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Universal scaling of respiratory metabolism, size and nitrogen in plants

Nature volume 439, pages 457–461 (2006)Cite this article

A Corrigendum to this article was published on 15 June 2006

Abstract

The scaling of respiratory metabolism to body size in animals is considered to be a fundamental law of nature1,2,3,4,5,6,7,8,9,10,11, and there is substantial evidence for an approximate -power relation. Studies suggest that plant respiratory metabolism also scales as the -power of mass12,13,14, and that higher plant and animal scaling follow similar rules owing to the predominance of fractal-like transport networks and associated allometric scaling8,9,10,11,12,13,14. Here, however, using data obtained from about 500 laboratory and field-grown plants from 43 species and four experiments, we show that whole-plant respiration rate scales approximately isometrically (scaling exponent ≈ 1) with total plant mass in individual experiments and has no common relation across all data. Moreover, consistent with theories about biochemically based physiological scaling15,16,17,18, isometric scaling of whole-plant respiration rate to total nitrogen content is observed within and across all data sets, with a single relation common to all data. This isometric scaling is unaffected by growth conditions including variation in light, nitrogen availability, temperature and atmospheric CO2 concentration, and is similar within or among species or functional groups. These findings suggest that plants and animals follow different metabolic scaling relations, driven by distinct mechanisms.

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Figure 1: Scaling of respiration, N and plant mass for plants.

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References

  1. Kleiber, M. Body size and metabolism. Hilgardia 6, 315–353 (1932)

    Article  CAS  Google Scholar 

  2. Peters, R. H. The Ecological Implications of Body Size (Cambridge Univ. Press, Cambridge, MA, 1983)

    Book  Google Scholar 

  3. Calder, W. A. Size, Function, and Life History (Harvard Univ. Press, Cambridge, MA, 1984)

    Google Scholar 

  4. Savage, V. M. et al. The predominance of quarter-power scaling in biology. Funct. Ecol. 18, 257–282 (2004)

    Article  Google Scholar 

  5. Riisgard, H. U. No foundation of a '¾ power scaling law' for respiration in biology. Ecol. Lett. 1, 71–73 (1998)

    Article  Google Scholar 

  6. Dodds, P. S., Rothman, D. H. & Weitz, J. S. Re-examination of the ¾-law of metabolism. J. Theor. Biol. 209, 9–27 (2001)

    Article  CAS  Google Scholar 

  7. White, C. R. & Seymour, R. S. Mammalian basal metabolic rate is proportional to body mass. Proc. Natl Acad. Sci. USA 100, 4046–4049 (2003)

    Article  ADS  CAS  Google Scholar 

  8. West, G. B., Brown, J. H. & Enquist, B. J. A general model for the origin of allometric scaling laws in biology. Science 276, 122–126 (1997)

    Article  CAS  Google Scholar 

  9. West, G. B., Brown, J. H. & Enquist, B. J. The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284, 1677–1679 (1999)

    Article  ADS  MathSciNet  CAS  Google Scholar 

  10. Banavar, J. R., Maritan, A. & Rinaldo, A. Size and form in efficient transportation networks. Nature 399, 130–134 (1999)

    Article  ADS  CAS  Google Scholar 

  11. Banavar, J. R., Damuth, J., Maritan, A. & Rinaldo, A. Supply–demand balance and metabolic scaling. Proc. Natl Acad. Sci. USA 99, 10506–10509 (2002)

    Article  ADS  CAS  Google Scholar 

  12. West, G. B., Brown, J. H. & Enquist, B. J. A general model for the structure, and allometry of plant vascular systems. Nature 400, 664–667 (1999)

    Article  ADS  CAS  Google Scholar 

  13. Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001)

    Article  ADS  CAS  Google Scholar 

  14. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004)

    Article  Google Scholar 

  15. Atkin, O. K. & Tjoelker, M. G. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci. 8, 343–351 (2003)

    Article  CAS  Google Scholar 

  16. Ryan, M. G. Foliar maintenance respiration of subalpine and boreal trees and shrubs in relation to nitrogen content. Plant Cell Environ. 18, 765–772 (1995)

    Article  CAS  Google Scholar 

  17. Reich, P. B. et al. Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia 114, 471–482 (1998)

    Article  ADS  Google Scholar 

  18. Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004)

    Article  ADS  CAS  Google Scholar 

  19. Kozlowski, J. & Konarzewski, M. Is West, Brown and Enquists model of allometric scaling mathematically correct and mathematically relevant? Funct. Ecol. 18, 283–289 (2004)

    Article  Google Scholar 

  20. Enquist, B. J., Brown, J. H. & West, G. B. Allometric scaling of plant energetics and population density. Nature 395, 163–166 (1998)

    Article  ADS  CAS  Google Scholar 

  21. Reich, P. B. Body size, geometry, longevity and metabolism: do plant leaves behave like animal bodies? Trends Ecol. Evol. 16, 674–680 (2001)

    Article  Google Scholar 

  22. Enquist, B. J. Universal scaling in tree and vascular plant allometry: towards a general quantitative theory linking plant form and function from cells to ecosystems. Tree Phys. 22, 1045–1064 (2002)

    Article  Google Scholar 

  23. Enquist, B. J. & Niklas, K. J. Global allocation rules for biomass partitioning in seed plants. Science 295, 1517–1520 (2002)

    Article  ADS  CAS  Google Scholar 

  24. Niklas, K. J. & Enquist, B. J. On the vegetative biomass partitioning of seed plant leaves, stems, and roots. Am. Nat. 159, 482–497 (2002)

    Article  Google Scholar 

  25. Niklas, K. J. & Enquist, B. J. Invariant scaling relationships for interspecific plant biomass production rates and body size. Proc. Natl Acad. Sci. USA 98, 2922–2927 (2001)

    Article  ADS  CAS  Google Scholar 

  26. Enquist, B. J. et al. Scaling metabolism from organisms to ecosystems. Nature 423, 639–642 (2003)

    Article  ADS  CAS  Google Scholar 

  27. Yokota, T., Ogawa, K. & Hagihara, A. Dependence of the above-ground respiration of hinoki cypress (Chamaecyparis obtusa) on tree size. Tree Physiol. 14, 467–479 (1994)

    Article  CAS  Google Scholar 

  28. Yokota, T. & Hagihara, A. Changes in the relationship between tree size and aboveground respiration in field-grown hinoki cypress (Chamaecyparis obtusa) trees over three years. Tree Physiol. 18, 37–43 (1998)

    Article  Google Scholar 

  29. Meinzer, F. C., Bond, B. J., Warren, J. M. & Woodruff, D. R. Does water transport scale universally with tree size? Funct. Ecol. 19, 558–565 (2005)

    Article  Google Scholar 

  30. McCulloh, K. A. & Sperry, J. S. Patterns in hydraulic architecture and their implications for transport efficiency. Tree Physiol. 25, 257–267 (2005)

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Wilderness Research Foundation and the National Science Foundation Long-Term Ecological Research Program for major support of the research reported herein and the Gordon Conference ‘Metabolic Basis of Ecology’ for inspiring us in this endeavour. Author Contributions The idea behind this paper was developed by P.B.R. and J.-L.M. while attending the Gordon Conference Metabolic Basis of Ecology. P.B.R. did the statistical analyses and wrote the paper with considerable assistance from M.G.T. All authors interpreted the results, commented on the manuscript and were involved in the design and implementation of one or more of the individual studies that collectively make up this paper (P.B.R., four studies; M.G.T., three; J.-L.M., two; J.O., one).

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Authors and Affiliations

  1. Department of Forest Resources, University of Minnesota, Minnesota, 55108, St Paul, USA

    Peter B. Reich

  2. Department of Forest Science, Texas A&M University, Texas, 77843, College Station, USA

    Mark G. Tjoelker

  3. Department of Biology, Swarthmore College, Pennsylvania, 19081, Swarthmore, USA

    Jose-Luis Machado

  4. Polish Academy of Sciences, Institute of Dendrology, PL-62-035, Kornik, Poland

    Jacek Oleksyn

Authors
  1. Peter B. Reich
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  3. Jose-Luis Machado
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  4. Jacek Oleksyn
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Correspondence to Peter B. Reich.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Methods

This file includes the details of the environmental conditions, plant species, and ages for each of the four studies making up the manuscript. It includes all measurement and handling details for the four studies. This file covers data analyses and how adjusted values were calculated and also contains additional references. (DOC 41 kb)

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Reich, P., Tjoelker, M., Machado, JL. et al. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439, 457–461 (2006). https://doi.org/10.1038/nature04282

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