Comments on point: counterpoint: high altitude is/is not for the birds!

TO THE EDITOR: The debate between Scott et al. (6) and Llanos et al. (4) highlights the remarkable ability of birds and mammals to adapt and survive at high altitudes and cope with reduced oxygen (O2) availability. Scott and colleagues (6) make a compelling argument that birds are far superior to mammals at adapting and thriving in hypoxic environments, both at rest and during exercise. While their argument is supported by comparisons between birds and terrestrial mammals, it ignores marine mammals. Marine mammals such as seals are routinely exposed to and tolerate long bouts of hypoxia during breath-hold diving. For example, elephant seals may dive to depths of nearly 1,600 m and occasionally remain submerged for 2 h (3). Moreover, marine mammals can be exposed to partial pressures of arterial oxygen (PaO2) as low as 12 mmHg during free dives (5), which is less than the 20 mmHg observed in the bar-headed goose (6). Interestingly, a PaO2 of 12 mmHg observed in elephant seals corresponds to arterial saturations and O2 content of only 8% and 2.7 ml O2/dl (5). Thus marine mammals such as the elephant seal demonstrate a remarkable hypoxia tolerance. The integration of several key physiological adaptations including 1) substantially greater myoglobin concentrations compared to other mammals, 2) reductions in metabolism, 3) a greater reliance on aerobic metabolism (i.e., less lactate production), 4) a host of dramatic acute cardiovascular adjustments; and 5) an increased intrinsic cerebral hypoxia tolerance allow marine mammals to thrive in hypoxic environments and enable long deep dives (1–3).

[1]  G. Moore,et al.  Mortality on Mount Everest, 1921-2006: descriptive study , 2008, BMJ : British Medical Journal.

[2]  A. Valenzuela,et al.  High altitude induced pulmonary hypertension and right heart failure in broiler chickens. , 1974, Research in veterinary science.

[3]  H. Gunga,et al.  Our ancestral physiological phenotype: an adaptation for hypoxia tolerance and for endurance performance? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  G. Dawes,et al.  The importance of cardiac glycogen for the maintenance of life in foetal lambs and new‐born animals during anoxia , 1959, The Journal of physiology.

[5]  Mason R. Mackey,et al.  Structure–function studies of blood and air capillaries in chicken lung using 3D electron microscopy , 2010, Respiratory Physiology & Neurobiology.

[6]  Megan J. Wilson,et al.  Greater uterine artery blood flow during pregnancy in multigenerational (Andean) than shorter-term (European) high-altitude residents. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[7]  K. Storey Anoxia tolerance in turtles: metabolic regulation and gene expression. , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[8]  Cassondra L. Williams,et al.  Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. , 2009, American journal of physiology. Regulatory, integrative and comparative physiology.

[9]  F. Léon-Velarde,et al.  Hemoglobin affinity and structure in high-altitude and sea-level carnivores from Peru. , 1996, Comparative biochemistry and physiology. Part A, Physiology.

[10]  M. Laughlin,et al.  Vascular nitric oxide: effects of exercise training in animals. , 2008, Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme.

[11]  J. Ramirez,et al.  Remarkable neuronal hypoxia tolerance in the deep-diving adult hooded seal (Cystophora cristata) , 2008, Neuroscience Letters.

[12]  J. Parer,et al.  Counterpoint: high altitude is not for the birds! , 2011, Journal of applied physiology.

[13]  D. Wharton Cold tolerance of New Zealand alpine insects. , 2011, Journal of insect physiology.

[14]  Charles M. Bishop,et al.  The trans-Himalayan flights of bar-headed geese (Anser indicus) , 2011, Proceedings of the National Academy of Sciences.

[15]  C. Bauer,et al.  Causes of high blood O2 affinity of animals living at high altitude. , 1977, Journal of applied physiology: respiratory, environmental and exercise physiology.

[16]  J. Meir,et al.  Point: high altitude is for the birds! , 2011, Journal of applied physiology.

[17]  P. Lutz,et al.  Anoxia Tolerant Brains , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  J. West,et al.  Major differences in the pulmonary circulation between birds and mammals , 2007, Respiratory Physiology & Neurobiology.

[19]  G. R. Ultsch,et al.  Physiology of hibernation under the ice by turtles and frogs. , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[20]  G. Scott Elevated performance: the unique physiology of birds that fly at high altitudes , 2011, Journal of Experimental Biology.

[21]  W. Milsom,et al.  Peripheral arterial chemoreceptors and the evolution of the carotid body , 2007, Respiratory Physiology & Neurobiology.

[22]  S. Egginton,et al.  Molecular evolution of cytochrome C oxidase underlies high-altitude adaptation in the bar-headed goose. , 2011, Molecular biology and evolution.

[23]  Thomas J. Park,et al.  Extreme hypoxia tolerance of naked mole-rat brain , 2009, Neuroreport.

[24]  Sudhir Kumar,et al.  Continental breakup and the ordinal diversification of birds and mammals , 1996, Nature.

[25]  A. Flouris,et al.  Early life mammalian biology and later life physical performance: maximising physiological adaptation , 2011, British Journal of Sports Medicine.

[26]  E R Weibel,et al.  The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. , 1978, Respiration physiology.

[27]  Charles M. Bishop,et al.  Development of metabolic enzyme activity in locomotor and cardiac muscles of the migratory barnacle goose. , 1995, The American journal of physiology.

[28]  S. Thomas,et al.  Metabolic and ventilatory adjustments and tolerance of the bat Pteropus poliocephalus to acute hypoxic stress. , 1995, Comparative biochemistry and physiology. Part A, Physiology.

[29]  C. Cebra Disorders of carbohydrate or lipid metabolism in camelids. , 2009, The Veterinary clinics of North America. Food animal practice.

[30]  R. Dudley,et al.  The physiology and biomechanics of avian flight at high altitude. , 2006, Integrative and comparative biology.

[31]  David M. Unwin,et al.  Respiratory Evolution Facilitated the Origin of Pterosaur Flight and Aerial Gigantism , 2009, PloS one.

[32]  I. Johnston,et al.  Effects of acclimation temperature on routine metabolism muscle mitrochondrial volume density and capillary supply in the elver (Anguilla anguilla L.) , 1984 .

[33]  J. Meir,et al.  Last word on point:counterpoint: high altitude is/is not for the birds! , 2011, Journal of applied physiology.

[34]  T. Williams,et al.  Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations? , 2002, The Journal of experimental biology.

[35]  Robert Boyle,et al.  New Pneumatical Experiments about Respiration , 1999 .

[36]  M. Grocott,et al.  Arterial blood gases and oxygen content in climbers on Mount Everest. , 2009, The New England journal of medicine.

[37]  Xavier Golay,et al.  Cerebral artery dilatation maintains cerebral oxygenation at extreme altitude and in acute hypoxia—an ultrasound and MRI study , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[38]  P. Ponganis,et al.  The physiological basis of diving to depth: birds and mammals. , 1998, Annual review of physiology.

[39]  P. Cerretelli,et al.  Economy of locomotion in high‐altitude Tibetan migrants exposed to normoxia , 2005, The Journal of physiology.