Carbon/nitrogen/phosphorus allometric relations across species

  • Karl J. Niklas
Part of the Plant Ecophysiology book series (KLEC, volume 7)

This chapter reviews some of the ecological and evolutionary implications of carbon (C), nitrogen (N), and phosphorus (P) stoichiometry and the allometric relationships among these elements reported for terrestrial plant species because the patterns of C mass allocation and N:P-stoichiometry for different plant organ-types are of general interest to understanding a broad range of ecological and evolutionary phenomena (Aerts and Chapin 2000; Bazzaz and Grace 1997; Chapin et al. 1986; Grime 1979; Niklas and Enquist 2001, 2002; Westoby et al. 2002; Wright et al. 2004; Niklas et al. 2005, 2007; Kerkhoff et al. 2006). Much of the functional-trait variation observed among species differing in overall size can be attributed to differences in the amount of C, N or P allocated to the construction of leaves, stems, roots, and reproductive structures as well as to differences in overall body size (Grime 1979; Field and Mooney 1986; Tilman 1988; Bazzaz and Grace 1997; Jackson et al. 1997; Milberg and Lamont 1997; Weiher et al. 1999; Niklas and Enquist 2001, 2002; Enquist and Niklas 2002; Westoby et al. 2002; Wright et al. 2004; Niklas et al. 2005, 2007; Kerkhoff et al. 2006). Likewise, the P and N concentrations in plant tissues critically influence the material and energy cycles of whole ecosystems (Chapin et al. 1997; De Angelis 1980; Kerkhoff et al. 2005; Koerselman and Meuleman 1996; Silver 1994; Sterner and Elser 2002; Vitousek 1982; Vogt et al. 1986; Ågren and Bosatta 1996) and phylogenetic functional trait differences in the ability to acquire and use N or P are temperature-dependent, such that climatic shifts of sufficient magnitude (e.g., along latitudinal or altitudinal gradients) can have major affects on the C economy of terrestrial vegetation (Kerkhoff et al. 2005; Wright et al. 2005; Westoby and Wright 2006).


Ordinary Little Square Relative Growth Rate Total Leaf Unicellular Alga Total Body Mass 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84: 597–608Google Scholar
  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30: 1–67Google Scholar
  3. Ågren GI (1988) Ideal nutrient productivities and nutrient proportions in plant growth. Plant Cell Environ 11: 613–620Google Scholar
  4. Ågren GI (2004) The C:N:P stoichiometry of autotrophs - theory and observations. Ecol Lett 7: 185–191Google Scholar
  5. Ågren GI, Bosatta E (1996) Theoretical Ecosystem Ecology: Understanding Nutrient Cycles. Cambridge University Press, CambridgeGoogle Scholar
  6. Anten NPR, Schieving F, Werger MJA (1995) Patterns of light and nitrogen distribution in relation to whole canopy carbon gain in C-3 and C-4 monocotyledonous and dicotyledonous species. Oecologia 101: 504–513Google Scholar
  7. Anten NPR, Hikosaka K, Hirose T (2000) Nitrogen utilisation and the photosynthetic system. In: Marshall B, Roberts JA (eds), Leaf Development and Canopy Growth. Sheffield Academic Press, Sheffield, pp 171–203Google Scholar
  8. Banse K (1976) Rates of growth, respiration and photosynthesis of unicellular algae as related to cell size - a review. J Phycol 12: 135–140Google Scholar
  9. Bazzaz FA, Grace J (1997) Plant Resource Allocation. Academic, San Diego, CAGoogle Scholar
  10. Blaxter KL (ed) (1965) Proceedings of the 3rd Symposium on Energy Metabolism. Troon, Scotland, May 1964. Academic, New YorkGoogle Scholar
  11. Blum JJ (1977) On the geometry of four-dimensions and the relationship between metabolism and body mass. J Theor Biol 64: 599–601PubMedGoogle Scholar
  12. Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2004) Phylogenetic variation in the shoot mineral concentration of angiosperms. J Exp Bot 55: 321–336PubMedGoogle Scholar
  13. Brown RH (1978) A difference in N use efficiency in C3 and C4 plants and its implications in adaptation and evolution. Crop Sci 18: 93–98Google Scholar
  14. Calder WA III (1984) Size, Function, and Life History. Harvard University Press, Cambridge, MAGoogle Scholar
  15. Calder WA III (1996) Size, Function, and Life History. Dover, New YorkGoogle Scholar
  16. Campana T, Schwartz LM (1981) Section 9. RNA and associated enzymes. In: Schwartz LM, Azar MM (eds), Advanced Cell Biology. Van Nostrand Reinhold, New York, pp 877–944Google Scholar
  17. Cebrian J (1999) Patterns in the fate of production in plant communities. Am Nat 154: 449–468PubMedGoogle Scholar
  18. Chapin FS, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64: 376–391Google Scholar
  19. Chapin FS, Vitousek PM, Vancleve K (1986) The nature of nutrient limitation in plant-communities. Am Nat 127: 48–58Google Scholar
  20. Chapin FS, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277: 500–504Google Scholar
  21. Darveau CA, Suarez RK, Andrews RD, Hochachka PW (2002) Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417: 166–170PubMedGoogle Scholar
  22. De Angelis DL (1980) Energy-flow, nutrient cycling, and ecosystem resilience. Ecology 61: 764–771Google Scholar
  23. Dobberfuhl DR (1999) Elemental Stoichiometry in Crustacean Zooplankton: Phylogenetic Patterns, Physiological Mechanisms, and Ecological Consequences. Dissertation, Arizona State University, Tempe, ArizonaGoogle Scholar
  24. Dodds, PS, Rothman DH, Weitz JS (2001) Re-examination of the “3/4 - law” of metabolism. J Theor Biol 209: 9–27PubMedGoogle Scholar
  25. Economos AE (1982) On the origin of biological similarity. J Theor Biol 94: 25–60Google Scholar
  26. Economos AE (1983) Elastic and/or geometric similarity in mammalian design. J Theor Biol 103: 167–172PubMedGoogle Scholar
  27. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley S, Schulz KL, Siemann EH, Sterner RW (2000a) Nutritional constraints in terrestrial and freshwater food webs. Nature 408: 578–580PubMedGoogle Scholar
  28. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF Hobbie SE, Odell GM, Weider LJ (2000b) Biological stoichiometry from genes to ecosystems. Ecol Lett 3: 540–550Google Scholar
  29. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie W, Fagan W, Schade J, Sterner RW (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6: 936–943Google Scholar
  30. Enquist BJ, Niklas KJ (2002) Global allocation rules for patterns of biomass partitioning in seed plants. Science 295: 1517–1520PubMedGoogle Scholar
  31. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9–19Google Scholar
  32. Feldman HA (1995) On the allometric mass exponent, when it exists. J Theor Biol 172: 187–197PubMedGoogle Scholar
  33. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed), On the Economy of Plant Form and Function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  34. Gray BF (1981) On the “surface law” and basal metabolic rate. J Theor Biol 93: 757–767PubMedGoogle Scholar
  35. Grime JP (1979) Plant Strategies and Vegetation Processes. Wiley, ChichesterGoogle Scholar
  36. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164: 243–266Google Scholar
  37. Harvey PH (1982) Rethinking allometry. J Theor Biol 95: 37–41PubMedGoogle Scholar
  38. Hemmingsen AM (1960) Energy metabolism as related to body size and respiratory surfaces, and its evolution. Reports of the Steno Memorial Hospital and Nordisk Insulin Laboratorium 9: 6–110Google Scholar
  39. Heusner A (1982) Energy metabolism and body size. I. Is the 0.75 mass exponent of Kleiber a statistical artifact? Resp Physiol 48: 1–12Google Scholar
  40. Hirose T, Werger MJA (1987) Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72: 520–526Google Scholar
  41. Hunt R (1990) Basic Growth Analysis. Unwin Hyman, LondonGoogle Scholar
  42. Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass surface area and nutrient contents. Proc Natl Acad Sci USA 94: 7362–7366PubMedGoogle Scholar
  43. Jolicoeur P (1990) Bivariate allometry: interval estimation of the sloped of the ordinary and standardized normal major axes and structural relationship. J Theor Biol 144: 275–285Google Scholar
  44. Karpinets TV, Greenwood DJ, Sams CE, Ammons JT (2006) RNA:protein ratio of the unicellular organism as a characteristic of phosphorus and nitrogen stoichiometry of the cellular requirement of ribosomes for protein synthesis. BMC Biol 4: 30PubMedGoogle Scholar
  45. Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF (2005) Plant allometry, stoichiometry and the temperature-dependence of primary productivity. Global Ecol Biogeogr 14: 585–598Google Scholar
  46. Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 168: E103–E122PubMedGoogle Scholar
  47. Klausmeier CA, Litchman E, Daufresne T, Levin SA (2004) Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429: 171–174PubMedGoogle Scholar
  48. Kleiber M (1932) Body size and metabolic rate. Physiol Rev 27: 511–541Google Scholar
  49. Kleiber M (1961) The Fire of Life. An Introduction to Animal Energetics. Wiley, New YorkGoogle Scholar
  50. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33: 1441–1450Google Scholar
  51. Lindstedt SL, Calder WA III (1981) Body size, physiological time, and longevity of homeothermic animals. Quart Rev Biol 56: 1–16Google Scholar
  52. Mathers EM, Houlihan DF, McCarthy ID, Burren LJ (1993) Rates of growth and protein-synthesis correlated with nucleic-acid content in fry of rainbow trout, Oncorhynchus mykiss - effects of age and temperature. J Fish Biol 43: 245–263Google Scholar
  53. Mattson WJ (1980) Herbivory in relation to plant nitrogen-content. Ann Rev Ecol Syst 11: 119–161Google Scholar
  54. McArdle BH (1988) The structural relationship: regression in biology. Can J Zool 66: 2329–2339Google Scholar
  55. McArdle BH (2003) Lines, models, and errors: regression in the field. Limnol Oceanogr 48: 1363–1366Google Scholar
  56. McKee MJ, Knowles CO (1987) Levels of protein, RNA, DNA, glycogen and lipid during growth and development of Daphnia magna Straus (Crustacea: Cladocera). Freshwater Biol 18: 342–351Google Scholar
  57. Meyer MM, Tukey HB Jr (1965) Nitrogen, phosphorus, and potassium plant reserves and the spring growth of Taxus and Forsythia. Proc Am Soc Hort Sci 87: 537–544Google Scholar
  58. Milberg P, Lamont BB (1997) Seed/cotyledon size and nutrient content play a major role in early performance of species on nutrient-poor soils. New Phytol 137: 665–672Google Scholar
  59. Mochizuki T, Hanada S (1958) The effect of nitrogen on the formation of the anisophylly on the terminal shoots of apple trees. Soil Plant Food 4: 68–74Google Scholar
  60. Nielsen SL, Enríquez S, Duarte CM, Sand-Jensen S (1996) Scaling maximum growth rates across photosynthetic organisms. Funct Ecol 10: 167–175Google Scholar
  61. Niklas KJ (1994) Size-dependent variations in plant growth rates and the “3/4-power rule”. Am J Bot 81: 134–144Google Scholar
  62. Niklas KJ (2004) Plant allometry: Is there a grand unifying theory? Biol Rev 79: 871–889PubMedGoogle Scholar
  63. Niklas KJ (2006) Plant allometry, leaf nitrogen and phosphorus stoichiometry and interspecific trends in annual growth rates. Ann Bot 97: 155–163PubMedGoogle Scholar
  64. Niklas KJ, Cobb ED (2005) N, P, and C stoichiometry of Eranthis hyemalis (L). Salib. (Ranunculaceae) and the allometry of plant growth. Am J Bot 92: 1263–1268Google Scholar
  65. Niklas KJ, Cobb ED (2006) Biomass partitioning and leaf N, P-stoichiometry: comparisons between tree and herbaceous current-year shoots. Plant Cell Environ 29: 2030–2042PubMedGoogle Scholar
  66. Niklas KJ, Enquist BJ (2001) Invariant scaling relations for interspecific plant biomass production rates and body size. Proc Natl Acad Sci USA 98: 2922–2927PubMedGoogle Scholar
  67. Niklas KJ, Enquist BJ (2002) On the vegetative biomass partitioning of seed plant leaves, stems, and roots. Am Nat 159: 1517–1520Google Scholar
  68. Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecol Lett 8: 636–642Google Scholar
  69. Niklas KJ, Cobb ED, Niinemets Ü, Reich PB, Sellin A, Shipley B, Wright IJ (2007) “Diminishing returns” in the scaling of functional leaf traits across and within species groups. Proc Natl Acad Sci USA 104: 8894–8896Google Scholar
  70. Peters RH (1983) The Ecological Implications of Body Size. Cambridge University Press, CambridgeGoogle Scholar
  71. Prothero J (1986a) Scaling of energy-metabolism in unicellular organisms - a reanalysis. Comp Biochem Physiol A: Physiol 83: 243–248Google Scholar
  72. Prothero J (1986b) Methodological aspects of scaling in biology. J Theor Biol 118: 259–286PubMedGoogle Scholar
  73. Rayner JMV (1985) Linear relations in biomechanics: the statistics of scaling functions. J Zool 206: 415–439Google Scholar
  74. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101: 11001–11006PubMedGoogle Scholar
  75. Reich PB, Tjoelker MG, Machado JL, Oleksyn J (2006) Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439: 457–461PubMedGoogle Scholar
  76. Rhee G-Y (1978) Effects of N:P atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake. Limnol Oceanogr 23: 10–25CrossRefGoogle Scholar
  77. Ryser P, Verduyn B, Lambers H (1997) Phosphorus allocation and utilization in three grass species with contrasting response to N and P supply. New Phytol 137: 293–302Google Scholar
  78. Sadava D (1993) Cell Biology: Organelles, Structure and Function. Jones and Bartlett, Boston, MAGoogle Scholar
  79. Sands PJ (1995) Modelling canopy production. I. Optimal distribution of photosynthetic resources. Aust J Plant Physiol 22: 603–614Google Scholar
  80. Schmidt-Nielsen K (1984) Scaling: Why Is Animal Size So Important? Cambridge University Press, CambridgeGoogle Scholar
  81. Seim E (1983) On rethinking allometry: which regression model to use? J Theor Biol 104: 161–168Google Scholar
  82. Sellers PJ, Berry JA, Collatz GJ, Field CB, Mooney HA (1992) Canopy reflectance photosynthesis and respiration. III. A reanalysis using improved leaf models and a new canopy integration scheme. Remote Sens Environ 42: 187–216Google Scholar
  83. Silver WL (1994) Is nutrient availability related to plant nutrient use in humid tropical forests. Oecologia 98: 336–343Google Scholar
  84. Sokal RR, Rohlf (1980) Biometry. Freeman, New YorkGoogle Scholar
  85. Smith RJ (1980) Rethinking allometry. J Theor Biol 87: 97–111PubMedGoogle Scholar
  86. Sterner RW, Elser JJ (2002) Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton, NJGoogle Scholar
  87. Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27: 1047–1054Google Scholar
  88. Taylor BK (1967) The nitrogen nutrition of the peach tree. I. Seasonal changes in nitrogenous constituents in mature trees. Aust J Biol Sci 20: 379–387Google Scholar
  89. Taylor BK, May LH (1967) The nitrogen nutrition of the peach tree. II. Storage and mobilization of nitrogen in young trees. Aust J Biol Sci 20: 389–411Google Scholar
  90. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Monographs in Population Biology. Volume 26. Princeton University Press, Princeton, NJGoogle Scholar
  91. Vitousek P (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119: 553–572Google Scholar
  92. Vogt KA, Grier CC, Vogt DJ (1986) Production, turnover, and nutrient dynamics of aboveground and belowground detritus of world forests. Adv Ecol Res 15: 303–377Google Scholar
  93. Vrede T, Dobberfuhl DR, Kooijman SALM, Elser JJ (2004) Fundamental connections among organism C:N:P stoichiometry, macromolecular composition and growth. Ecology 85: 1217–1229Google Scholar
  94. Warton D, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods in allometry. Biol Rev 81: 259–291PubMedGoogle Scholar
  95. Watanabe T, Broadley MR, Jansen S, White PJ, Takada J, Satake K, Takamatsu T, Tuah SJ, Osaki M (2007) Evolutionary control of leaf element composition in plants. New Phytol 174: 516–523PubMedGoogle Scholar
  96. Weibel ER (2002) Physiology - The pitfalls of power laws. Nature 417: 131–132PubMedGoogle Scholar
  97. Weiher E, vanderWerf A, Thompson K, Roderick M, Garnier E, Eriksson O (1999) Challenging Theophrastus: a common core list of plant traits for functional ecology. J Veg Sci 10: 609–620Google Scholar
  98. Werger MJA, Hirose T (1991) Leaf nitrogen distribution and whole canopy photosynthetic carbon gain in herbaceous stands. Vegetatio 97: 11–20Google Scholar
  99. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276: 122–126PubMedGoogle Scholar
  100. West GB, Brown JH, Enquist BJ (1999) The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284: 167–169Google Scholar
  101. West GB, Brown JH, Enquist BJ (2001) A general model for ontogenetic growth. Nature 413: 628–631PubMedGoogle Scholar
  102. Westoby M, Wright IJ (2006) Land-plant ecology on the basis of functional traits. Trends Ecol Evol 21: 261–268PubMedGoogle Scholar
  103. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Ann Rev Ecol Syst 33: 125–159Google Scholar
  104. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428: 821–827PubMedGoogle Scholar
  105. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Global Ecol Biogeogr 14: 411–421Google Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Karl J. Niklas
    • 1
  1. 1.Department of Plant BiologyCornell UniversityIthacaUSA

Personalised recommendations