Comments on Point:Counterpoint: High altitude is/is not for the birds!

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POINT:COUNTERPOINT | High altitude is/is not for the birdsHigh altitude is/is not for the birdsComments on Point:Counterpoint: High altitude is/is not for the birds!Published Online:01 Nov 2011https://doi.org/10.1152/japplphysiol.01117.2011MoreSectionsPDF (71 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat FROM THE MOUNTAINS TO THE SEA—HYPOXIA TOLERANCE ACROSS SPECIESDarren P. Casey.Author AffiliationsAssistant Professor of Physiology Mayo Clinic.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).REFERENCES1. Folkow LP , Ramirez JM , Ludvigsen S , Ramirez N , Blix AS. Remarkable neuronal hypoxia tolerance in the deep-diving adult hooded seal (Cystophora cristata). Neurosci Lett 446: 147–150, 2008.Crossref | PubMed | ISI | Google Scholar2. Kanatous SB , Davis RW , Watson R , Polasek L , Williams TM , Mathieu-Costello O. Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations? J Exp Biol 205: 3601–3608, 2002.Crossref | PubMed | ISI | Google Scholar3. Kooyman GL , Ponganis PJ. The physiological basis of diving to depth: birds and mammals. Annu Rev Physiol 60: 19–32, 1998.Crossref | PubMed | ISI | Google Scholar4. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: High Altitude is not for the birds! J Appl Physiol; doi:10.1152.japplphysiol.00821.2011a.ISI | Google Scholar5. Meir JU , Champagne CD , Costa DP , Williams CL , Ponganis PJ. Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am J Physiol Regul Integr Comp Physiol 297: R927–R939, 2009.Link | ISI | Google Scholar6. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: High altitude is/is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google ScholarREFERENCES1. Folkow LP , Ramirez JM , Ludvigsen S , Ramirez N , Blix AS. Remarkable neuronal hypoxia tolerance in the deep-diving adult hooded seal (Cystophora cristata). Neurosci Lett 446: 147–150, 2008.Crossref | PubMed | ISI | Google Scholar2. Kanatous SB , Davis RW , Watson R , Polasek L , Williams TM , Mathieu-Costello O. Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations? J Exp Biol 205: 3601–3608, 2002.Crossref | PubMed | ISI | Google Scholar3. Kooyman GL , Ponganis PJ. The physiological basis of diving to depth: birds and mammals. Annu Rev Physiol 60: 19–32, 1998.Crossref | PubMed | ISI | Google Scholar4. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: High Altitude is not for the birds! J Appl Physiol; doi:10.1152.japplphysiol.00821.2011a.ISI | Google Scholar5. Meir JU , Champagne CD , Costa DP , Williams CL , Ponganis PJ. Extreme hypoxemic tolerance and blood oxygen depletion in diving elephant seals. Am J Physiol Regul Integr Comp Physiol 297: R927–R939, 2009.Link | ISI | Google Scholar6. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: High altitude is/is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google ScholarHIGH ALTITUDE IS/IS NOT FOR THE BIRDS: THE DIFFERENCE IS IN OUR HEADSChristopher H. E. ImrayVascular Surgeon and Mark H. WilsonWarwick Medical School.to the editor: Every March, two Himalayan migrations occur. The bar-headed goose sets off from the lowland plains of India in the early mornings of the pre-monsoon season (median departure 24th March), climbs at 1,100 m/h, reaches altitudes as high as 9,000 m and so crosses the Himalayas all within a day (median 8 h) (3). At the same time of year, Everest climbers set off from Kathmandu to attempt to climb Everest. Most expeditions take 60–80 days and summit attempts are launched from about 8,000 m, also in the early hours of the morning. Ascent rates using supplementary oxygen are typically 150–250 m/h.Although avian heart, lung, muscle, and blood have evolved to allow rapid ascent to altitude, in our opinion, it is the avian cerebral circulation's insensitivity to hypocapnia that is most important (5). Humans have lowland adaptations (such as PaCO2 being a surrogate marker for hypoxia), meaning that they need to acclimatize to high altitude. A human exposed to 8,848 m would become unconscious within 5 min. However after 60 days acclimatization, some mountaineers are able to summit, despite being profoundly hypoxic. Breathing ambient air at 8,400 m mean PaO2 was 3.28 kPa (2) At 7,950 m, mean EtCO2 was 1.73 kPa, yet cerebral oxygen delivery was maintained by a number of processes including cerebral arterial vasodilatation (6).Both birds (bar-headed goose) and mammals (humans) can travel to 8,848 m; the former has evolved to be able to do it in a day, while the latter needs 60 days to acclimatize and there is still an associated attrition rate (1).REFERENCES1. Firth PG , Zheng H , Windsor JS , Sutherland AI , Imray CH , Moore GW , Semple JL , Roach RC , Salisbury RA. Mortality on Mount Everest, 1921 to 2006: descriptive study. BMJ 337: a2654, 2001.Crossref | Google Scholar2. Grocott MP , Martin DS , Levett DZ , McMorrow R , Windsor J , Montgomery HE. Arterial blood gases, and oxygen content in climbers on Mount Everest. N Engl J Med 360: 140–149, 2009.Crossref | PubMed | ISI | Google Scholar3. Hawkes LA , Balachandran S , Batbayar N , Butler PJ , Frappell PB , Milsom WK , Tseveenmyadag N , Newman SH , Scott GH , Sathiyaselvam P , Takekawa JY , Wikelski M , Bishop CM. The trans-Himalayan flights of bar-headed geese (Anser indicus). Proc Natl Acad Sci USA 108: 9516–9519, 2011.Crossref | PubMed | ISI | Google Scholar4. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani JT. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar5. Scott GR , Meir JU , Hawkes LA , Frappell , Milsom WK PB. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar6. Wilson MH , Mark Edsell M , Davagnanam I , Hirani SP , Martin D , Levett DZH , Thornton J , Golay X , Strycharczuk L , Newman S , Montgomery H , Grocott MPW, Imray CHE for the Caudwell Xtreme Everest Research Group. Cerebral artery dilatation maintains cerebral oxygenation at extreme altitude and in acute hypoxia—an ultrasound and MRI study. J Cereb Blood Flow Metab; doi:10.1038/jcbfm.2011.81 (2011 Jun 8) [Epub ahead of print].Crossref | ISI | Google ScholarREFERENCES1. Firth PG , Zheng H , Windsor JS , Sutherland AI , Imray CH , Moore GW , Semple JL , Roach RC , Salisbury RA. Mortality on Mount Everest, 1921 to 2006: descriptive study. BMJ 337: a2654, 2001.Crossref | Google Scholar2. Grocott MP , Martin DS , Levett DZ , McMorrow R , Windsor J , Montgomery HE. Arterial blood gases, and oxygen content in climbers on Mount Everest. N Engl J Med 360: 140–149, 2009.Crossref | PubMed | ISI | Google Scholar3. Hawkes LA , Balachandran S , Batbayar N , Butler PJ , Frappell PB , Milsom WK , Tseveenmyadag N , Newman SH , Scott GH , Sathiyaselvam P , Takekawa JY , Wikelski M , Bishop CM. The trans-Himalayan flights of bar-headed geese (Anser indicus). Proc Natl Acad Sci USA 108: 9516–9519, 2011.Crossref | PubMed | ISI | Google Scholar4. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani JT. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar5. Scott GR , Meir JU , Hawkes LA , Frappell , Milsom WK PB. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar6. Wilson MH , Mark Edsell M , Davagnanam I , Hirani SP , Martin D , Levett DZH , Thornton J , Golay X , Strycharczuk L , Newman S , Montgomery H , Grocott MPW, Imray CHE for the Caudwell Xtreme Everest Research Group. Cerebral artery dilatation maintains cerebral oxygenation at extreme altitude and in acute hypoxia—an ultrasound and MRI study. J Cereb Blood Flow Metab; doi:10.1038/jcbfm.2011.81 (2011 Jun 8) [Epub ahead of print].Crossref | ISI | Google ScholarEVOLUTIONARY ADAPTATION TO HYPOXIC ENVIRONMENTSAndreas D. FlourisSenior Researcher and Andres E. CarrilloFAME Laboratory Institute of Human Performance & Rehabilitation Centre for Research & Technology T.to the editor: That living organisms have an immense capability of adapting to a hypoxic environment was eloquently expressed by both Scott and Llanos and colleagues (3, 5). Based on the presented evidence as well as data that we recently discussed (1), it is our opinion that high altitude is not only for the birds. The biological needs of an animal appear to dictate the type of adaptation to an environment such as hypoxia. For example, differences in oxygen demand between species may provoke functional differences in physiological adaption trajectories. Furthermore, the level of adaptation may depend on multi-generational high-altitude ancestry, as genetic adaptations typically require prolonged periods of time (1). This is important to consider because responses to hypoxia are highly variable within species. As we recently discussed in this Journal (2), prenatal exposure to high altitude generates important vascular adjustments (e.g., increased blood flow in the uterine artery) in humans of multi-generational high-altitude ancestry that are not found in shorter-term residents of highland destinations who often demonstrate reductions in birth weight with increasing altitude (6). Thus depending on ancestry certain organisms may be in the process of adapting to hypoxia while others may have already evolved. In terms of adapting to exercise at high altitude, Tibetans exhibit extraordinary running economy during submaximal exercise compared with acclimated lowlanders (4), while athletes from the Kenyan Kalenjin tribes dominate marathon performance (1). These important considerations support our contention that high altitude is not only for the birds.REFERENCES1. Carrillo AE , Koutedakis Y , Flouris AD. Early life mammalian biology and later life physical performance: maximising physiological adaptation. Br J Sports Med 45: 1000–1001, 2011.Crossref | ISI | Google Scholar2. Flouris AD , Carrillo AE. Influence of early life factors on elite performance. J Appl Physiol 110: 284; discussion 294, 2011.ISI | Google Scholar3. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar4. Marconi C , Marzorati M , Sciuto D , Ferri A , Cerretelli P. Economy of locomotion in high-altitude Tibetan migrants exposed to normoxia. J Physiol 569: 667–675, 2005.Crossref | ISI | Google Scholar5. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar6. Wilson MJ , Lopez M , Vargas M , Julian C , Tellez W , Rodriguez A , Bigham A , Armaza JF , Niermeyer S , Shriver M , Vargas E , Moore LG. Greater uterine artery blood flow during pregnancy in multigenerational (Andean) than shorter-term (European) high-altitude residents. Am J Physiol Regul Integr Comp Physiol 293: R1313–R1324, 2007.Link | ISI | Google ScholarREFERENCES1. Carrillo AE , Koutedakis Y , Flouris AD. Early life mammalian biology and later life physical performance: maximising physiological adaptation. Br J Sports Med 45: 1000–1001, 2011.Crossref | ISI | Google Scholar2. Flouris AD , Carrillo AE. Influence of early life factors on elite performance. J Appl Physiol 110: 284; discussion 294, 2011.ISI | Google Scholar3. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar4. Marconi C , Marzorati M , Sciuto D , Ferri A , Cerretelli P. Economy of locomotion in high-altitude Tibetan migrants exposed to normoxia. J Physiol 569: 667–675, 2005.Crossref | ISI | Google Scholar5. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar6. Wilson MJ , Lopez M , Vargas M , Julian C , Tellez W , Rodriguez A , Bigham A , Armaza JF , Niermeyer S , Shriver M , Vargas E , Moore LG. Greater uterine artery blood flow during pregnancy in multigenerational (Andean) than shorter-term (European) high-altitude residents. Am J Physiol Regul Integr Comp Physiol 293: R1313–R1324, 2007.Link | ISI | Google ScholarDOWN JACKETS AND WOOLLY SWEATERS: HIGH ALTITUDE ISN'T JUST ABOUT HYPOXIAVincent TedjasaputraGraduate Student and Susan R. HopkinsPulmonary Imaging Laboratory University of California, San Diego.to the editor: “Most people are heartless about turtles because a turtle's heart will beat for hours after he has been cut up and butchered.”- Ernest Hemingway (1).Scott et al. and Llanos et al. (3, 4) have elegantly outlined the abilities of bar-headed Geese and llamas to prosper in hypoxic environments. However, if the debate pertains only to the survival of birds compared with the rest of kingdom animalia in hypoxic environments, then the champion would be the freshwater turtle of the Trachemys and Chrysemys genera. Turtles can live in an anoxic environment for several months, a feat unmatched by birds or llamas (5). Also, there are other very hypoxia-tolerant animals to consider: the naked mole rat Heterocephalus glaber, who dwells in hypoxic environments or the bat Pteropus poliocephalus, with very high metabolic scope and excellent hypoxia tolerance (2, 6).Our colleagues have not considered an important environmental factor aside from hypoxia: the cold. Anyone who has worn a down jacket or alpaca sweater knows the effect of insulating coats that protect both birds and llamas. Neither the naked mole rat nor the bat would survive at the altitude where birds and llamas thrive (3, 6). This is probably not because of lack of hypoxia tolerance, but because the mole rat lacks fur, and bat wings (equally furless) are heat exchangers. Thus the bird and llama's survivability at altitude likely relies on tolerance to cold as much as tolerance to hypoxia. To have a complete discussion of success at altitude, all environmental factors should be considered.REFERENCES1. Hemingway E. The Old Man and the Sea. New York: Charles Scribner's Sons, 1952.Google Scholar2. Larson J , Park TJ. Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport 20: 1634–1637, 2009.Crossref | PubMed | ISI | Google Scholar3. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar4. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar5. Storey KB. Anoxia tolerance in turtles: metabolic regulation and gene expression. Comp Biochem Physiol A Physiol 147: 263–276, 2007.Crossref | PubMed | ISI | Google Scholar6. Thomas SP , Follette DB , Thomas GS. Metabolic and ventilatory adjustments and tolerance of the bat Pteropus poliocephalus to acute hypoxic stress. Comp Biochem Physiol A Physiol 112: 43–54, 1995.Crossref | ISI | Google ScholarREFERENCES1. Hemingway E. The Old Man and the Sea. New York: Charles Scribner's Sons, 1952.Google Scholar2. Larson J , Park TJ. Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport 20: 1634–1637, 2009.Crossref | PubMed | ISI | Google Scholar3. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar4. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar5. Storey KB. Anoxia tolerance in turtles: metabolic regulation and gene expression. Comp Biochem Physiol A Physiol 147: 263–276, 2007.Crossref | PubMed | ISI | Google Scholar6. Thomas SP , Follette DB , Thomas GS. Metabolic and ventilatory adjustments and tolerance of the bat Pteropus poliocephalus to acute hypoxic stress. Comp Biochem Physiol A Physiol 112: 43–54, 1995.Crossref | ISI | Google ScholarHIGH ALTITUDE IS MOSTLY ABOUT AEROBIC CAPACITYGeoffrey F. Birchard.Author AffiliationsProfessor George Mason University.to the editor: Whether high altitude is or is not for the birds (vs. mammals) has been placed in an evolutionary context by the authors (2, 3). It is notable that high altitude is generally regarded as about 2,500 m and above so the discussion is actually about extreme high altitude. I will comment on what I feel are two major issues relevant to the evolutionary discussion. First, the term ”avian respiratory system“ is phylogenetically incorrect. This type of respiratory system evolved in the archosaurs, millions of years before birds, and as such does not represent an avian adaptation (1). The second issue is that most, if not all of the adaptations commented on probably do not qualify as traits selected for by a high-altitude environment. The context of supporting an energetically expensive form of locomotion has been ignored. When bats and birds are compared, a number of the differences mentioned are eliminated or markedly reduced [e.g., times to unconsciousness, morphological and physiological parameters related to oxygen delivery (4, 6)]. Furthermore, exercise results in significant modifications in vascular regulation (vascular endothelial nitric oxide system). Exercise-related changes could be at least part of the solution to the issues raised about the mammalian pulmonary and cerebral circulations, and this is supported by the lack of problems in native extreme HA species (2, 5). Considering the above, high altitude in the context of this discussion was likely first for the Pterosaurs and was only claimed by birds and mammals millions of years later.REFERENCES1. Claessens LPAM , O'Connor PM , Unwin DM. Respiratory evolution facilitated the origin of pterosaur flight, and aerial gigantism. PLoS ONE 4: e4497. doi:10.1371/journal.pone.0004497.Crossref | ISI | Google Scholar2. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar3. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar4. Maina JN. The lungs of the flying vertebrates—birds and bats: is their structure optimized for this elite mode of locomotion? In: Principles of Animal Design: The Optimization and Symmorphosis Debate, , Weibel ER , Taylor CR , Bolis L, eds. New York: Cambridge University Press, 1998, p. 177–195.Google Scholar5. McAllister RM , Newcomer SC , Laughlin MH. Vascular nitric oxide: effects of exercise training in animals. Appl Physiol Nutr Metab 33: 173–178, 2008.Crossref | PubMed | ISI | Google Scholar6. Thomas SP , Follette DB , Thomas GS. Metabolic and ventilatory adjustments and tolerance of the bat Pteropus poliocephalus to acute hypoxic stress. Comp Biochem Physiol 112A: 43–54, 1995.Crossref | Google ScholarREFERENCES1. Claessens LPAM , O'Connor PM , Unwin DM. Respiratory evolution facilitated the origin of pterosaur flight, and aerial gigantism. PLoS ONE 4: e4497. doi:10.1371/journal.pone.0004497.Crossref | ISI | Google Scholar2. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar3. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar4. Maina JN. The lungs of the flying vertebrates—birds and bats: is their structure optimized for this elite mode of locomotion? In: Principles of Animal Design: The Optimization and Symmorphosis Debate, , Weibel ER , Taylor CR , Bolis L, eds. New York: Cambridge University Press, 1998, p. 177–195.Google Scholar5. McAllister RM , Newcomer SC , Laughlin MH. Vascular nitric oxide: effects of exercise training in animals. Appl Physiol Nutr Metab 33: 173–178, 2008.Crossref | PubMed | ISI | Google Scholar6. Thomas SP , Follette DB , Thomas GS. Metabolic and ventilatory adjustments and tolerance of the bat Pteropus poliocephalus to acute hypoxic stress. Comp Biochem Physiol 112A: 43–54, 1995.Crossref | Google ScholarVeronique Billat, PhD.Author AffiliationsFaculty of Sport Sciences University Evry, France.to the editor: This Point:Counterpoint about high altitude is/is not for the birds (3, 4) mainly focused on oxygen transport factor of the energy metabolism must also consider the carburant limitation. Bird flight requires high levels of mechanical and metabolic power (1). Migratory birds must adapt the physiology of their flight muscle to cope with a number of requirements, such as use of stored triglycerides as the major fuel, due to its high energy density; provision of additional power to meet higher flight costs, due to increases in body mass; and development of sufficient endurance to fly continuously for 3,000 km (1). At the end, we have to consider that llama are rather selected for their ability to have remarkable wool and are known for developing a number of disturbances related to energy metabolism (2). Some are similar to disorders seen in other species, but most relate to camelids' unusual characteristics of poor glucose tolerance, partial insulin resistance, and low concentrations of circulating insulin (2). So I do agree with Scott et al. (4) who pointed out the ability of several highland species for flying between altitudes of 4,000 and 6,500 m well above the llama's home in the Andean altiplano. However, humans are maybe one of the most efficient mammals in altitude considering their ability for climbing Everest (8,848 m) with V̇o2max declining from an average of 49.0 to 15.3 ml·kg−1·min−1 at the summit (5) thanks to their anaerobic metabolism, which must also be discussed when speaking about exercise in altitude.REFERENCES1. Bishop CM , Butler PJ , Egginton S , el Haj AJ , Gabrielsen GW. Development of metabolic enzyme activity in locomotor and cardiac muscles of the migratory barnacle goose. Am J Physiol Regul Integr Comp Physiol 269: R64–R72, 1995.Link | ISI | Google Scholar2. Cebra CK. Disorders of carbohydrate or lipid metabolism in camelids. Vet Clin North Am Food Anim Pract 25: 339–352, 2009.Crossref | ISI | Google Scholar3. Llanos GR , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar4. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milson WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar5. Wagner P. Operation Everest II. Am J Physiol Regul Integr Comp Physiol 269: R64–R72, 1995.Google ScholarREFERENCES1. Bishop CM , Butler PJ , Egginton S , el Haj AJ , Gabrielsen GW. Development of metabolic enzyme activity in locomotor and cardiac muscles of the migratory barnacle goose. Am J Physiol Regul Integr Comp Physiol 269: R64–R72, 1995.Link | ISI | Google Scholar2. Cebra CK. Disorders of carbohydrate or lipid metabolism in camelids. Vet Clin North Am Food Anim Pract 25: 339–352, 2009.Crossref | ISI | Google Scholar3. Llanos GR , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar4. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milson WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar5. Wagner P. Operation Everest II. Am J Physiol Regul Integr Comp Physiol 269: R64–R72, 1995.Google ScholarAVIAN LUNGS ARE BETTERJohn B. West.Author AffiliationsProfessor UCSD.to the editor: Scott et al. (3) make a compelling case for the superior pulmonary gas exchange in birds compared with mammals (2). Here are some additional points.Birds have separated the gas exchange and ventilatory functions of the lung. What a crazy idea to use delicate alveoli for the process of ventilation when robust air sacs would do. No wonder that breakdown of the alveolar walls as in emphysema is so common in humans. Next the bird uses a flow-through rather than reciprocating form of ventilation that allows the gas exchanging tissue to be exposed to the full Po2 of the inspired air. By contrast in the human, the pulmonary capillaries are exposed to alveolar gas that has already lost about 1/3 of the available Po2. Another disadvantage of the mammalian lung is that the capillaries are strung out along the alveolar wall and are therefore unsupported at right angles to the wall. Contrast this with the situation in the bird parabronchi where the capillaries are supported by surrounding air capillaries (4). The result is that bird capillaries have much thinner walls than in mammals. Furthermore the walls are uniformly thin, unlike the situation in mammals where a type I collagen cable snakes along the alveolar wall and thickens one side of the capillaries. The result is that in humans only half of the area of the blood-gas barrier is available for efficient gas exchange (1). No question about it. Birds have superior lungs and therefore tolerate hypoxia better.REFERENCES1. Gehr P , Bachofen M , Weibel ER. The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. Respir Physiol 32: 121–140, 1978.Crossref | PubMed | Google Scholar2. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar3. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar4. West JB , Fu Z , Deerinck TJ , Mackey MR , Obayashi JT , Ellisman MH. Structure-function studies of blood and air capillaries in chicken lung using 3D electron microscopy. Resp Physiol Neuro 170: 202–209, 2010.Crossref | PubMed | ISI | Google ScholarREFERENCES1. Gehr P , Bachofen M , Weibel ER. The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. Respir Physiol 32: 121–140, 1978.Crossref | PubMed | Google Scholar2. Llanos AJ , Ebensperger G , Herrera EA , Reyes RV , Moraga FA , Parer JT , Giussani DA. Counterpoint: high altitude is not for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011a.ISI | Google Scholar3. Scott GR , Meir JU , Hawkes LA , Frappell PB , Milsom WK. Point: high altitude is for the birds! J Appl Physiol; doi:10.1152/japplphysiol.00821.2011.ISI | Google Scholar4. West JB , Fu Z , Deerinck TJ , Mackey MR , Obayashi JT , Ellisman MH. Structure-function studies of blood and air capillaries in chicken lung using 3D electron microscopy. Resp Physiol Neuro 170: 202–209, 2010.Crossref | PubMed | ISI | Google ScholarPHYSIOLOGICAL ADAPTATIONS AND OPTIMAL CONTROL IN BIRDS WHICH FLY AT HIGH ALTITUDESMary C. VagulaAssistant Professor and Charles NelaturyGannon University.to the editor: In a sense, one could propose that birds are the living solutions of the famous Goddard problem dealing with high altitudes. Many birds on their long distance migration fly at high altitudes, at which some environmental features like oxygen availability, humidity, wind speeds, air temperature, and density have a significant consequence on avian flight performances (1). Authors (3, 4) elegantly elaborated on the adaptations in birds and llamas, respectively, during hypoxia.Compared with other v