Abstract
Nitrogen (N) to phosphorus (P) allocation in plant organs is of particular interest, as both elements are important to regulate plant growth. We analyzed the scaling relationship of N and P in leaves, stems and fine roots of 224 plant species along an altitudinal transect (500–2,300 m) on the northern slope of Changbai Mountain, China. We tested whether the scaling relationships of N and P were conserved in response to environmental variations. We found that the N and P concentrations of the leaves, stems and fine roots decreased, whereas the N:P ratios increased with increasing altitude. Allometric scaling relationships of N and P were found in the leaves, stems and fine roots, with allometric exponents of 0.78, 0.71 and 0.87, respectively. An invariant allometric scaling of N and P in the leaves, stems and fine roots was detected for woody plants along the altitudinal gradient. These results may advance our understanding of plant responses to climate change, and provide a basis for practical implication of various ecological models.
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Adler PB, Salguero-Gómez R, Compagnoni A, Hsu JS, Ray-Mukherjee J, Mbeau-Ache C, Franco M (2014) Functional traits explain variation in plant life history strategies. Proc Natl Acad Sci USA 111:740–745. doi:10.1073/pnas.1315179111
Ågren GI (2004) The C: N: P stoichiometry of autotrophs–theory and observations. Ecol Lett 7:185–191. doi:10.1111/j.1461-0248.2004.00567.x
Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Annu Rev Ecol, Evol Syst 39:153–170. doi:10.1146/annurev.ecolsys.39.110707.173515
Ågren GI, Weih M (2012) Plant stoichiometry at different scales: element concentration patterns reflect environment more than genotype. New Phytol 194:944–952. doi:10.1111/j.1469-8137.2012.04114.x
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. doi:10.1890/03-9000
Burton AJ, Pregitzer KS, Hendrick RL (2000) Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests. Oecologia 125:389–399. doi:10.1007/s004420000455
Chapin FS III, Vitousek PM, Vancleve K (1986) The nature of nutrient limitation in plant communities. Am Nat 127:48–58
Chen WL, Zeng H, Eissenstat DM, Guo DL (2013) Variation of first-order root traits across climatic gradients and evolutionary trends in geological time. Glob Ecol Biogeogr 22:846–856. doi:10.1111/geb.12048
Chen YH, Han WX, Tang LY, Tang ZY, Fang JY (2011) Leaf nitrogen and phosphorus concentrations of woody plants differ in responses to climate, soil and plant growth form. Ecography 36:178–184. doi:10.1111/j.1600-0587.2011.06833.x
Dijkstra FA, Pendall E, Morgan JA et al (2012) Climate change alters stoichiometry of phosphorus and nitrogen in a semiarid grassland. New Phytol 196:807–815. doi:10.1111/j.1469-8137.2012.04349.x
Elser JJ, Bracken ME, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. doi:10.1111/j.1461-0248.2007.01113.x
Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608. doi:10.1111/j.1469-8137.2010.03214.x
Fisher JB, Malhi Y, Torres IC et al (2013) Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes. Oecologia 172:889–902. doi:10.1007/s00442-012-2522-6
Fortunel C, Fine PV, Baraloto C (2012) Leaf, stem and root tissue strategies across 758 Neotropical tree species. Funct Ecol 26:1153–1161. doi:10.1111/j.1365-2435.2012.02020.x
Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance New Phytol 164:243-266 doi:10.1111/j.1469-8137.2004.01192.x
Garkoti SC (2012) Dynamics of fine root N. Pand K in high elevation forests of central Himalaya Forestry Studies in China 14:145–151. doi:10.1007/s11632-012-0203-5
Garten CT (1976) Correlations between concentrations of elements in plants. Nature 261:686–688. doi:10.1038/261686a0
Geng Y, Wang L, Jin DM, Liu HY, He JS (2014) Alpine climate alters the relationships between leaf and root morphological traits but not chemical traits. Oecologia 175:445–455. doi:10.1007/s00442-014-2919-5
Gordon WS, Jackson RB (2000) Nutrient concentrations in fine roots. Ecology 81:275–280. doi:10.1890/0012-9658(2000)081[0275:NCIFR]2.0.CO;2
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194
Han WX, Fang JY, Guo DL, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385. doi:10.1111/j.1469-8137.2005.01530.x
Han WX, Fang JY, Reich PB, Ian Woodward F, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14:788–796
Hao Z, Kuang Y, Kang M (2014) Untangling the influence of phylogeny, soil and climate on leaf element concentrations in a biodiversity hotspot. Funct Ecol 29:165–176. doi:10.1111/1365-2435.12344
Heberling JM, Fridley JD (2012) Biogeographic constraints on the world-wide leaf economics spectrum. Glob Ecol Biogeogr 21:1137–1146. doi:10.1111/j.1466-8238.2012.00761.x
Heikkinen RK, Luoto M, Kuussaari M, Pöyry J (2005) New insights into butterfly–environment relationships using partitioning methods. P R Soc B 272:2203–2210
Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community- level patterns in fine root traits along a 120,000-year soil chronosequence in temperate rain forest. J Ecol 99:954–963
Iversen CM (2014) Using root form to improve our understanding of root function. New Phytol 203:707–709. doi:10.1111/nph.12902
Köhler L, Gieger T, Leuschner C (2006) Altitudinal change in soil and foliar nutrient concentrations and in microclimate across the tree line on the subtropical island mountain Mt. Teide (Canary Islands). Flora 201:202–214 doi:10.1016/j.flora.2005.07.003
Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF (2005) Plant allometry, stoichiometry and the temperature dependence of primary productivity. Glob Ecol Biogeogr 14:585–598. doi:10.1111/j.1466-822X.2005.00187.x
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. doi:10.1086/507879
Legendre P, Legendre L (1998) Numerical ecology, 2nd English edition edn. Elsevier Science BV, Amsterdam
Li A, Guo DL, Wang ZQ, Liu HY (2010) Nitrogen and phosphorus allocation in leaves, twigs, and fine roots across 49 temperate, subtropical and tropical tree species: a hierarchical pattern. Funct Ecol 24:224–232
Liu GF, Freschet GT, Pan X, Cornelissen JHC, Li Y, Dong M (2010) Coordinated variation in leaf and root traits across multiple spatial scales in Chinese semi-arid and arid ecosystems. New Phytol 188:543–553. doi:10.1111/j.1469-8137.2010.03388.x
Macek P, Macková J, de Bello F (2009) Morphological and ecophysiological traits shaping altitudinal distribution of three Polylepis treeline species in the dry tropical Andes. Acta Oecol 35:778–785. doi:10.1016/j.actao.2009.08.013
Marschner H, Kirkby E, Cakmak I (1996) Effect of mineral nutritional status on shoot-root partitioning of photoassimilates and cycling of mineral nutrients. J Exp Bot 47:1255–1263. doi:10.1093/jxb/47.Special_Issue.1255
Minden V, Kleyer M (2014) Internal and external regulation of plant organ stoichiometry. Plant Biol 16:897–907. doi:10.1111/plb.12155
Pregitzer KS, King JS, Burton AJ, Brown SE (2000) Responses of tree fine roots to temperature. New Phytol 147:105–115. doi:10.1046/j.1469-8137.2000.00689.x
Price CA, Weitz JS, Savage VM et al (2012) Testing the metabolic theory of ecology. Ecol Lett 15:1465–1474. doi:10.1111/j.1461-0248.2012.01860.x
R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006. doi:10.1073/pnas.0403588101
Reich PB, Oleksyn J, Wright IJ, Niklas KJ, Hedin L, Elser JJ (2010) Evidence of a general 2/3-power law of scaling leaf nitrogen to phosphorus among major plant groups and biomes. P R Soc B 277:877–883. doi:10.1098/rspb.2009.1818
Shao G, Shugart HH, Zhao G, Zhao S, Wang S, Schaller J (1996) Forest cover types derived from Landsat Thematic Mapper imagery for Changbai Mountain area of China. Can J For Res 26:206–216. doi:10.1139/x26-024
Shi WQ, Wang GA, Han WX (2012) Altitudinal variation in leaf nitrogen concentration on the eastern slope of Mount Gongga on the Tibetan Plateau. China. PloS one 7:e44628. doi:10.1371/journal.pone.0044628
Soethe N, Lehmann J, Engels C (2008) Nutrient availability at different altitudes in a tropical montane forest in Ecuador. J Trop Ecol 24:397. doi:10.1017/S026646740800504X
Sokal RR, Rohlf FJ (1981) Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Company, New York
Stock WD, Verboom GA (2012) Phylogenetic ecology of foliar N and P concentrations and N: P ratios across mediterranean-type ecosystems. Glob Ecol Biogeogr 21:1147–1156. doi:10.1111/j.1466-8238.2011.00752.x
Sundqvist MK, Giesler R, Wardle DA (2011) Within-and across-species responses of plant traits and litter decomposition to elevation across contrasting vegetation types in subarctic tundra. PloS One 6:e27056. doi:10.1371/journal.pone.0027056
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15. doi:10.1890/08-0127.1
Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol, Evol Syst. 125–159 doi:10.1146/annurev.ecolsys.33.010802.150452
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. doi:10.1038/nature02403
Xiang S, Reich PB, Sun SC, Atkin OK (2013) Contrasting leaf trait scaling relationships in tropical and temperate wet forest species. Funct Ecol 27:522–534. doi:10.1111/1365-2435.12047
Yang X, Tang ZY, Ji CJ et al (2014) Scaling of nitrogen and phosphorus across plant organs in shrubland biomes across Northern China. Sci Rep 4:5448. doi:10.1038/srep05448
Yuan ZY, Chen HY, Reich PB (2011) Global-scale latitudinal patterns of plant fine-root nitrogen and phosphorus. Nat Commun 2:344. doi:10.1038/ncomms1346
Zhang M, Zhang XK, Liang WJ, Jiang Y, Dai GH, Wang XG, Han SJ (2011) Distribution of soil organic carbon fractions along the altitudinal gradient in Changbai Mountain. China Pedosphere 21:615–620. doi:10.1016/S1002-0160(11)60163-X
Zhang SB, Zhang JL, Slik J, Cao KF (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Glob Ecol Biogeogr 21:809–818. doi:10.1111/j.1466-8238.2011.00729.x
Zhao N, He NP, Wang QF, Zhang XY, Wang RL, Xu ZW, Yu GR (2014) The altitudinal patterns of leaf C: N: P stoichiometry are regulated by plant growth form, climate and soil on Changbai Mountain, China. PloS one 9:e95196. doi:10.1371/journal.pone.0095196
Zhu B, Wang XP, Fang JY, Piao SL, Shen HH, Zhao SQ, Peng CH (2010) Altitudinal changes in carbon storage of temperate forests on Mt Changbai, Northeast China. J Plant Res 123:439–452. doi:10.1007/s10265-009-0301-1
Acknowledgments
This work was supported by the Major Program of the National Natural Science Foundation of China [No. 31290221], and the Program for “Kezhen” Distinguished Talents in Institute of Geographic Sciences and Natural Resources Research, CAS. We thank teachers and students of Beihua University of China for field sampling assistance and the staff of Key Laboratory of Ecosystem Network Observation and Modelling of IGSNRR, CAS for laboratory analysis.
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Zhao, N., Yu, G., He, N. et al. Invariant allometric scaling of nitrogen and phosphorus in leaves, stems, and fine roots of woody plants along an altitudinal gradient. J Plant Res 129, 647–657 (2016). https://doi.org/10.1007/s10265-016-0805-4
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DOI: https://doi.org/10.1007/s10265-016-0805-4