Journal of Comparative Physiology B

, Volume 158, Issue 4, pp 469–477 | Cite as

Oxygen binding properties, capillary densities and heart weights in high altitude camelids

  • Klaus D. Jürgens
  • Manfred Pietschmann
  • Kazuhiro Yamaguchi
  • Traute Kleinschmidt
Article

Summary

The oxygen binding properties of the blood of the camelid species vicuna, llama, alpaca and dromedary camel were measured and evaluated with respect to interspecific differences. The highest blood oxygen affinity, not only among camelids but of all mammals investigated so far, was found in the vicuna (P50=17.6 Torr compared to 20.3–21.6 Torr in the other species). Low hematocrits (23–34%) and small red blood cells (21–30 μm3) are common features of all camelids, but the lowest values are found in theLama species. Capillary densities were determined in heart and soleus muscle of vicuna and llama. Again, the vicuna shows exceptional values (3720 cap/mm2 on average in the heart) for a mammal of this body size. Finally, heart weight as percent of body weight is higher in the vicuna (0.7–0.9%) than in the other camelids studied (0.5–0.7%). The possibility that these parameters, measured in New World tylopodes at sea level, are not likely to change considerably with transfer to high altitude, is discussed.

In the vicuna, a unique combination of the following features seems to be responsible for an out-standing physical capability at high altitude: saturation of blood with oxygen in the lung is favored by a high blood oxygen affinity, oxygen supply being facilitated by low diffusion distances in the muscle tissue. Loading, as well as unloading, of oxygen is improved by a relatively high oxygen transfer conductance of the red blood cells, which is due to their small size and which compensates the negative effect of a low hematocrit on the oxygen conductance of blood. Blood oxygen transport is presumably favored by two factors: a relatively large heart mass and, as a result of low hematocrit, a low blood viscosity. Both are advantageous for achieving a high maximal cardiac output.

Keywords

High Altitude Soleus Muscle Blood Viscosity Capillary Density Heart Weight 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andersen P, Kroese AJ (1978) Capillary supply in soleus and gastrocnemius muscles of man. Pflügers Arch 375:245–249Google Scholar
  2. Banchero N, Grover RT (1972) Effect of different levels of simulated altitude on O2-transport in llama and sheep. Am J Physiol 222:1239–1245Google Scholar
  3. Banchero N, Grover RT, Will JA (1971a) Oxygen transport in the llama (Lama glama). Respir Physiol 13:102–115Google Scholar
  4. Banchero N, Grover RT, Will JA (1971 b) High altitude-induced pulmonary arterial hypertension in the llama (Lama glama). Am J Physiol 220:245–249Google Scholar
  5. bartels H, Hilpert P, Barbey K, Betke K, Riegel K, Lang EM, Metcalfe J (1963) Respiratory functions of blood of the yak, llama, camel, Dybowski deer, and African elephant. Am J Physiol 205:331–336Google Scholar
  6. Bauer C, Rollema HS, Till HW, Braunitzer G (1980) Phosphate binding by llama and camel hemoglobin. J Comp Physiol 136:67–70Google Scholar
  7. Braunitzer G, Schrank B, Stangl A, Bauer C (1978) Hämoglobine XXII. Phosphat/Protein-Wechselwirkung und die Atmung des Lamas, des menschlichen Fötus und die des Pferdes. Hoppe-Seyler's Z Physiol Chem 359:547–558Google Scholar
  8. Braunitzer G, Schrank B, Stangl A, Wiesner H (1979) Höhenatmung, Phosphat-Proteinwechselwirkung: Die Sequenz der Hämoglobine des Meerschweinschens (Cavidae) und des Dromedars (Camelus dromedarius). Hoppe-Seyler's Z Physiol Chem 360:1941–1946Google Scholar
  9. Chiodi H (1970/71) Comparative study of the blood gas transport in high altitude and sea level camelidae and goats. Respir Physiol 11:84–93Google Scholar
  10. Conley KE, Kayar SR, Rösler K, Hoppeler H, Weibel ER, Taylor CR (1987) Adaptive variation in the mammalian respiratory system in relation to energy demand: IV. Capillaries and their relationship to oxidative capacity. Respir Physiol 69:47–64Google Scholar
  11. Ericson A, Verdier CH de (1972) A modified method for the determination of 2,3-diphosphoglycerate in erythrocytes. Scand J Clin Lab Invest 29:85–90Google Scholar
  12. Hall FG, Dill DB, Guzman-Barron ES (1936) Comparative physiology in high altitudes. J Cell Comp Physiol 8:301–313Google Scholar
  13. Herre W (1982) Zur Stammesgeschichte der Tylopoden. Verh Dtsch Zool Ges 159–171Google Scholar
  14. Herre W, Röhrs M (1973) Haustiere — Zoologisch gesehen. Fischer, StuttgartGoogle Scholar
  15. Hochachka PW, Mommsen TP, Jones JH, Taylor CR (1987) Substrate and O2 fluxes during rest and exercise in a high-altitude adapted animal, the llama. Am J Physiol 253:R298-R305Google Scholar
  16. Hultgren HN, Miller H (1967) Human heart weight at high altitude. Circulation 35:207–218Google Scholar
  17. Hurtado A (1964) Animals in high altitudes: resident man. In: Dill DB (ed) Handbook of physiology. American Physiological Society, Washington DC, pp 843–860Google Scholar
  18. Jürgens KD, Bartels H, Bartels R (1981) Blood oxygen transport and organ weights of small bats and small non-flying mammals. Respir Physiol 45:243–260Google Scholar
  19. Kayar SR, Banchero N (1985) Myocardial capillarity in acclimation to hypoxia. Pflügers Arch 404:319–325Google Scholar
  20. Kleihauer E, Betke K (1957) Zur Hämoglobinbestimmung mittels Cyanhämoglobin nach Betke und Savelsberg. Ärztl Lab 3:202–205Google Scholar
  21. Kleinschmidt T, März J, Jürgens KD, Braunitzer G (1986) The primary structure of two tylopoda hemoglobins with high oxygen affinity: Vicuna (Lama vicugna) and alpaca (Lama pacos). Biol Chem Hoppe-Seyler 367:153–160Google Scholar
  22. Meyer M (1982) Analyse des alveolär-kapillären Gasaustausches in der Lunge. Funktionsanal Biol Syst 9:1–162Google Scholar
  23. Miller P, Banchero N (1971) Hematology of the resting llama. Acta Physiol Lat Am 21:81–86Google Scholar
  24. Pietschmann M, Bartels H, Fons R (1982) Capillary supply of heart and skeletal muscle of small bats and non-flying mammals. Respir Physiol 50:267–282Google Scholar
  25. Prothero J (1979) Heart weight as a function of body weight in mammals. Growth 43:139–150Google Scholar
  26. Rakusan K (1971) Quantitative morphology of capillaries of the heart. In: Bajusz E, Jasmin G (eds) Methods and achievements in experimental pathology 5. Karger, basel, pp 272–286Google Scholar
  27. Rakusan K, Turek Z, Kreuzer F (1981) Myocardial capillaries in guinea pigs native to high altitude (Junin, Peru, 4105 m). Pflügers Arch 391:22–24Google Scholar
  28. Recavarren S, Arias-Stella J (1964) Righ ventricular hypertrophy in people born and living at high altitudes. Br Heart J 26:806–812Google Scholar
  29. Riegel KH, Bartels H, El-Yassin D, Oufi J, Kleihauer E, Parer JT, Metcalfe J (1967) Studies on the respiratory function of mammalian blood. III Fetal and adult dromedary camel blood. Respir Physiol 2:173–181Google Scholar
  30. Sillau AH, Cueva S, Valenzuela A, Candela E (1976) O2 transport in the alpaca (Lama pacos) at sea level and at 3300 m. Respir Physiol 27:147–155Google Scholar
  31. Sillau AH, Aquin L, Bui MV, Banchero N (1980) Chronic hypoxia does not affect guinea pig skeletal muscle capillarity. Pflügers Arch 386:39–45Google Scholar
  32. Stone HO, Thompson HK, Schmidt-Nielsen K (1968) Influence of erythrocytes on blood viscosity. Am J Physiol 214:913–918Google Scholar
  33. Taylor CR (1987) Structural and functional limits to oxidative metabolism: Insights from scaling. Annu Rev Physiol 49:135–146Google Scholar
  34. Wagner PD, Gale GE, Moon RE, Torre-Bueno JR, Stolp BW, Saltzman HA (1986) Pulmonary gas exchange in humans exercising at sea level and simulated altitude. J Appl Physiol 61:260–270Google Scholar
  35. Wearn JT (1928) The extent of the capillary bed of the heart. J Exp Med 47:273Google Scholar
  36. Whittembury J, Lozano R, Torres C, Monge C (1968) Blood viscosity in high altitude polycythemia. Acta Physiol Lat Am 18:353–359Google Scholar
  37. Winslow RM, Monge CC, Statham NJ, Gibson CG, Charache S, Whittembury J, Moran O, Berger RL (1981) Variability of oxygen affinity of blood: human subjects native to high altitude. J Appl Physiol 51:1411–1416Google Scholar
  38. Yamaguchi K, Jürgens KD, Bartels H, Piiper J (1986) Oxygen transfer properties and dimensions of red blood cells in high altitude camelids, dromedary camel and goat. J Comp Physiol B 157:1–9Google Scholar
  39. Zak R (1974) Development and proliferative capacity of cardiac muscle cells. Circ Res [Suppl II] 34/35:II17-II26Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • Klaus D. Jürgens
    • 1
  • Manfred Pietschmann
    • 1
  • Kazuhiro Yamaguchi
    • 2
  • Traute Kleinschmidt
    • 3
  1. 1.Zentrum PhysiologieMedizinische Hochschule HannoverHannover 61Federal Republic of Germany
  2. 2.School of MedicineKeio UniversityTokyoJapan
  3. 3.Abteilung ProteinchemieMax-Planck-Institut für BiochemieMartinsriedFederal Republic of Germany

Personalised recommendations