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Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes

Oecologia volume 155, pages 301–310 (2008)Cite this article

Abstract

Leaf N and P stoichiometry covaries with many aspects of plant biology, yet the drivers of this trait at biogeographic scales remain uncertain. Recently we reported the patterns of leaf C and N based on systematic census of 213 species over 199 research sites in the grassland biomes of China. With the expanded analysis of leaf P, here we report patterns of leaf P and N:P ratios, and analyze the relative contribution of climatic variables and phylogeny in structuring patterns of leaf N:P stoichiometry. Average values of leaf P and N:P ratio were 1.9 mg g−1 and 15.3 (mass ratio), respectively, consistent with the previous observation of a higher N:P ratio in China’s flora than the global averages (ca. 13.8), resulting from a lower leaf P. Climatic variables had very little direct correlation with leaf P and N:P ratios, with growing season precipitation and temperature together explaining less than 2% of the variation, while inter-site differences and within-site phylogenetic variation explained 55 and 26% of the total variation in leaf P and N:P ratios. Across all sites and species, leaf N and P were highly positively correlated at all levels. However, the within-site, within-species covariations of leaf N and P were weaker than those across sites and across species. Leaf N and P relationships are driven by both variation between sites at the landscape scale (explaining 58% of the variance) and within sites at the local scale (explaining 24%), while the climatic factors exerted limited influence (explaining less than 3%). In addition, leaf N:P ratios in two dominant genera Kobresia and Stipa had different responses to precipitation. This study suggests that geographic variation and between-species variation, rather than climatic variation, are the major determinants of grassland foliar stoichiometry at the biome level.

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References

  • Ackerly DD (2004) Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecol Monogr 74:25–44

    Article  Google Scholar 

  • Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    CAS  Article  Google Scholar 

  • Ågren GI (2004) The C:N:P stoichiometry of autotrophs—theory and observations. Ecol Lett 7:185–191

    Article  Google Scholar 

  • Bowman RA (1988) A rapid method to determine total phosphorus in soils. Soil Sci Soc Am J 52:1301–1304

    CAS  Article  Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • Chapin FS III, Matson PA, Mooney H (2002) Principles of terrestrial ecosystem ecology. Springer, New York

    Google Scholar 

  • Chapin FS III, Schulze E-D, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Chapin FS III, Shaver GR (1989) Differences in growth and nutrient use among arctic plant growth forms. Funct Ecol 3:73–80

    Article  Google Scholar 

  • Chapin FS, Oechel WC (1983) Photosynthesis, respiration, and phosphate absorption by Carex aquatilis ecotypes along latitudinal and local environmental gradients. Ecology 64:743–751

    Article  CAS  Google Scholar 

  • Chen S, Bai Y, Zhang L, Han X (2005) Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China. Environ Exp Bot 53:65–75

    Article  Google Scholar 

  • Chen ZZ, Wang SP (2000) Typical steppe ecosystems of China. Science Press, Beijing

    Google Scholar 

  • Cordell S, Goldstein G, Meinzer FC, Vitousek PM (2001) Morphological and physiological adjustment to N and P fertilization in nutrient-limited Metrosideros polymorpha canopy trees in Hawaii. Tree Physiol 21:43–50

    PubMed  CAS  Google Scholar 

  • Cornelissen JHC, Werger MJA, Castro-Díez P, van Rheenen JWA, Rowland AP (1997) Foliar nutrients in relation to growth, allocation and leaf traits in seedlings of a wide range of woody plant species and types. Oecologia 111:460–469

    Article  Google Scholar 

  • Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecol Monogr 69:569–588

    Article  Google Scholar 

  • Dodds WK, Marti E, Tank JL, Pontius J, Hamilton SK, Grimm NB, Bowden WB, McDowell WH, Peterson BJ, Valett HM, Webster JR, Gregory S (2004) Carbon and nitrogen stoichiometry and nitrogen cycling rates in streams. Oecologia 140:458–467

    PubMed  Article  Google Scholar 

  • Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate-stoichiometry couplings in diverse biota. Ecol Lett 6:936–943

    Article  Google Scholar 

  • Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580

    PubMed  Article  CAS  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Essex

    Google Scholar 

  • Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  • Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Ecol Evol Syst 5:37–61

    Article  Google Scholar 

  • Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377

    PubMed  Article  CAS  Google Scholar 

  • He J-S, Fang J, Wang Z, Guo D, Flynn DFB, Geng Z (2006a) Stoichiometry and large-scale patterns of leaf carbon and nitrogen in the grasslands of China. Oecologia 149:115–122

    PubMed  Article  Google Scholar 

  • He J-S, Wang Z, Wang X, Schmid B, Zuo W, Zhou M, Zheng C, Wang M, Fang J (2006b) A test of the generality of leaf trait relationships on the Tibetan Plateau. New Phytol 170:835–848

    PubMed  Article  Google Scholar 

  • Hedin LO, Vitousek PM, Matson PA (2003) Nutrient losses over four million years of tropical forest development. Ecology 84:2231–2255

    Article  Google Scholar 

  • Hessen DO, Agren GI, Anderson TR, Elser JJ, De Ruiter PC (2004) Carbon, sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–1192

    Article  Google Scholar 

  • Hou H-Y (1982a) Vegetation geography and chemical elements: comparative analyses of the dominant plant species. Science Press, Beijing

    Google Scholar 

  • Hou H-Y (1982b) Vegetation Map of the People’s Republic of China (1:4M). Chinese Map Publisher, Beijing

    Google Scholar 

  • Judd T, Bennett LT, Weston CJ, Attiwill PM, Whiteman PH (1996) The response of growth and foliar nutrients to fertilizers in young Eucalyptus globulus (Labill) plantations in Gippsland, southeastern Australia. For Ecol Manage 82:87–101

    Article  Google Scholar 

  • Kay AD, Ashton IW, Gorokhova EC, Kerhoff AJ, Liess A, Litchman E (2005) Toward a stoichiometric framework for evolutionary biology. Oikos 109:6–17

    Article  Google Scholar 

  • Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF (2005) Plant allometry, stoichiometry and the temperature-dependence of primary productivity. Global Ecol Biogeogr 14:485–598

    Article  Google Scholar 

  • 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–E122

    PubMed  Article  Google Scholar 

  • Knecht MR, Goransson A (2004) Terrestrial plants require nutrients in similar proportions. Tree Physiol 24:447–460

    PubMed  CAS  Google Scholar 

  • Koerselman W, Meuleman AFM (1996) The vegetation N/P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450

    Article  Google Scholar 

  • Körner C (1989) The nutrient status of plants from high altitudes: a worldwide comparison. Oecologia 81:379–391

    Google Scholar 

  • Körner C (1999) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Heidelberg

    Google Scholar 

  • Kuo S (1996) Phosphorus. In: Bigham JM (ed) Methods of soil analysis. Part 3. Chemical methods. Soil Science Society of America, American Society of Agronomy, Madison, Wis., pp 869–919

  • Lambers H, Chapin FS III, Pons TL (1998) Plant physiological ecology. Springer, New York

    Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • Moe SJ, Stelzer RS, Forman MR, Harpole WS, Daufresne T, Yoshida T (2005) Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos 109:29–39

    Article  Google Scholar 

  • Niklas KJ (2006) Plant allometry, leaf nitrogen and phosphorus stoichiometry, and interspecific trends in annual growth rates. Ann Bot 97:155–163

    PubMed  Article  CAS  Google Scholar 

  • Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecol Lett 8:636–642

    Article  Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Reich P (2005) Global biogeography of plant chemistry: filling in the blanks. New Phytol 168:263–266

    PubMed  Article  CAS  Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969

    Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci 101:11001–11006

    PubMed  Article  CAS  Google Scholar 

  • Schlesinger WH (1997) Biogeochemistry: an analysis of global change, 2nd edn. Academic Press, San Diego, Calif.

    Google Scholar 

  • Schmid B, Hector A, Huston MA, Inchausti P, Nijs I, Leadley PW, Tilman D (2002) The design and analysis of biodiversity experiments. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 61–75

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Thompson K, Parkinson JA, Band SR, Spencer RE (1997) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytol 136:679–689

    Article  CAS  Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572

    Article  Google Scholar 

  • Vitousek PM (2004) Nutrient cycling and limitation: Hawai’i as a model system. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Wang JT (1988) The steppes and deserts of the Xizang Plateau (Tibet). Vegetatio 75:135–142

    Google Scholar 

  • Woods HA, Makino W, Cotner JB, Hobbie SE, Harrison JF, Acharya K, Elser JJ (2003) Temperature and the chemical composition of poikilothermic organisms. Funct Ecol 17:237–245

    Article  Google Scholar 

  • Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Global Ecol Biogeogr 14:411–421

    Article  Google Scholar 

  • 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 WJ, Lusk C, Midgley JJ, Navas M-L, Niinemets U, 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 428:821–827

    PubMed  Article  CAS  Google Scholar 

  • Zhang C, Tian HQ, Liu JY, Wang SQ, Liu ML, Pan SF, Shi XZ (2005) Pools and distributions of soil phosphorus in China. Global Biogeochem Cycles 19:GB1020. doi:1010.1029/2004GB002296

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful to Wenyun Zuo, Hongqing Feng, Xuefei Li, Chengjun Ji and Yahan Chen for assistance with field sample collections, Cunzhi Liang, Zhongling Liu, Zongyuan Zhu, and Qing Du for plant species identification in the field, and Bernhard Schmid for statistical advice. Dali Guo and Bernhard Schmid provided constructive comments on an earlier version of the manuscript. This research was supported by the Natural Science Foundation of China (grant no. 30670322, 90411004 to J. S. H. and 90211016 to J. Y. F.). We declare that the work reported here complies with the current laws of the People’s Republic of China.

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Authors and Affiliations

  1. Department of Ecology, Peking University, 5 Yiheyuan Road, 100871, Beijing, China

    Jin-Sheng He, Liang Wang, Dan F. B. Flynn, Xiangping Wang, Wenhong Ma & Jingyun Fang

  2. Department of Ecology, Evolution, and Environmental Biology, Columbia University, New York, NY, 10027, USA

    Dan F. B. Flynn

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  1. Jin-Sheng He
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  2. Liang Wang
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Correspondence to Jin-Sheng He.

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Communicated by Guy Midgley.

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He, JS., Wang, L., Flynn, D.F.B. et al. Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155, 301–310 (2008). https://doi.org/10.1007/s00442-007-0912-y

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  • DOI: https://doi.org/10.1007/s00442-007-0912-y

Keywords

  • Leaf traits
  • Biogeographic patterns
  • Inner Mongolia
  • The Tibetan Plateau
  • Xinjiang