Phylogenetic and Growth Form Variation in the Scaling of Nitrogen and Phosphorus in the Seed Plants

Andrew J. Kerkhoff, William F. Fagan, James J. Elser and Brian J. Enquist
The American Naturalist
Vol. 168, No. 4 (October 2006), pp. E103-E122
DOI: 10.1086/507879
Stable URL:
Page Count: 20
  • Download PDF
  • Cite this Item

You are not currently logged in.

Access your personal account or get JSTOR access through your library or other institution:


Log in to your personal account or through your institution.

Phylogenetic and Growth Form Variation in the Scaling of Nitrogen and Phosphorus in the Seed Plants
We're having trouble loading this content. Download PDF instead.


Abstract: Plant biomass and nutrient allocation explicitly links the evolved strategies of plant species to the material and energy cycles of ecosystems. Allocation of nitrogen (N) and phosphorus (P) is of particular interest because N and P play pivotal roles in many aspects of plant biology, and their availability frequently limits plant growth. Here we present a comparative scaling analysis of a global data compilation detailing the N and P contents of leaves, stems, roots, and reproductive structures of 1,287 species in 152 seed plant families. We find that P and N contents (as well as N:P) are generally highly correlated both within and across organs and that differences exist between woody and herbaceous taxa. Between plant organs, the quantitative form of the scaling relationship changes systematically, depending on whether the organs considered are primarily structural (i.e., stems, roots) or metabolically active (i.e., leaves, reproductive structures). While we find significant phylogenetic signals in the data, similar scaling relationships occur in independently evolving plant lineages, which implies that both the contingencies of evolutionary history and some degree of environmental convergence have led to a common set of rules that constrain the partitioning of nutrients among plant organs.

Notes and References

This item contains 92 references.

Literature Cited
  • ['Ackerly, D. D. 2000. Taxon sampling, correlated evolution, and independent contrasts. Evolution 54:1480–1492.']
  • ['———. 2004a. Adaptation, niche conservatism, and convergence: comparative studies of leaf evolution in the California chaparral. American Naturalist 163:654–671.']
  • ['———. 2004b. Analysis of traits (AOT) manual. Version 3.0. A module of Phylocom.']
  • ['Ackerly, D. D., and M. J. Donoghue. 1998. Leaf size, sapling allometry, and Corner’s rules: phylogeny and correlated evolution in maples (Acer). American Naturalist 152:767–791.']
  • ['Ackerly, D. D., and P. B. Reich. 1999. Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. American Journal of Botany 86:1272–1281.']
  • ['Aerts, R., and F. S. Chapin. 2000. The mineral nutrition of wild plants revisited: a re‐evaluation of processes and patterns. Advances in Ecological Research 30:1–67.']
  • ['Ågren, G. I. 1988. Ideal nutrient productivities and nutrient proportions in plant growth. Plant Cell and Environment 11:613–620.']
  • ['———. 2004. The C:N:P stoichiometry of autotrophs: theory and observations. Ecology Letters 7:185–191.']
  • ['Ågren, G. I., and E. Bosatta. 1996. Theoretical ecosystem ecology: understanding nutrient cycles. Cambridge University Press, Cambridge.']
  • ['APG II (Angiosperm Phylogeny Group). 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141:399–436.']
  • ['Bazzaz, F. A., and J. Grace. 1997. Plant resource allocation. Academic Press, San Diego, CA.']
  • ['Blomberg, S. P., and T. Garland. 2002. Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. Journal of Evolutionary Biology 15:899–910.']
  • ['Bowman, W. D., L. Bahnj, and M. Damm. 2003. Alpine landscape variation in foliar nitrogen and phosphorus concentrations and the relation to soil nitrogen and phosphorus availability. Arctic Antarctic and Alpine Research 35:144–149.']
  • ['Broadley, M. R., H. C. Bowen, H. L. Cotterill, J. P. Hammond, M. C. Meacham, A. Mead, and P. J. White. 2004. Phylogenetic variation in the shoot mineral concentration of angiosperms. Journal of Experimental Botany 55:321–336.']
  • ['Cavender‐Bares, J., D. D. Ackerly, D. A. Baum, and F. A. Bazzaz. 2004. Phylogenetic overdispersion in Floridian oak communities. American Naturalist 163:823–843.']
  • ['Cebrian, J. 1999. Patterns in the fate of production in plant communities. American Naturalist 154:449–468.']
  • ['Chapin, F. S. 2003. Effects of plant traits on ecosystem and regional processes: a conceptual framework for predicting the consequences of global change. Annals of Botany 91:455–463.']
  • ['Chapin, F. S., P. M. Vitousek, and K. Vancleve. 1986. The nature of nutrient limitation in plant communities. American Naturalist 127:48–58.']
  • ['Chapin, F. S., B. H. Walker, R. J. Hobbs, D. U. Hooper, J. H. Lawton, O. E. Sala, and D. Tilman. 1997. Biotic control over the functioning of ecosystems. Science 277:500–504.']
  • ['Corner, E. J. H. 1949. The Durian theory or the origin of the modern tree. Annals of Botany 13:367–414.']
  • ['Cowling, S. A. 2001. Plant carbon balance evolutionary innovation and extinction in land plants. Global Change Biology 7:231–239.']
  • ['Craine, J. M., W. G. Lee, W. J. Bond, R. J. Williams, and L. C. Johnson. 2005. Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology 86:12–19.']
  • ['Davies, T. J., T. G. Barraclough, M. W. Chase, P. S. Soltis, D. E. Soltis, and V. Savolainen. 2004. Darwin’s abominable mystery: insights from a supertree of the angiosperms. Proceedings of the National Academy of Sciences of the USA 101:1904–1909.']
  • ['De Angelis, D. L. 1980. Energy‐flow, nutrient cycling, and ecosystem resilience. Ecology 61:764–771.']
  • ['Diaz, S., J. G. Hodgson, K. Thompson, M. Cabido, J. H. C. Cornelissen, A. Jalili, G. Montserrat‐Marti, et al. 2004. The plant traits that drive ecosystems: evidence from three continents. Journal of Vegetation Science 15:295–304.']
  • ['Diaz‐Uriarte, R., and T. Garland. 1998. Effects of branch length errors on the performance of phylogenetically independent contrasts. Systematic Biology 47:654–672.']
  • ['Duarte, C. M. 1992. Nutrient concentration of aquatic plants: patterns across species. Limnology and Oceanography 37:882–889.']
  • ['Duarte, C. M., K. Sand‐Jensen, S. L. Nielsen, S. Enriquez, and S. Agusti. 1995. Comparative functional plant ecology: rationale and potentials. Trends in Ecology & Evolution 10:418–421.']
  • ['Elser, J. J., R. W. Sterner, E. Gorokhova, W. F. Fagan, T. A. Markow, J. B. Cotner, J. F. Harrison, S. Hobbie, G. Odell, and L. J. Weider. 2000a. Biological stoichiometry from genes to ecosystems. Ecology Letters 3:540–550.']
  • ['Elser, J. J., W. F. Fagan, R. F. Denno, D. R. Dobberfuhl, A. Folarin, A. Huberty, S. Interlandi, et al. 2000b. Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580.']
  • ['Enquist, B. J., and K. J. Niklas. 2002. Global allocation rules for patterns of biomass partitioning in seed plants. Science 295:1517–1520.']
  • ['Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1–15.']
  • ['Field, C., and H. A. Mooney. 1986. The photosynthesis‐nitrogen relationship in wild plants. Pages 25–55 in T. J. Givnish, ed. On the economy of plant form and function. Cambridge University Press, Cambridge.']
  • ['Foley, J. A., I. C. Prentice, N. Ramankutty, S. Levis, D. Pollard, S. Sitch, and A. Haxeltine. 1996. An integrated biosphere model of land surface processes, terrestrial carbon balance, and vegetation dynamics. Global Biogeochemical Cycles 10:603–628.']
  • ['Friedlingstein, P., G. Joel, C. B. Field, and I. Y. Fung. 1999. Toward an allocation scheme for global terrestrial carbon models. Global Change Biology 5:755–770.']
  • ['Garland, T., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:18–32.']
  • ['Garten, C. T. 1976. Correlations between concentrations of elements in plants. Nature 261:686–688.']
  • ['Gingerich, P. D. 2000. Arithmetic or geometric normality of biological variation: an empirical test of theory. Journal of Theoretical Biology 204:201–221.']
  • ['Grime, J. P. 1979. Plant strategies and vegetation processes. Wiley, Chichester.']
  • ['Güsewell, S. 2004. N:P ratios in terrestrial plants: variation and functional significance. New Phytologist 164:243–266.']
  • ['Güsewell, S., and M. Koerselman. 2002. Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology Evolution and Systematics 5:37–61.']
  • ['Hirose, T., and M. J. A. Werger. 1994. Photosynthetic capacity and nitrogen partitioning among species in the canopy of a herbaceous plant community. Oecologia (Berlin) 100:203–212.']
  • ['Hobbie, S. E., and L. Gough. 2002. Foliar and soil nutrients in tundra on glacial landscapes of contrasting ages in northern Alaska. Oecologia (Berlin) 131:453–462.']
  • ['Jackson, R. B., H. A. Mooney, and E. D. Schulze. 1997. A global budget for fine root biomass surface area and nutrient contents. Proceedings of the National Academy of Sciences of the USA 94:7362–7366.']
  • ['Kay, A. D., I. W. Ashton, E. Gorokhova, A. J. Kerkhoff, A. Liess, and E. Litchman. 2005. Toward a stoichiometric framework for evolutionary biology. Oikos 109:6–17.']
  • ['Kerkhoff, A. J., B. J. Enquist, J. J. Elser, and W. F. Fagan. 2005. Plant allometry, stoichiometry and the temperature‐dependence of primary productivity. Global Ecology and Biogeography 14:585–598.']
  • ['Kleidon, A., and H. A. Mooney. 2000. A global distribution of biodiversity inferred from climatic constraints: results from a process‐based modelling study. Global Change Biology 6:507–523.']
  • ['Knops, J. M. H., and W. D. Koenig. 1997. Site fertility and leaf nutrients of sympatric evergreen and deciduous species of Quercus in central coastal California. Plant Ecology 130:121–131.']
  • ['Koerselman, W., and A. F. M. Meuleman. 1996. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33:1441–1450.']
  • ['Lavorel, S., and E. Garnier. 2002. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Functional Ecology 16:545–556.']
  • ['Lisanti, L. E., C. Testini, and M. Polemio. 1971. Nitrogen‐phosphorus interaction in plants. Agrochimica 16:53–61.']
  • ['Marschner, H., E. A. Kirkby, and C. Engels. 1997. Importance of cycling and recycling of mineral nutrients within plants for growth and development. Botanica Acta 110:265–273.']
  • ['Mattson, W. J. 1980. Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11:119–161.']
  • ['McGroddy, M. E., T. Daufresne, and L. O. Hedin. 2004. Scaling of C:N:P stoichiometry in forest ecosystems worldwide: implications of terrestrial Redfield‐type ratios. Ecology 85:2390–2401.']
  • ['McJannet, C. L., P. A. Keddy, and F. R. Pick. 1995. Nitrogen and phosphorus tissue concentrations in 41 wetland plants: a comparison across habitats and functional groups. Functional Ecology 9:231–238.']
  • ['Melillo, J. M., J. D. Aber, and J. F. Muratore. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626.']
  • ['Milberg, P., and B. B. Lamont. 1997. Seed/cotyledon size and nutrient content play a major role in early performance of species on nutrient‐poor soils. New Phytologist 137:665–672.']
  • ['Moorcroft, P. R. 2003. Recent advances in ecosystem‐atmosphere interactions: an ecological perspective. Proceedings of the Royal Society B: Biological Sciences 270:1215–1227.']
  • ['Moorcroft, P. R., G. C. Hurtt, and S. W. Pacala. 2001. A method for scaling vegetation dynamics: the ecosystem demography model (ED). Ecological Monographs 71:557–585.']
  • ['Nielsen, S. L., S. Enriquez, C. M. Duarte, and K. Sand‐Jensen. 1996. Scaling maximum growth rates across photosynthetic organisms. Functional Ecology 10:167–175.']
  • ['Niklas, K. J. 1994. Plant allometry: the scaling of form and process. University of Chicago Press, Chicago.']
  • ['Niklas, K. J., T. Owens, P. B. Reich, and E. D. Cobb. 2005. Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecology Letters 8:636–642.']
  • ['Norby, R. J. 1998. Nitrogen deposition: a component of global change analyses. New Phytologist 139:189–200.']
  • ['Olff, H. 1992. Effects of light and nutrient availability on dry‐matter and N‐allocation in 6 successional grassland species: testing for resource ratio effects. Oecologia (Berlin) 89:412–421.']
  • ['Pagel, M. D. 1992. A method for the analysis of comparative data. Journal of Theoretical Biology 156:431–442.']
  • ['Pinheiro, J. C., and D. M. Bates. 2000. Mixed effects models in S and S‐PLUS: statistics and computing. Springer, New York.']
  • ['Preston, K. A., and D. D. Ackerly. 2004. The evolution of allometry in modular organisms. Pages 80–106 in M. Pigliucci and K. A. Preston, eds. Phenotypic integration: studying ecology and evolution of complex phenotypes. Oxford University Press, Oxford.']
  • ['Reich, P. B., and J. Oleksyn. 2004. Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences of the USA 101:11001–11006.']
  • ['Reich, P. B., M. B. Walters, and D. S. Ellsworth. 1997. From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences of the USA 94:13730–13734.']
  • ['Reich, P. B., D. S. Ellsworth, M. B. Walters, J. M. Vose, C. Gresham, J. C. Volin, and W. D. Bowman. 1999. Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969.']
  • ['Reich, P. B., D. Tilman, S. Naeem, D. S. Ellsworth, J. Knops, J. Craine, D. Wedin, and J. Trost. 2004. Species and functional group diversity independently influence biomass accumulation and its response to CO2 and N. Proceedings of the National Academy of Sciences of the USA 101:10101–10106.']
  • ['Schieving, F., T. L. Pons, M. J. A. Werger, and T. Hirose. 1992. The vertical distribution of nitrogen and photosynthetic activity at different plant densities in Carex acutiformis. Plant and Soil 142:9–17.']
  • ['Schimel, D. S., T. G. F. Kittel, A. K. Knapp, T. R. Seastedt, W. J. Parton, and V. B. Brown. 1991. Physiological interactions along resource gradients in a tallgrass prairie. Ecology 72:672–684.']
  • ['Silver, W. L. 1994. Is nutrient availability related to plant nutrient use in humid tropical forests? Oecologia (Berlin) 98:336–343.']
  • ['Sokal, R. R., and F. J. Rohlf. 1995. Biometry: the principles and practice of statistics in biological research. W. H. Freeman, New York.']
  • ['Sterner, R. W., and J. J. Elser. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, NJ.']
  • ['Suding, K. N., S. L. Collins, L. Gough, C. Clark, E. E. Cleland, K. L. Gross, D. G. Milchunas, and S. Pennings. 2005. Functional‐ and abundance‐based mechanisms explain diversity loss due to N fertilization. Proceedings of the National Academy of Sciences of the USA 102:4387–4392, doi:10.1073/pnas.0408648102.']
  • ['Thompson, K., J. A. Parkinson, S. R. Band, and R. E. Spencer. 1997. A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytologist 136:679–689.']
  • ['Tilman, D. 1988. Plant strategies and the dynamics and structure of plant communities. Monographs in Population Biology. Vol. 26. Princeton University Press, Princeton, NJ.']
  • ['Vitousek, P. 1982. Nutrient cycling and nutrient use efficiency. American Naturalist 119:553–572.']
  • ['———. 1998. Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems 1:401–407.']
  • ['Vogt, K. A., C. C. Grier, and D. J. Vogt. 1986. Production, turnover, and nutrient dynamics of aboveground and belowground detritus of world forests. Advances in Ecological Research 15:303–377.']
  • ['Warton, D. I., and N. C. Weber. 2002. Common slope tests for bivariate errors‐in‐variables models. Biometrical Journal 44:161–174.']
  • ['Webb, C. O., and M. J. Donoghue. 2005. Phylomatic: tree assembly for applied phylogenetics. Molecular Ecology Notes 5:181–183.']
  • ['Webb, C. O., D. D. Ackerly, and S. W. Kembel. 2005. Phylocom: software for the analysis of community phylogenetic structure and character evolution. Version 3.34.']
  • ['Wedin, D., and D. Tilman. 1993. Competition among grasses along a nitrogen gradient: initial conditions and mechanisms of competition. Ecological Monographs 63:199–229.']
  • ['Weiher, E., A. Van der Werf, K. Thompson, M. Roderick, E. Garnier, and O. Eriksson. 1999. Challenging Theophrastus: a common core list of plant traits for functional ecology. Journal of Vegetation Science 10:609–620.']
  • ['Westoby, M., D. S. Falster, A. T. Moles, P. A. Vesk, and I. J. Wright. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33:125–159.']
  • ['Wikstrom, N., V. Savolainen, and M. W. Chase. 2001. Evolution of the angiosperms: calibrating the family tree. Proceedings of the Royal Society B: Biological Sciences 268:2211–2220.']
  • ['Woodwell, G. M., R. H. Whittaker, and R. A. Houghton. 1975. Nutrient concentrations in plants in Brookhaven oak‐pine forest. Ecology 56:318–332.']
  • ['Wright, I. J., P. B. Reich, and M. Westoby. 2001. Strategy shifts in leaf physiology, structure and nutrient content between species of high‐ and low‐rainfall and high‐ and low‐nutrient habitats. Functional Ecology 15:423–434.']
  • ['Wright, I. J., P. B. Reich, M. Westoby, D. D. Ackerly, Z. Baruch, F. Bongers, J. Cavender‐Bares, et al. 2004. The worldwide leaf economics spectrum. Nature 428:821–827.']