However, unique specializations also appear to have arisen, presumably by high-altitude adaptation, at every step in the O 2 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 O 2 affinity, further augmentation of O 2 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 O 2 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.
Most of the previous work looking for inherent differences between high- and low-altitude birds compared animals in a common environment at sea level. This will be the case in the following discussion unless otherwise stated. It is useful to begin this discussion by outlining the most influential steps in the O 2 transport pathway during exercise in hypoxia. We have assessed this issue in waterfowl using theoretical modeling to calculate the physiological control coefficient for each step in the pathway Fig.
This approach allows physiological traits to be altered individually so that their influence on the whole O 2 pathway can be assessed without compensatory changes in other traits. A physiological trait with a larger control coefficient will have a greater influence on flux through the pathway, so an increase in the capacity of this trait will have a greater overall benefit.
Interestingly, the proportion of control vested in each step was dependent on the inspired O 2 Fig. These results suggest that every step in the O 2 transport pathway can be influential and that the relative benefit of each step changes with altitude.
Schematics of A the cross-current model of gas exchange in the avian lung and B the uniform pool model of gas exchange in the lungs of mammals and most other terrestrial vertebrates.
In the cross-current model, inspired air flows through rigid parabronchioles that are oriented perpendicular to blood capillaries. The partial pressure of O 2 P O2 in the parabronchioles P P O 2 declines along their length as O 2 diffuses into the blood, such that capillaries leaving the exchanger near the entrance of airflow right side of figure take up more O 2 than capillaries leaving near the exit left side.
In the uniform pool model, gas flows in and out of terminal alveoli. Capillary blood flowing past these alveoli extract O 2 , such that capillary P O2 rises and alveolar P O2 P A O 2 declines uniformly to less than the P O2 of gas that entered the alveoli. The cross-current model is therefore considered to be more efficient at gas exchange than the uniform pool model Piiper and Scheid, High capacities at several steps in the O 2 transport pathway have been shown to distinguish high-flying birds from their lowland cousins Fig.
The first step of this pathway, ventilation, appears to be enhanced in high-altitude birds to improve O 2 uptake into the respiratory system. Bar-headed geese also breathe with a more effective breathing pattern, taking much deeper breaths i. There are at least two mechanistic causes for these differences: 1 ventilatory insensitivity to respiratory hypocapnia and 2 a blunting of the metabolic-depression response to hypoxia Scott and Milsom, ; Scott et al.
These differences increase the amount and partial pressure of O 2 that ventilates the pulmonary gas-exchange surface during hypoxia. Bar-headed geese also have enlarged lungs Scott et al. The respiratory system of high-altitude birds therefore seems capable of loading more O 2 into the blood during hypoxia than that of lowland birds. Physiological control analysis of flux through the O 2 transport pathway in waterfowl.
The capacity for O 2 diffusion in the muscle D m has a large influence on O 2 transport at all partial pressures of inspired O 2. Control coefficients were calculated using theoretical modelling of the respiratory system with a haemoglobin P 50 that is typical of highland birds 25 Torr or 3. Expressed as a percentage, the control coefficients for all steps in the pathway will sum to The circulatory delivery of O 2 throughout the body is also enhanced in high-altitude birds.
The most pervasive mechanism for sustaining the circulation of O 2 in hypoxia is an alteration in the O 2 -binding properties of haemoglobin in the blood. Numerous high-altitude birds, such as the bar-headed goose Fig. This can dramatically increase O 2 delivery and pulmonary O 2 loading in hypoxia by increasing the saturation of haemoglobin and thus the O 2 content of the blood at a given O 2 partial pressure Fig. The genetic and structural bases for haemoglobin adaptation to high altitude have been resolved in many species.
Parallel genetic changes can sometimes arise in the haemoglobin of different highland species e. Andean waterfowl McCracken et al.
Highland haemoglobin genotypes can even be maintained when gene flow from low altitudes is high, presumably because they are strongly favoured by natural selection McCracken et al. High-altitude adaptations in the haemoglobin Hb of bar-headed geese. A The O 2 affinity of bar-headed goose Hb is higher than that of lowland waterfowl, as reflected by a leftward shift in the O 2 equilibrium curve of blood measured at a pH of 7. Redrawn from Black and Tenney Black and Tenney, This cartoon was drawn in Pymol from the previously published structure of oxygenated Hb Zhang et al.
The circulation of O 2 may also be sustained in hypoxia by specializations in the heart that safeguard cardiac output. Bar-headed geese have a higher density of capillaries in the left ventricle of the heart Fig.
Cellular function could also be challenged if the production of reactive O 2 species increases at high altitudes, as occurs in some lowland animals when declining O 2 levels at cytochrome c oxidase COX, the enzyme that consumes O 2 in oxidative phosphorylation shift the electron transport chain of mitochondria towards a more reduced state akin to a buildup of electrons Aon et al.
However, COX from bar-headed goose hearts has a higher affinity for its substrate cytochrome c in its reduced state Fig. A possible cause of this difference is a single mutation in subunit 3 of the COX protein, which occurs at a site that is otherwise conserved across vertebrates Trp to Arg green in Fig.
These and likely other unique specializations may explain how bar-headed geese maintain arterial blood pressure and increase cardiac power output to deeper levels of hypoxia than Pekin ducks G. Milsom, unpublished. Cardiac specializations in high-altitude birds may have a transcriptional basis, based on a comparison of cardiac gene expression in late-stage embryos of Tibetan chickens and lowland breeds Li and Zhao, : embryonic hypoxia altered the expression of over 70 transcripts in all chickens, but an additional 12 genes involved in energy metabolism, signal transduction, transcriptional regulation, cell proliferation, contraction and protein folding were differentially expressed in only the highland Tibetan breed.
Overall, these findings lend some credence to a previous suggestion that the hypoxaemia tolerance of the heart has a strong influence on the ability to fly at high altitudes Scheid, Cardiac adaptations to high altitude in bar-headed geese. A Capillary density is enhanced in the hearts left ventricle of bar-headed geese compared with low-altitude geese. Insets are representative images of capillary staining in bar-headed geese left , pink-footed geese centre and barnacle geese right.
Asterisk represents a significant difference from both low-altitude species. Modified from Scott et al. Scott et al. The capacity for O 2 to diffuse from the blood to mitochondria in the flight muscle is also enhanced in high-altitude birds. Because there were no differences in muscle aerobic capacity between coot populations, the increase in O 2 diffusing capacity should serve to improve O 2 transport in hypoxia rather than to match differences in cellular O 2 demands.
Similar differences exist between bar-headed geese and lowland waterfowl from a common environment at sea level Scott et al. Mitochondria are also redistributed closer to capillaries in the aerobic fibres of bar-headed geese Scott et al.
These various mechanisms for improving the diffusion capacity for O 2 in the flight muscle should help sustain mitochondrial O 2 supply when hypoxaemia occurs at high altitudes. In addition to improvements in the capacity to transport O 2 during hypoxia, various features of metabolic O 2 utilization and ATP turnover are altered in the flight muscle of high-altitude birds.
This does not generally include changes in the inherent metabolic capacity of individual muscle fibres, based on observations in bar-headed geese of the abundance and respiratory capacities of mitochondria as well as the activities of metabolic enzymes Scott et al.
However, inherently higher aerobic capacities can exist for the whole muscle by virtue of increases in the proportional abundance of aerobic fibres Scott et al. Furthermore, the metabolic capacity of individual fibres can sometimes Mathieu-Costello et al. Increases in aerobic capacity, and the associated increases in overall mitochondrial abundance, could be important for counterbalancing the inhibitory effects of low O 2 levels on the respiration of individual mitochondria [this strategy is discussed in Hochachka Hochachka, ].
Mitochondrial ATP production is also more strongly regulated by creatine kinase in bar-headed geese than in low-altitude waterfowl Scott et al. A potential consequence of these alterations is that energy supply and demand in the muscle is better coupled via the creatine kinase shuttle, a system important for moving ATP equivalents around the cell [this system is described in Andrienko et al.
Andrienko et al. An interesting possibility is that bar-headed geese developed a more active shuttle to compensate for the redistribution of mitochondria, which moved these organelles closer to capillaries but further from the contractile elements that constitute the major sites of ATP demand in the flight muscle.
It has been suggested that the iconic migration of bar-headed geese, which takes some individuals of this species over the highest peaks in the Himalayas, is impossible without vertical wind assistance Butler, However, it was clearly not an impairment of the cardiorespiratory system at supplying O 2 that impaired running performance in this study, as ventilation and cardiac output were both well below what can be sustained by this species during severe hypoxia at rest Black and Tenney, ; Scott and Milsom, The more parsimonious explanation is that the leg muscles cannot sustain high activity during hypoxaemia, which is not terribly surprising given that this tissue is inactive when bar-headed geese fly at high altitudes.
Nevertheless, the possibility that some of the highest-flying birds depend on wind assistance is intriguing and warrants examination with empirical data. Most birds migrate below m elevation and, when possible, may alter flight altitude to take advantage of favourable wind, temperature, humidity or pressure Liechti et al.
It is unclear to what extent this strategy is employed by high-altitude birds, but some evidence suggests that favourable conditions are not requisite for flying high. For example, demoiselle cranes Anthropoides virgo that were tracked on their southward migration between central and southern Asia flew over the Himalayas at — m elevation into a headwind Kanai et al.
We have found that bar-headed geese climbing the southern Himalayan face actually avoid flying in the afternoons when upslope tailwinds could reduce the metabolic requirements of flight, and prefer instead to fly in the stable and colder conditions overnight and early morning when there is a slight downdraft Hawkes et al.
These data suggest that active flight is indeed possible without wind assistance up to at least m elevation. A definitive answer to whether flapping flight can be sustained above the highest peaks awaits physiological and biomechanical data for birds flying at even higher altitudes. The ability of birds to fly at high altitudes is critically dependent on the effective transport of O 2 from hypoxic air to all of the tissues of the body.
Part of this effectiveness comes from many characteristics that distinguish the O 2 transport pathway of all birds in general from that of other vertebrates. Although not truly adaptive for high-altitude flight, these characteristics were undoubtedly an important basis upon which high-altitude adaptation could proceed.
As it did so, unique specializations appear to have arisen at every step of the O 2 transport pathway of high fliers to facilitate their impressive exercise performance. However, it is not yet certain whether the numerous examples above are sufficient to entirely explain high-altitude flight. One area we know relatively little about is the relative roles of genetic adaptation versus phenotypic plasticity in the ability of birds to fly at high altitudes.
Most of the previous work aimed at revealing the unique attributes of high fliers compared birds in a common environment at sea level. These studies were a useful first step in elucidating inherent and heritable differences, but it is probable that acclimatization to high-altitude hypoxia also shapes the physiology and flight capacity of highland residents Cheviron et al.
This could also be true of elevational migrants that spend time staging higher than their native altitudes before they cross high mountain ranges e. However, not all hypoxia responses are beneficial — some are in fact maladaptive Storz et al. We know less about the uniquely derived specializations for coping with low barometric pressure, cold and dry air than we do about those for coping with hypoxia.
Birds that are adapted to high altitudes have larger wings to help offset the detrimental effects of low air density on lift generation Feinsinger et al. This reduces the power output required to fly at elevation, but it does not completely eliminate the need for highland birds to flap harder i. Scott studies how vertebrates — animals with backbones — perform in physically challenging environments.
According to Scott, birds as small as sparrows and hummingbirds in the Alpine region can be found at altitudes of 16, feet 5, m , while massive Andean condors glide on air currents at heights of 18, feet 5, m.
Mallard ducks are known to reach altitudes of 21, feet 6, m , and Central Asia's bar-headed geese have been directly tracked at 23, feet 7, m. Somehow, these high flyers can exert themselves at exceptional altitudes. But what allows them to navigate the air up there?
While these birds vary in size, they have one thing in common: a longer wingspan relative to their bodies, compared with birds that fly lower. But it takes more than longer wings to navigate high altitudes, which come with enormous physical trials, Scott added. The oxygen levels become more limited. At high altitudes, it gets colder, and they need to keep their bodies warm. And the air gets drier — they're more likely to lose water from breathing and evaporation, and be thirsty.
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