Morphological and morphometric specializations of the lung of the Andean goose, Chloephaga melanoptera: A lifelong high-altitude resident.

John N Maina,William K Milsom,Kevin G Mccracken,Julia M York,Beverly Chua,James West

doi:10.1371/journal.pone.0174395

John N Maina, William K Milsom + Show 4 more

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https://doi.org/10.1371/journal.pone.0174395

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Abstract

High altitude flight in rarefied, extremely cold and hypoxic air is a very challenging activity. Only a few species of birds can achieve it. Hitherto, the structure of the lungs of such birds has not been studied. This is because of the rarity of such species and the challenges of preparing well-fixed lung tissue. Here, it was posited that in addition to the now proven physiological adaptations, high altitude flying birds will also have acquired pulmonary structural adaptations that enable them to obtain the large amounts of oxygen (O2) needed for flight at high elevation, an environment where O2 levels are very low. The Andean goose (Chloephaga melanoptera) normally resides at altitudes above 3000 meters and flies to elevations as high as 6000 meters where O2 becomes limiting. In this study, its lung was morphologically- and morphometrically investigated. It was found that structurally the lungs are exceptionally specialized for gas exchange. Atypically, the infundibulae are well-vascularized. The mass-specific volume of the lung (42.8 cm3.kg-1), the mass-specific respiratory surface area of the blood-gas (tissue) barrier (96.5 cm2.g-1) and the mass-specific volume of the pulmonary capillary blood (7.44 cm3.kg-1) were some of the highest values so far reported in birds. The pulmonary structural specializations have generated a mass-specific total (overall) pulmonary morphometric diffusing capacity of the lung for oxygen (DLo2) of 0.119 mlO2.sec-1.mbar-1.kg-1, a value that is among some of the highest ones in birds that have been studied. The adaptations of the lung of the Andean goose possibly produce the high O2 conductance needed to live and fly at high altitude.

Highlights

Biologists have long strived to understand how differences in the functional designs of the vertebrate respiratory systems correlate with metabolism, lifestyle and environment inhabited [1,2,3,4]
Interparabronchial blood vessels gave rise to relatively smaller intraparabronchial ones (Figs 1C–1E, 2A and 2B), the atria were conspicuous (Figs 1C, 1D and 2A–2D) and the infundibulae were intensely vascularized (Fig 2C–2F). This is an uncharacteristic feature of the lungs of birds that have so far been studied where the surface of the infundibulae is nonvascular (Fig 3A) with blood capillaries (BCs) being located in the lung parenchyma (LP)
While most of the BCs connected by means of epithelial-epithelial cell retinaculae that separated the air capillaries (ACs) (Fig 3D and 3E), some BCs attached directly (Fig 3D and 3E)

Summary

Introduction

Biologists have long strived to understand how differences in the functional designs of the vertebrate respiratory systems correlate with metabolism, lifestyle and environment inhabited [1,2,3,4]. Powered (active) flight is the most costly mode of locomotion [13,14,15,16]. It exacts various physiological and morphological adaptations [17]. Birds that fly at extreme altitude, the so-called ‘super birds’ [18], operate under very low ambient temperature and dry, rarefied and hypoxic air [19, 20]. To avoid the challenges presented by flight at high elevation, lowland resident birds that cannot tolerate extreme hypoxia [5] cover long distances to avoid flying over high obstacles [21]

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