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A comparative meta-analysis of maximal aerobic metabolism of vertebrates: implications for respiratory and cardiovascular limits to gas exchange

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Abstract

Maximal aerobic metabolic rates (MMR) in vertebrates are supported by increased conductive and diffusive fluxes of O2 from the environment to the mitochondria necessitating concomitant increases in CO2 efflux. A question that has received much attention has been which step, respiratory or cardiovascular, provides the principal rate limitation to gas flux at MMR? Limitation analyses have principally focused on O2 fluxes, though the excess capacity of the lung for O2 ventilation and diffusion remains unexplained except as a safety factor. Analyses of MMR normally rely upon allometry and temperature to define these factors, but cannot account for much of the variation and often have narrow phylogenetic breadth. The unique aspect of our comparative approach was to use an interclass meta-analysis to examine cardio-respiratory variables during the increase from resting metabolic rate to MMR among vertebrates from fish to mammals, independent of allometry and phylogeny. Common patterns at MMR indicate universal principles governing O2 and CO2 transport in vertebrate cardiovascular and respiratory systems, despite the varied modes of activities (swimming, running, flying), different cardio-respiratory architecture, and vastly different rates of metabolism (endothermy vs. ectothermy). Our meta-analysis supports previous studies indicating a cardiovascular limit to maximal O2 transport and also implicates a respiratory system limit to maximal CO2 efflux, especially in ectotherms. Thus, natural selection would operate on the respiratory system to enhance maximal CO2 excretion and the cardiovascular system to enhance maximal O2 uptake. This provides a possible evolutionary explanation for the conundrum of why the respiratory system appears functionally over-designed from an O2 perspective, a unique insight from previous work focused solely on O2 fluxes. The results suggest a common gas transport blueprint, or Bauplan, in the vertebrate clade.

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Acknowledgments

We thank G. Brodowicz, L. Crawshaw, B. Buckley, P. Withers and J. Podrabsky for fruitful discussions about the data, and S. Katz for a preliminary review of the manuscript. We also thank the reviewers for thoughtful, provocative input that strengthened the clarity of the manuscript. We gratefully acknowledge funding from the National Science Foundation (IOS-0843082).

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Authors and Affiliations

  1. Department of Biology, Portland State University, Portland, OR, 97207, USA

    Stanley S. Hillman

  2. Department of Biology, Eastern Washington University, Cheney, WA, 99004, USA

    Thomas V. Hancock

  3. Department of Biological Sciences, University of North Texas, Denton, TX, 76203, USA

    Michael S. Hedrick

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  1. Stanley S. Hillman
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  2. Thomas V. Hancock
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  3. Michael S. Hedrick
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Correspondence to Michael S. Hedrick.

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Communicated by I.D. Hume.

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Hillman, S.S., Hancock, T.V. & Hedrick, M.S. A comparative meta-analysis of maximal aerobic metabolism of vertebrates: implications for respiratory and cardiovascular limits to gas exchange. J Comp Physiol B 183, 167–179 (2013). https://doi.org/10.1007/s00360-012-0688-1

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