Experientia

, Volume 48, Issue 6, pp 565–570 | Cite as

Hummingbird flight: Sustaining the highest mass-specific metabolic rates among vertebrates

  • R. K. Suarez
Multi-author Review Ecological Implications of Metabolic Biochemistry

Abstract

Resting and maximal mass-specific metabolic rates scale inversely with body mass. Small hummingbirds achieve the highest known mass-specific metabolic rates among vertebrate homeotherms. Maximal capacities for O2 and substrate delivery to muscle mitochondria, as well as mitochondrial oxidative capacities in these animals may be at the upper limits of what are structurally and functionally possible given the constraints inherent in vertebrate design. Such constraints on the evolutionary design of functional capacities may play an important role in determining the lower limits to vertebrate homeotherm size and the upper limits to mass-specific metabolic rate.

Key words

Oxygen consumption exercise evolutionary design muscle mitochondria energy metabolism enzymes 

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References

  1. 1.
    Alp, P. R., Newsholme, E. A., and Zammit, V. A., Activities of citrate synthase and NAD+-linked isocitrate dehydrogenase in muscle from vertebrates and invertebrates. Biochem. J.154 (1976) 689–700.PubMedGoogle Scholar
  2. 2.
    Bartholomew, G. A., and Lighton, J. R. B., Oxygen consumption during hover-feeding in free-ranging Anna hummingbirds. J. exp. Biol.123 (1986) 191–199.PubMedGoogle Scholar
  3. 3.
    Berger, M., Sauerstoffverbrauch von Kolibris (Colibri coruscans undC. thalassinus) beim Horizontalflug, in: BIONA Report 3, pp. 307–314. Ed. W. Nachtigall. Akad. Wiss. Mainz G. Fischer, Stuttgart and New York 1985.Google Scholar
  4. 4.
    Carpenter, F. L., Paton, D. C., and Hixon, M. A., Weight gain and adjustment of feeding territory size in migrant hummingbirds. Proc. natl Acad. Sci. USA80 (1983) 7259–7263.Google Scholar
  5. 5.
    Casey, T. M., and Ellington, C. P., Energetics of insect flight, in: Energy Transformations in Cells and Organisms, pp. 200–210. Eds W. Wieser and E. Gnaiger. Georg Thieme Verlag, Stuttgart and New York 1990.Google Scholar
  6. 6.
    Conley, K. E., Christian, K. A., Hoppeler, H., and Weibel, E. R., Capillary and mitochondrial unit in muscles of a large lizard. Am. J Physiol.256 (1989) R982-R989.PubMedGoogle Scholar
  7. 7.
    Davis, R. A., and Fraenkel, G., The oxygen consumption of flies during flight. J. exp. Biol.17 (1940) 402–407.Google Scholar
  8. 8.
    Diamond, J. M., Karasov, W. H., Phan, D., and Carpenter, F. L., Digestive physiology is a determinant of foraging bout frequency in hummingbirds. Nature320 (1986) 62–63.CrossRefPubMedGoogle Scholar
  9. 9.
    Drummond, G. I., Microenvironment and enzyme function: control of energy metabolism during muscle work. Am. Zool.11 (1971) 83–97.Google Scholar
  10. 10.
    Dubach, M., Quantitative analysis of the respiratory system of the house sparrow, budgerigar and violet-eared hummingbird. Respir. Physiol.46 (1981) 43–60.CrossRefPubMedGoogle Scholar
  11. 11.
    Emmett, B., and Hochachka, P. W., Scaling of oxidative and glycolytic enzymes in mammals. Respir. Physiol.45 (1981) 261–272.CrossRefPubMedGoogle Scholar
  12. 12.
    Epting, R. J., Functional dependence of the power for hovering on wing disc loading in hummingbirds. Physiol. Zool.53 (1980) 347–352.Google Scholar
  13. 13.
    Greenewalt, C. H., Hummingbirds. Doubleday, New York 1960.Google Scholar
  14. 14.
    Grunyer, I., and George, J. C., Some observations on the ultrastructure of the hummingbird pectoral muscles. Can. J. Zool.47 (1969) 771–774.PubMedGoogle Scholar
  15. 15.
    Hainsworth, F. R., Energy regulation in hummingbirds. Am. Sci.69 (1981) 420–429.PubMedGoogle Scholar
  16. 16.
    Hartman, F. A., Locomotor mechanisms of birds. Smithson. Inst. misc. Collect.143 (1961) 1–91.Google Scholar
  17. 17.
    Hochachka, P. W., Fuels and pathways as designed systems for muscle work. J. exp. Biol.115 (1985) 149–164.Google Scholar
  18. 18.
    Hochachka, P. W., Limits: How fast and how slow muscle metabolism can go, in: Advances in Myochemistry vol. 1, pp. 3–12. Ed. G. Benzi. John Libbey, Eurotext 1987.Google Scholar
  19. 19.
    Hochachka, P. W., Emmett, B., and Suarez, R. K., Limits and constraints in the scaling of oxidative and glycolytic enzymes in homeotherms. Can. J. Zool.66 (1988) 1128–1138.Google Scholar
  20. 20.
    Hochachka, P. W., Neely, J. R., and Driedzic, W. R., Integration of lipid utilization with Krebs cycle activity in muscle. Fedn Proc.36 (1977) 2009–2014.Google Scholar
  21. 21.
    Hochachka, P. W., and Somero, G. N., Strategies of Biochemical Adaptation. Saunders, Philadelphia 1973.Google Scholar
  22. 22.
    Hoppeler, H., and Lindstedt, S. L., Malleability of skeletal muscle in overcoming limitations: structural elements. J. exp. Biol.115 (1985) 355–364.PubMedGoogle Scholar
  23. 23.
    Johansen, K., The world as a laboratory: physiological insights from Nature's experiments, in: Advances in Physiological Research, pp. 377–396. Eds H. McLennan, J. R. Ledsome, C. H. S. McIntosh and D. R. Jones. Plenum Press, New York 1987.Google Scholar
  24. 24.
    Johansen, K., Berger, M., Bicudo, J. E. P. W., Ruschi, A., and De Almeida, P. J., Respiratory properties of blood and myoglobin in hummingbirds. Physiol. Zool.60 (1987) 269–278.Google Scholar
  25. 25.
    Karasov, W. H., Phan, D., Diamond, J. M., and Carpenter, F. L., Food passage and intestinal nutrient absorption in hummingbirds. Auk103 (1986) 453–464.Google Scholar
  26. 26.
    Krebs, J. R., and Harvey, P. H., Busy doing nothing — efficiently. Nature320 (1986) 18–19.CrossRefGoogle Scholar
  27. 27.
    Lasiewski, R. C., The energetics of migrating hummingbirds. Condor64 (1962) 324.Google Scholar
  28. 28.
    Lasiewski, R. C., Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiol. Zool.36 (1963) 122–140.Google Scholar
  29. 29.
    Lasiewski, R. C., Body temperatures, heart and breathing rate, and evaporative water loss in hummingbirds. Physiol. Zool.37 (1964) 212–223.Google Scholar
  30. 30.
    Lasiewski, R. C., Galey, F. R., and Vasquez, C., Morphology and physiology of the pectoral muscles of hummingbirds. Nature206 (1965) 404–405.PubMedGoogle Scholar
  31. 31.
    Mainwood, G. W., and Rakusan, K., A model for intracellular energy transport. Can. J. Physiol. Pharmac.60 (1982) 98–102.Google Scholar
  32. 32.
    Mansour, T. E., Wakid, N., and Sprouse, H. M., Studies on heart phosphofructokinase. Purification, crystallization, and properties of sheep heart phosphofructokinase. J. biol. Chem.241 (1966) 1512–1521.PubMedGoogle Scholar
  33. 33.
    Martinez del Rio, C., Dietary, phylogenetic, and ecological correlates of intestinal sucrase and maltase activity in birds. Physiol. Zool.63 (1990) 987–1011.Google Scholar
  34. 34.
    Newsholme, E. A., and Crabtree, B., Maximum catalytic activity of some key enzymes in provision of physiologically useful information about metabolic fluxes. J. exp. Zool.239 (1986) 159–167.CrossRefPubMedGoogle Scholar
  35. 35.
    Odum, E. P., Connell, C. E., and Stoddard, H. L., Flight energy and estimated flight ranges of some migratory birds. Auk78 (1961) 515–527.Google Scholar
  36. 36.
    Pennycuick, C. J., and Rezende, M. A., The specific power output of aerobic muscle, related to the power density of mitochondria. J. exp. Biol.108 (1984) 377–392.Google Scholar
  37. 37.
    Powers, D. R., and Nagy, K. A., Field metabolic rate and food consumption by free-living Anna's hummingbirds (Calypte anna). Physiol. Zool.61 (1988) 500–506.Google Scholar
  38. 38.
    Ramadoss, C. S., Luby, L. J., and Uyeda, K., Affinity chromatography of phosphofructokinase. Archs Biochem. Biophys.175 (1976) 487–494.CrossRefGoogle Scholar
  39. 39.
    Schmidt-Nielsen, K., Scaling. Why is Animal Size So Important? Cambridge Univ. Press, Cambridge 1984.Google Scholar
  40. 40.
    Schwerzmann, K., Hoppeler, H., Kayar, S. R., and Weibel, E. R., Oxidative capacity of muscle and mitochondria: correlation of physiological biochemical and morphometric characteristics. Proc. natl Acad. Sci. USA86 (1989) 1583–1587.PubMedGoogle Scholar
  41. 41.
    Smith, D. S., The structure of flight muscle sarcosomes in the blowflyCalliphora erythrocephala (Diptera). J. Cell Biol.19 (1963) 114–138.CrossRefGoogle Scholar
  42. 42.
    Srere, P. A., Organisation of proteins within the mitochondrion, in: Organized Multienzyme Systems. Catalytic Properties, pp. 1–61. Ed. G. Rickey Welch, Academic Press, New York and London 1985.Google Scholar
  43. 43.
    Suarez, R. K., Oxygen and VO2max: are muscle mitochondria created equal? Proc. 7th Int. Hypoxia Symp. (1992) in press.Google Scholar
  44. 44.
    Suarez, R. K., Brown, G. S. and Hochachka, P. W., Metabolic sources of energy for hummingbird flight. Am. J. Physiol.251 (1986) R537-R542.PubMedGoogle Scholar
  45. 45.
    Suarez, R. K., Brownsey, R. W., Vogl, W., Brown, G. S. and Hochachka, P. W., Biosynthetic capacity of hummingbird liver. Am. J. Physiol.255 (1988) R699-R702.PubMedGoogle Scholar
  46. 46.
    Suarez, R. K., Lighton, J. R. B., Brown, G. S., and Mathieu-Costello, O., Mitochondrial respiration in hummingbird flight muscles. Proc. natl Acad. Sci. USA88 (1991) 4870–4873.PubMedGoogle Scholar
  47. 47.
    Suarez, R. K., Lighton, J. R. B., Moyes, C. D., Brown, G. S., Gass, C. L., and Hochachka, P. W., Fuel selection in hummingbirds: ecological implications of metabolic biochemistry. Proc. Natl Acad. Sci. USA87 (1990) 9207–9210.PubMedGoogle Scholar
  48. 48.
    Taylor, C. R., Structural and functional limits to oxidative metabolism: insights from scaling. A. Rev. Physiol.49 (1987) 135–146.CrossRefGoogle Scholar
  49. 49.
    Taylor, C. R., Maloiy, G. M. O., Weibel, E. R., Langman, V. A., Kamai, J. M. Z., Seeherman, H. J., and Heglund, N. C., Design of the mammalian respiratory system. III. Scaling maximum aerobic capacity to body mass: wild and domestic animals. Respir. Physiol.44 (1980) 25–37.Google Scholar
  50. 50.
    Weibel, E. R., Design and performance of muscular systems: an overview. J. exp. Biol.115 (1985) 405–412.PubMedGoogle Scholar
  51. 51.
    Weis-Fogh, T., Energetics of hovering flight in hummingbirds and inDrosophila. J. exp. Biol.56 (1972) 79–104.Google Scholar
  52. 52.
    Woeltje, K. F., Kuwajima, M., Foster, D. W., and McGarry, J. D., Characterization of the mitochondrial carnitine palmitoyltransferase enzyme system. II. Use of detergents and antibodies. J. biol. Chem.262 (1987) 9822–9827.PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag 1992

Authors and Affiliations

  • R. K. Suarez
    • 1
  1. 1.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  2. 2.Dept. of ZoologyUniversity of British ColumbiaVancouverCanada

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