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Patterns and controlling factors of plant nitrogen and phosphorus stoichiometry across China’s forests

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Abstract

Plant stoichiometry is critical for the structure and functions of ecosystems. Previous studies on large-scale patterns of plant stoichiometry have focused on single tissues; and the controlling factors have focused on climatic factors or plant functional groups. Here we present results based on an intensive field investigation across China’s forest ecosystems, to comprehensively assess the effect of climatic factors, plant functional groups, soil N and P stoichiometry on N and P stoichiometry of different tree tissues. The P concentrations in all tissues were significantly lower when mean annual temperature (MAT) and mean annual precipitation (MAP) were higher, and the N:P ratios in all tissues were significantly higher when MAT and MAP were higher. The N concentrations of branches and trunks were negatively related to MAT and MAP, however, the leaf N concentrations did not change with MAT and MAP. The root N also did not change with MAT, but decreased significantly with MAP. Soil total N had little influence on tree N, however, tree tissue P concentrations significantly increased when soil P increased. The N contents of all tissues were mainly affected by plant functional groups, however, climate factors and soil P content were the main predictors of P and N:P ratios of all tissues. Our results suggest that tree tissue N:P ratios were largely related to climatic factors, and were shaped by soil P rather than soil N in China’s forest ecosystems.

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References

  • Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641

    Article  Google Scholar 

  • Baron JS, Driscoll CT, Stoddard JL, Richer E (2011) Empirical critical loads of atmospheric nitrogen deposition for nutrient enrichment and acidification of sensitive US lakes. Bioscience 61:602–613

    Article  Google Scholar 

  • Batjes NH (2014) Total carbon and nitrogen in the soils of the world. Eur J Soil Sci 65:10–21

    Article  Google Scholar 

  • Chen Y, Han W, Tang L, Tang Z, Fang J (2013) Leaf nitrogen and phosphorus concentrations of woody plants differ in responses to climate, soil and plant growth form. Ecography 36:178–184

    Article  Google Scholar 

  • Crowley KF, McNeil BE, Lovett GM, Canham CD, Driscoll CT, Rustad LE, Denny E, Hallett RA, Arthur MA, Boggs JL, Goodale CL, Kahl JS, McNulty SG, Ollinger SV, Pardo LH, Schaberg PG, Stoddard JL, Weand MP, Weathers KC (2012) Do nutrient limitation patterns shift from nitrogen toward phosphorus with increasing nitrogen deposition across the northeastern United States? Ecosystems 15:940–957

    Article  Google Scholar 

  • Du EZ, Jiang Y, Fang JY, de Vries W (2014) Inorganic nitrogen deposition in China’s forests: status and characteristics. Atmos Environ 98:474–482

    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

    Article  Google Scholar 

  • Fan H, Wu J, Liu W, Yuan Y, Hu L, Cai Q (2015) Linkages of plant and soil C:N:P stoichiometry and their relationships to forest growth in subtropical plantations. Plant Soil 392:127–138

    Article  Google Scholar 

  • Fang YT, Gundersen P, Mo JM, Zhu WX (2008) Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5:339–352

    Article  Google Scholar 

  • Fang JY, Shen ZH, Tang ZY, Wang XP, Wang ZH, Feng JM, Liu YN, Qiao XJ, Wu XP, Zheng CY (2012) Forest community survey and the structural characteristics of forests in China. Ecography 35:1059–1071

    Article  Google Scholar 

  • Geng Y, Wang ZH, Liang CZ, Fang JY, Baumann F, Kühn P, Scholten T, He JS (2012) Effect of geographical range size on plant functional traits and the relationships between plant, soil and climate in Chinese grasslands. Glob Ecol Biogeogr 21:416–427

    Article  Google Scholar 

  • Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fennica 36:703–743

    Article  Google Scholar 

  • Gurmesa GA, Lu XK, Gundersen P, Mao QG, Zhou KJ, Fang YT, Mo JM (2016) High retention of 15N-labeled nitrogen deposition in a nitrogen-saturated old-growth tropical forest. Glob Chang Biol 22:3608–3620

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • He JS, Wang L, Flynn DFB, Wang XP, Ma WH, Fang JY (2008) Leaf nitrogen:phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155:301–310

    Article  Google Scholar 

  • He JS, Wang XP, Schmid B, Flynn DFB, Li XF, Reich PB, Fang JY (2010) Taxonomic identity, phylogeny, climate and soil fertility as drivers of leaf traits across Chinese grassland biomes. J Plant Res 123:551–561

    Article  Google Scholar 

  • He MZ, Zhang K, Tan HJ, Hu R, Su JQ, Wang J, Huang L, Zhang YF, Li XR (2015) Nutrient levels within leaves, stems, and roots of the xeric species Reaumuria soongorica in relation to geographical, climatic, and soil conditions. Ecol Evol 5:1494–1503

    Article  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Jia YL, Yu GR, He NP, Zhan XY, Fang HJ, Sheng WP, Zuo Y, Zhang DY, Wang QF (2014) Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Sci Rep 4:3763

    Article  Google Scholar 

  • Jones JB (2001) Laboratory guide for conducting soil tests and plant analysis. CRC Press, New York

    Google Scholar 

  • Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growthform variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 168:E103–E122

    Article  Google Scholar 

  • Koerselman W, Mueleman 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 

  • Liu JX, Huang WJ, Zhou GY, Zhang DQ (2013a) Nitrogen to phosphorus ratios of tree species in response to elevated carbon dioxide and nitrogen addition in subtropical forests. Glob Chang Biol 19:208–216

    Article  Google Scholar 

  • Liu XJ, Zhang Y, Han WX, Tang A, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS (2013b) Enhanced nitrogen deposition over China. Nature 494:459–463

    Article  Google Scholar 

  • Luo W, Elser JJ, Lü XT, Wang Z, Bai E, Yan C, Wang C, Li M-H, Zimmermann NE, Han X, Xu Z, Li H, Wu Y, Jiang Y (2015) Plant nutrients do not covary with soil nutrients under changing climatic conditions. Glob Biogeochem Cycles 29:1298–1308

    Article  Google Scholar 

  • Malaeb ZA, Summers JK, Pugesek BH (2000) Using structural equation modeling to investigate relationships among ecological variables. Environ Ecol Stat 7:93–111

    Article  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 

  • Ordoñez JC, Van Bodegom PM, Witte J-PM, Wright IJ, Reich PB, Aerts R (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr 18:137–149

    Article  Google Scholar 

  • Orwin KH, Buckland SM, Johnson D, Turner BL, Smart S, Oakley S, Bardgett RD (2010) Linkages of plant traits to soil properties and the functioning of temperate grassland. J Ecol 98:1074–1083

    Article  Google Scholar 

  • Ostertag R (2016) DiManno NM (2016) Detecting terrestrial nutrient limitation: a global meta-analysis of foliar nutrient concentrations after fertilization. Front Earth Sci 4:23

    Article  Google Scholar 

  • Park JH, Day TA (2007) Temperature response of CO2 exchange and dissolved organic carbon release in a maritime Antarctic tundra ecosystem. Polar Biol 30:1535–1544

    Article  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 USA 101:11001–11006

    Article  Google Scholar 

  • Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL (2008) Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecol Lett 11:793–801

    Article  Google Scholar 

  • Ren SJ, Yu GR, Tao B, Wang SQ (2007) Leaf nitrogen and phosphorus stoichimmetry across 654 terrestrial plant species in NSTEC. Environ Sci 28:2665–2673

    Google Scholar 

  • Sanaullah M, Chabbi A, Girardin C, Durand J-L, Poirier M, Rumpel C (2014) Effects of drought and elevated temperature on biochemical composition of forage plants and their impact on carbon storage in grassland soil. Plant Soil 374:767–778

    Article  Google Scholar 

  • Sardans J, Peñuelas J (2013) Tree growth changes with climate and forest type are associated with relative allocation of nutrients, especially phosphorus, to leaves and wood. Glob Ecol Biogeogr 22:494–507

    Article  Google Scholar 

  • Sardans J, Rivas-Ubach A, Peñuelas J (2011) Factors affecting nutrient concentration and stoichiometry of forest trees in Catalonia (NE Spain). For Ecol Manag 262:2024–2034

    Article  Google Scholar 

  • Schreeg LA, Santiago LS, Wright SJ, Turner BL (2014) Stem, root, and older leaf N:P ratios are more responsive indicators of soil nutrient availability than new foliage. Ecology 95:2062–2068

    Article  Google Scholar 

  • Sistla SA, Schimel JP (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196:68–78

    Article  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell Environ 27:1047–1054

    Article  Google Scholar 

  • Tang XL, Zhao X, Bai YF, Tang ZY, Wang WT, Zhao YC, Wan HW, Xie ZQ, Shi XZ, Wu BF, Wang GX, Yan JH, Ma KP, Du S, Li SG, Han SJ, Ma YX, Hu HF, He NP, Yang YH, Han WX, He HL, Yu GR, Fang JY, Zhou GY (2018) Carbon pools in China’s terrestrial ecosystems: new estimates based on an intensive field survey. Proc Natl Acad Sci USA 115:4021–4026

    Article  Google Scholar 

  • Tian HQ, Chen GS, Zhang C, Melillo JM, Hall CAS (2010) Pattern and variation of C:N:P ratios in China’s soils: a synthesis of observational data. Biogeochemistry 98:139–151

    Article  Google Scholar 

  • Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118

    Article  Google Scholar 

  • Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–373

    Article  Google Scholar 

  • van Ommen Kloeke AEE, Douma JC, Ordo ez JC, Reich PB, Van Bodegom PM (2012) Global quantification of contrasting leaf life span strategies for deciduous and evergreen species in response to environmental conditions. Glob Ecol Biogeogr 21:224–235

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  Google Scholar 

  • Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets U, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr 14(5):411–421

    Article  Google Scholar 

  • Wright SJ, Turner BL, Yavitt JB, Harms KE, Kaspari M, Tanner EVJ, Bujan J, Griffin EA, Mayor JR, Pasquini SC, Sheldrake M, Garcia MN (2018) Plant responses to fertilization experiments in lowland, species-rich, tropical forests. Ecology 99(5):1129–1138

    Article  Google Scholar 

  • Wu TG, Yu MK, Geoff Wang G, Dong Y, Cheng XR (2012) Leaf nitrogen and phosphorus stoichiometry across forty-two woody species in Southeast China. Biochem Syst Ecol 44:255–263

    Article  Google Scholar 

  • Xia JY, Wan SQ (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179:428–439

    Article  Google Scholar 

  • Xia CX, Yu D, Wang Z, Xie D (2014) Stoichiometry patterns of leaf carbon, nitrogen and phosphorous in aquatic macrophytes in eastern China. Ecol Eng 70:406–413

    Article  Google Scholar 

  • Xu ZH, Chen CR, He JZ, Liu JX (2009) Trends and challenges in soil research 2009: linking global climate change to local long-term forest productivity. J Soils Sediments 9:83–88

    Article  Google Scholar 

  • Xu W, Luo XS, Pan YP, Zhang L, Tang AH, Shen JL, Zhang Y, Li KH, Wu QH, Yang DW, Zhang YY, Xue J, Li WQ, Li QQ, Tang L, Lu SH, Liang T, Tong YA, Liu P, Zhang Q, Xiong ZQ, Shi XJ, Wu LH, Shi WQ, Tian K, Zhong XH, Shi K, Tang QY, Zhang LJ, Huang JL, He CE, Kuang FH, Zhu B, Liu H, Jin X, Xin YJ, Shi XK, Du EZ, Dore AJ, Tang S, Collett JL Jr, Goulding K, Sun YX, Ren J, Zhang FS, Liu XJ (2015) Quantifying atmospheric nitrogen deposition through a nationwide monitoring network across China. Atmos Chem Phys 15:12345–12360

    Article  Google Scholar 

  • Yan ZB, Li P, Chen YH, Han WX, Fang JY (2016) Nutrient allocation strategies of woody plants: an approach from the scaling of nitrogen and phosphorus between twig stems and leaves. Sci Rep 6:20099

    Article  Google Scholar 

  • Yang YH, Luo YQ (2011) Carbon: nitrogen stoichiometry in forest ecosystems during stand development. Glob Ecol Biogeogr 20:354–361

    Article  Google Scholar 

  • Yang X, Chi XL, Ji CJ, Liu HY, Ma WH, Mohhammat A, Shi ZY, Wang XP, Yu SL, Yue M, Tang ZY (2016) Variations of leaf N and P concentrations in shrubland biomes across northern China: phylogeny, climate, and soil. Biogeosciences 13:4429–4438

    Article  Google Scholar 

  • Yu ZP, Wang MH, Huang ZQ, Lin TC, Vadeboncoeur MA, Searle EB, Chen HYH (2018) Temporal changes in soil C-N-P stoichiometry over the past 60 years across subtropical China. Glob Change Biol 24:1308–1320

    Article  Google Scholar 

  • Yuan ZY, Chen HYH (2009) Global trends in senesced-leaf nitrogen and phosphorus. Glob Ecol Biogeogr 18:532–542

    Article  Google Scholar 

  • Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Chang 5(5):465–469

    Article  Google Scholar 

  • Yuan ZY, Chen HYH, Reich PB (2011) Global-scale latitudinal patterns of plant fine-root nitrogen and phosphorus. Nat Commun 2:344

    Article  Google Scholar 

  • Zhang SB, Zhang JL, Slik JWF, Cao KF (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Glob Ecol Biogeogr 21:809–818

    Article  Google Scholar 

  • Zhu JX, He NP, Wang QF, Yuan GF, Wen D, Yu GR, Jia YL (2015) The composition, spatial patterns, and influencing factors of atmospheric wet nitrogen deposition in Chinese terrestrial ecosystems. Sci Total Environ 511:777–785

    Article  Google Scholar 

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Acknowledgements

This work was funded by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA05050000) and National Natural Science Foundations of China (41430529 and 31570482). We are very grateful to all the field investigators, who made up a group of more than 1000 participants. We also thank the editor and two anonymous reviewers for thoughtful and constructive comments.

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  1. Juxiu Liu and Xiong Fang contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Xingke Road 723, Tianhe District, 510650, Guangzhou, China

    Juxiu Liu, Xiong Fang, Xuli Tang, Wantong Wang, Guoyi Zhou, Shan Xu, Wenjuan Huang & Junhua Yan

  2. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, 350002, Fuzhou, China

    Xiong Fang

  3. College of Tourism, Henan Normal University, 453007, Xinxiang, China

    Wantong Wang

  4. Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, 610041, Chengdu, China

    Gengxu Wang

  5. Institute of Botany, Chinese Academy of Sciences, 100093, Beijing, China

    Keping Ma

  6. Institute of Soil and Water Conservation, Chinese Academy of Sciences, 712100, Yangling, China

    Sheng Du

  7. Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, 100101, Beijing, China

    Shenggong Li

  8. Institute of Applied Ecology, Chinese Academy of Sciences, 110016, Shenyang, China

    Shijie Han

  9. Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, 666303, Mengla, China

    Youxin Ma

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  1. Juxiu Liu
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Correspondence to Guoyi Zhou.

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Liu, J., Fang, X., Tang, X. et al. Patterns and controlling factors of plant nitrogen and phosphorus stoichiometry across China’s forests. Biogeochemistry 143, 191–205 (2019). https://doi.org/10.1007/s10533-019-00556-7

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