Elevated performance: the unique physiology of birds that fly at high altitudes

Abstract

Summary Birds that fly at high altitudes must support vigorous exercise in oxygen-thin environments. Here I discuss the characteristics that help high fliers sustain the high rates of metabolism needed for flight at elevation. Many traits in the O2 transport pathway distinguish birds in general from other vertebrates. These include enhanced gas-exchange efficiency in the lungs, maintenance of O2 delivery and oxygenation in the brain during hypoxia, augmented O2 diffusion capacity in peripheral tissues and a high aerobic capacity. These traits are not high-altitude adaptations, because they are also characteristic of lowland birds, but are nonetheless important for hypoxia tolerance and exercise capacity. However, unique specializations also appear to have arisen, presumably by high-altitude adaptation, at every step in the O2 pathway of highland species. The distinctive features of high fliers include an enhanced hypoxic ventilatory response, an effective breathing pattern, larger lungs, haemoglobin with a higher O2 affinity, further augmentation of O2 diffusion capacity in the periphery and multiple alterations in the metabolic properties of cardiac and skeletal muscle. These unique specializations improve the uptake, circulation and efficient utilization of O2 during high-altitude hypoxia. High-altitude birds also have larger wings than their lowland relatives to reduce the metabolic costs of staying aloft in low-density air. High fliers are therefore unique in many ways, but the relative roles of adaptation and plasticity (acclimatization) in high-altitude flight are still unclear. Disentangling these roles will be instrumental if we are to understand the physiological basis of altitudinal range limits and how they might shift in response to climate change.

Flying high: Limits to flight performance by sparrows on the Qinghai-Tibet Plateau

“…Relative heart and lung masses, by contrast, tend to increase significantly at higher field sites (Fig. 3B,D), suggesting a concomitant physiological response to environmental hypoxia (Dunson, 1965;Carey and Morton, 1976;Monge and León-Velarde, 1991;Scott, 2011). In aggregate, these morphological trends represent a sustained pattern of phenotypic response to longterm montane residence by this species.…”

Hemoglobin–oxygen affinity in high-altitude vertebrates: is there evidence for an adaptive trend?

“…In order for air-breathing vertebrates to cope with the low ambient P O2 at high altitude, blood O 2 transport capacity must be increased to sustain O 2 flux to the tissue mitochondria in support of aerobic ATP synthesis (Mairbäurl, 1994;Samaja et al, 2003;Storz et al, 2010b;Scott, 2011;Mairbäurl and Weber, 2012). Such changes complement physiological adjustments in other convective and diffusive steps in the O 2 transport pathway (Bouverot, 1985;Scott and Milsom, 2006).…”

Simultaneous high-resolution pH and spectrophotometric recordings of oxygen binding in native blood microvolumes

“…Chanutin and Curnish, 1967;Festa and Asakura, 1979) or the environmental adaptation of various organisms (e.g. Brix, 1983;Herbert et al, 2006;Meir et al, 2009;Scott, 2011), and have even resolved crime (Olson et al, 2010). Ever since, researchers have developed and refined techniques to comprehend the complex physiology of oxygen transport, leading to a variety of currently employed methods (supplementary material Table S1).…”