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

Experientia volume 48, pages 565–570 (1992)Cite this article

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.

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References

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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. 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. 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. 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.

    PubMed  Google Scholar 

  7. Davis, R. A., and Fraenkel, G., The oxygen consumption of flies during flight. J. exp. Biol.17 (1940) 402–407.

    Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  9. Drummond, G. I., Microenvironment and enzyme function: control of energy metabolism during muscle work. Am. Zool.11 (1971) 83–97.

    Google Scholar 

  10. Dubach, M., Quantitative analysis of the respiratory system of the house sparrow, budgerigar and violet-eared hummingbird. Respir. Physiol.46 (1981) 43–60.

    Article  PubMed  Google Scholar 

  11. Emmett, B., and Hochachka, P. W., Scaling of oxidative and glycolytic enzymes in mammals. Respir. Physiol.45 (1981) 261–272.

    Article  PubMed  Google Scholar 

  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. Greenewalt, C. H., Hummingbirds. Doubleday, New York 1960.

    Google Scholar 

  14. Grunyer, I., and George, J. C., Some observations on the ultrastructure of the hummingbird pectoral muscles. Can. J. Zool.47 (1969) 771–774.

    PubMed  Google Scholar 

  15. Hainsworth, F. R., Energy regulation in hummingbirds. Am. Sci.69 (1981) 420–429.

    PubMed  Google Scholar 

  16. Hartman, F. A., Locomotor mechanisms of birds. Smithson. Inst. misc. Collect.143 (1961) 1–91.

    Google Scholar 

  17. Hochachka, P. W., Fuels and pathways as designed systems for muscle work. J. exp. Biol.115 (1985) 149–164.

    Google Scholar 

  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. 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. 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. Hochachka, P. W., and Somero, G. N., Strategies of Biochemical Adaptation. Saunders, Philadelphia 1973.

    Google Scholar 

  22. Hoppeler, H., and Lindstedt, S. L., Malleability of skeletal muscle in overcoming limitations: structural elements. J. exp. Biol.115 (1985) 355–364.

    PubMed  Google Scholar 

  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. 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. 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. Krebs, J. R., and Harvey, P. H., Busy doing nothing — efficiently. Nature320 (1986) 18–19.

    Article  Google Scholar 

  27. Lasiewski, R. C., The energetics of migrating hummingbirds. Condor64 (1962) 324.

    Google Scholar 

  28. Lasiewski, R. C., Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiol. Zool.36 (1963) 122–140.

    Google Scholar 

  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. Lasiewski, R. C., Galey, F. R., and Vasquez, C., Morphology and physiology of the pectoral muscles of hummingbirds. Nature206 (1965) 404–405.

    PubMed  Google Scholar 

  31. Mainwood, G. W., and Rakusan, K., A model for intracellular energy transport. Can. J. Physiol. Pharmac.60 (1982) 98–102.

    Google Scholar 

  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.

    PubMed  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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. 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. 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. Ramadoss, C. S., Luby, L. J., and Uyeda, K., Affinity chromatography of phosphofructokinase. Archs Biochem. Biophys.175 (1976) 487–494.

    Article  Google Scholar 

  39. Schmidt-Nielsen, K., Scaling. Why is Animal Size So Important? Cambridge Univ. Press, Cambridge 1984.

    Google Scholar 

  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.

    PubMed  Google Scholar 

  41. Smith, D. S., The structure of flight muscle sarcosomes in the blowflyCalliphora erythrocephala (Diptera). J. Cell Biol.19 (1963) 114–138.

    Article  Google Scholar 

  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. Suarez, R. K., Oxygen and VO2max: are muscle mitochondria created equal? Proc. 7th Int. Hypoxia Symp. (1992) in press.

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  48. Taylor, C. R., Structural and functional limits to oxidative metabolism: insights from scaling. A. Rev. Physiol.49 (1987) 135–146.

    Article  Google Scholar 

  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. Weibel, E. R., Design and performance of muscular systems: an overview. J. exp. Biol.115 (1985) 405–412.

    PubMed  Google Scholar 

  51. Weis-Fogh, T., Energetics of hovering flight in hummingbirds and inDrosophila. J. exp. Biol.56 (1972) 79–104.

    Google Scholar 

  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.

    PubMed  Google Scholar 

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Author notes

  1. R. K. Suarez

    Present address: Dept. of Zoology, University of British Columbia, V6T 2A9, Vancouver, B.C., Canada

Authors and Affiliations

  1. Department of Biological Sciences, Simon Fraser University, V5A 1S6, Burnaby, B.C., Canada

    R. K. Suarez

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Suarez, R.K. Hummingbird flight: Sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48, 565–570 (1992). https://doi.org/10.1007/BF01920240

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  • DOI: https://doi.org/10.1007/BF01920240

Key words

  • Oxygen consumption
  • exercise
  • evolutionary design
  • muscle
  • mitochondria
  • energy metabolism
  • enzymes