-volant ectotherms voids the traditional hypothesis that this trait evolved to supply the high aerobic demands of flight and endothermy, and there is a need for new scenarios in our understanding of lung evolution. The potential value of unidirectional pulmonary airflow for allowing economic lung gas mixing, facilitating lung gas washout, and providing for adequate gas exchange during hypoxic conditions is discussed.

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Acknowledgments

The authors thank Scott Echols for the computed tomography dataset used in Figs. 24a. This work was supported by the United States National Science Foundation (IOS 0818973 and IOS 1055080 to C.G.F., and a Graduate Research Fellowship to R.L.C).

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Correspondence to Robert L. Cieri.

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Communicated by I.D. Hume.

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Cieri, R.L., Farmer, C.G. Unidirectional pulmonary airflow in vertebrates: a review of structure, function, and evolution. J Comp Physiol B 186, 541–552 (2016). https://doi.org/10.1007/s00360-016-0983-3

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  • DOI: https://doi.org/10.1007/s00360-016-0983-3

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