Chin J Plant Ecol ›› 2019, Vol. 43 ›› Issue (3): 185-196.doi: 10.17521/cjpe.2018.0240

• Review •     Next Articles

Impacts of nitrogen addition on plant phosphorus content in forest ecosystems and the underlying mechanisms

FENG Chan-Ying1,ZHENG Cheng-Yang1,*(),TIAN Di2   

  1. 1 College of Urban and Environmental Sciences, Peking University, Beijing 100871, China
    2 College of Life Sciences, Capital Normal University, Beijing 100048, China
  • Received:2018-09-27 Revised:2019-03-05 Online:2019-07-25 Published:2019-03-20
  • Contact: ZHENG Cheng-Yang E-mail:zhengcy@pku.edu.cn
  • Supported by:
    Supported by the National Natural Science Foundation of China(31321061);The National Key R&D Program of China(2017YFC05039)

Abstract:

Nitrogen (N) deposition has profound impacts on the phosphorus (P) cycling in forest ecosystems. Especially, the aggravated P limitation on tree growth under N addition has caused much attention to researchers. This article reviews the effects of N addition on plant P content in forest ecosystems. The result showed that N addition increased soil available P and facilitated the absorption of P by plants by promoting soil phosphatase activity, thereby increasing plant P content. Furthermore, changes in tree P content following N addition were also affected by species, life forms as well as experimental duration. Due to the inconsistency, the underlying mechanisms of changes in P content under N addition were further summarized as follows: 1) changes in soil available P content induced by exogenous N input affected the source of plant P; 2) N input affected the P uptake capacity of plants by affecting plant root exudates, mycorrhizal symbiosis and root morphological structure; 3) plant P utilization efficiency was also influenced with changes of P re-distribution and P re-absorption. Overall, for the changes in plant P under increasing exogenous N inputs, alterations of soil available P under N addition was the primary factor, while changes in plant P uptake capacity and P utilization efficiency ulteriorly regulated plant P content.

Key words: nitrogen deposition, forest ecosystems, plant phosphorus concentration, stoichiometry, underlying mechanisms

Fig. 1

Plant-soil phosphorus cycling in forest ecosystems (adapted from Reed et al., 2015; Chen et al., 2016)."

[1] Aber J, Mcdowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I ( 1998). Nitrogen saturation in temperate forest ecosystems: Hypotheses revisited. Bioscience, 48, 921-934.
[2] Aerts R ( 1996). Nutrient resorption from senescing leaves of perennials: Are there general patterns? Journal of Ecology, 84, 597-608.
[3] Allen MF, Swenson W, Querejeta JI, Egertonwarburton LM, Treseder KK ( 2003). Ecology of mycorrhizae: A conceptual framework for complex interactions among plants and fungi. Annual Review of Phytopathology, 41, 271-303.
[4] Alvarez-Clare S, Mack MC, Brooks M ( 2013). A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology, 94, 1540-1551.
[5] Bünemann E, Oberson A, Frossard E ( 2011). Phosphorus in Action. Springer, Berlin Heidelberg.
[6] Casson NJ, Eimers MC, Watmough SA ( 2012). An assessment of the nutrient status of sugar maple in Ontario: Indications of phosphorus limitation. Environmental Monitoring and Assessment, 184, 5917-5927.
[7] Chapin III FS, Matson PA, Vitousek PM ( 2012). Principles of Terrestrial Ecosystem Ecology. Springer, New York.
[8] Chapin III FS, Shaver GR, Kedrowski RA ( 1986). Environmental controls over carbon, nitrogen and phosphorus fractions in Eriophorum vaginatum in Alaskan tussock tundra. Journal of Ecology, 74, 167-195.
[9] Chen FS, Niklas KJ, Liu Y, Fang XM, Wan SZ, Wang H ( 2015). Nitrogen and phosphorus additions alter nutrient dynamics but not resorption efficiencies of Chinese fir leaves and twigs differing in age. Tree Physiology, 35, 1106-1117.
[10] Chen GT, Peng Y, Zheng J, Li S, Peng TC, Qiu XR, Tu LH ( 2017 a). Effects of short-term nitrogen addition on fine root biomass, lifespan and morphology of Castanopsis platyacantha in a subtropical secondary evergreen broad-leaved forest. Chinese Journal of Plant Ecology, 41, 1041-1050.
[ 陈冠陶, 彭勇, 郑军, 李顺, 彭天驰, 邱细容, 涂利华 ( 2017 a). 氮添加对亚热带次生常绿阔叶林扁刺栲细根生物量、寿命和形态的短期影响. 植物生态学报, 41, 1041-1050.]
[11] Chen GT, Zheng J, Peng TC, Li S, Qiu XR, Chen YQ, Ma HY, Tu LH ( 2017 b). Fine root morphology and chemistry characteristics in different branch orders of Castanopsis platyacantha and their responses to nitrogen addition. Chinese Journal of Applied Ecology, 28, 3461-3468.
[ 陈冠陶, 郑军, 彭天驰, 李顺, 邱细容, 陈雨芩, 马豪宇, 涂利华 ( 2017 b). 扁刺栲不同根序细根形态和化学特征及其对短期氮添加的响应. 应用生态学报, 28, 3461-3468.]
[12] Chen ML, Chen H, Mao QG, Zhu XM, Mo JM ( 2016). Effect of nitrogen deposition on the soil phosphorus cycle in forest ecosystems: A review. Acta Ecologica Sinica, 36, 4965-4976.
[ 陈美领, 陈浩, 毛庆功, 朱晓敏, 莫江明 ( 2016). 氮沉降对森林土壤磷循环的影响. 生态学报, 36, 4965-4976.]
[13] Chen WW, Kou L, Jiang L, Gao WL, Yang H, Wang HM, Li SG ( 2017). Short-term responses of foliar multi-element stoichiometry and nutrient resorption of slash pine to N addition in subtropical China. Chinese Journal of Applied Ecology, 28, 1094-1102.
[ 陈微微, 寇亮, 蒋蕾, 高文龙, 杨浩, 王辉民, 李胜功 ( 2017). 亚热带湿地松叶片多元素化学计量与养分回收对氮添加的短期响应. 应用生态学报, 28, 1094-1102.]
[14] Crous K, Ósvaldsson A, Ellsworth D ( 2015). Is phosphorus limiting in a mature Eucalyptus woodland? Phosphorus fertilisation stimulates stem growth. Plant and Soil, 391, 293-305.
[15] 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.
[16] Dai KJ, He F, Guan HL, Shen YX, Zhang GM ( 2006). Research advances in plant and its low-phosphorus environment inducement, adaptation and countermeasures. Chinese Journal of Ecology, 25, 1580-1585.
[ 戴开结, 何方, 官会林, 沈有信, 张光明 ( 2006). 植物与低磷环境研究进展——诱导、适应与对策. 生态学杂志, 25, 1580-1585.]
[17] Deng HJ, Zhang LN, Zhang GS, Lin YM, Wu CZ, Hong W ( 2015). Effects of nitrogen deposition on leaf elements and their stoichiometric ratios in Schima superba and Pinus massoniana mixed forest. Journal of Forest and Environment, 35, 118-124.
[ 邓浩俊, 张丽娜, 张广帅, 林勇明, 吴承祯, 洪伟 ( 2015). 氮添加对木荷马尾松林叶片元素计量比的影响. 森林与环境学报, 35, 118-124.]
[18] Deng MF, Liu LL, Sun ZZ, Piao SL, Ma YC, Chen YW, Wang J, Qiao CL, Wang X, Li P ( 2016). Increased phosphate uptake but not resorption alleviates phosphorus deficiency induced by nitrogen deposition in temperate Larix principis-‌rupprechtii plantations. New Phytologist, 212, 1019-1029.
[19] Deng Q, Hui D, Dennis S, Reddy KC ( 2017). Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: A meta analysis. Global Ecology and Biogeography, 26, 713-728.
[20] Devau N, Le Cadre E, Hinsinger P, Jaillard B, Gerard F ( 2009). Soil pH controls the environmental availability of phosphorus: Experimentaland mechanistic modelling approaches. Applied Geochemistry, 24, 2163-2174.
[21] Diepen LTAV, Lilleskov EA, Pregitzer KS, Miller RM ( 2007). Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen additions. New Phytologist, 176, 175-183.
[22] Dodd JC, Burton CC, Burns RG, Jeffries P ( 1987). Phosphatase activity associated with the roots and the rhizosphere of plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytologist, 107, 163-172.
[23] Du E ( 2016). Rise and fall of nitrogen deposition in the United States. Proceedings of the National Academy of Sciences of the United States of America, 113, 3594-3595.
[24] Elser JJ, Bracken ME, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE ( 2007). Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters, 10, 1135-1142.
[25] Elvir JA, Rustad L, Wiersma GB, Fernandez I, White AS, White GJ ( 2005). Eleven-year response of foliar chemistry to chronic nitrogen and sulfur additions at the Bear Brook Watershed in Maine. Canadian Journal of Forest Research, 35, 1402-1410.
[26] Emmett BA ( 2007). Nitrogen saturation of terrestrial ecosystems: Some recent findings and their implications for our conceptual framework. Water, Air, & Soil Pollution, 7, 99-109.
[27] Filippelli GM ( 2002). The global phosphorus cycle. Reviews in Mineralogy & Geochemistry, 48, 391-425.
[28] Fujita Y, Venterink HO, van Bodegom PM ( 2014). Low investment in sexual reproduction threatens plants adapted to phosphorus limitation. Nature, 505, 82-86.
[29] Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vorosmarty CJ ( 2004). Nitrogen cycles: Past, present, and future. Royal Horticultural Society, 70, 153-226.
[30] Garrish V, Cernusak LA, Winter K, Turner BL ( 2010). Nitrogen to phosphorus ratio of plant biomass versus soil solution in a tropical pioneer tree, Ficus insipida. Journal of Experimental Botany, 61, 3735-3748.
[31] Garten CT ( 1976). Correlations between concentrations of elements in plants. Nature, 261, 686-688.
[32] Gianinazzi S, Gianinazzi-Pearson V, Dexheimer J ( 1979). Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhiza. III. ultrastructural localization of acid and alkaline phosphatase in onion roots infected by glomus mosseae (nicol. & gerd.). New Phytologist, 82, 127-132.
[33] Gundersen P, Emmett BA, Kjønaas OJ, Koopmans CJ, Tietema A ( 1998). Impact of nitrogen deposition on nitrogen cycling in forests: A synthesis of NITREX data. Forest Ecology and Management, 101, 37-55.
[34] Güsewell S ( 2004). N:P ratios in terrestrial plants: Variation and functional significance. New Phytologist, 164, 243-266.
[35] Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken ME ( 2011). Nutrient co-limitation of primary producer communities. Ecology Letters, 14, 852-862.
[36] Hedley MJ, Stewart JWB, Chauhan BS ( 1982). Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Journal of the Soil Science Society of America, 46, 970-976.
[37] Heerwaarden LMV, Toet S, Aerts R ( 2003). Nitrogen and phosphorus resorption efficiency and proficiency in six sub-arctic bog species after 4 years of nitrogen fertilization. Journal of Ecology, 91, 1060-1070.
[38] Hodge A ( 2004). The plastic plant: Root responses to heterogeneous supplies of nutrients. New Phytologist, 162, 9-24.
[39] Homeier J, Hertel D, Camenzind T, Cumbicus NL, Maraun M, Martinson GO, Poma M, Rillig MC, Sandmann D, Scheu S, Veldkamp E, Wilcke W, Wullaert H, Leuschner C ( 2012). Tropical andean forests are highly susceptible to nutrient inputs—Rapid effects of experimental N and P addition to an ecuadorian montane forest. PLOS ONE, 7, e47128. DOI: 10.1371/journal.pone.‌0047128.
[40] Jakobsen I, Abbott LK, Robson AD ( 2010). External hyphae of vesicular—Arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytologist, 120, 509-516.
[41] Jansa J, Mozafar A, Frossard E ( 2005). Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant and Soil, 276, 163-176.
[42] Koerselman W ( 1996). The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology, 33, 1441-1450.
[43] Kou L, Guo DL, Yang H, Gao WL, Li SG ( 2015). Growth, morphological traits and mycorrhizal colonization of fine roots respond differently to nitrogen addition in a slash pine plantation in subtropical China. Plant and Soil, 391, 207-218.
[44] Kou L, Wang HM, Gao WL, Chen WW, Yang H, Li SG ( 2017). Nitrogen addition regulates tradeoff between root capture and foliar resorption of nitrogen and phosphorus in a subtropical pine plantation. Trees, 31, 77-91.
[45] Lee W, Fenner M ( 1989). Mineral nutrient allocation in seeds and shoots of twelve Chionochloa species in relation to soil fertility. Journal of Ecology, 77, 704-716.
[46] Lehmann J, Muraoka T, Zech W ( 2001). Root activity patterns in an Amazonian agroforest with fruit trees determined by 32P, 33P and 15N applications . Agroforestry Systems, 52, 185-197.
[47] Li HY, Zhu YG, Marschner P, Smith FA, Smith SE ( 2005). Wheat responses to arbuscular mycorrhizal fungi in a highly calcareous soil differ from those of clover, and change with plant development and P supply. Plant and Soil, 277, 221-232.
[48] Li QK ( 1986). The progress of modern phosphate fertilizer research. Progress in Soil Science, 14(2), 1-7.
[ 李庆逵 ( 1986). 现代磷肥研究的进展. 土壤学进展, 14(2), 1-7.]
[49] Li Y, Niu SL, Yu GR ( 2016). Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: A meta-analysis. Global Change Biology, 22, 934-943.
[50] Li Y, Tian D, Yang H, Niu S ( 2018). Size-dependent nutrient limitation of tree growth from subtropical to cold temperate forests. Functional Ecology, 32, 863-875.
[51] Liu JX, Huang WJ, Zhou GY, Zhang DQ, Liu SZ, Li YY ( 2013 a). Nitrogen to phosphorus ratios of tree species in response to elevated carbon dioxide and nitrogen addition in subtropical forests. Global Change Biology, 19, 208-216.
[52] Liu L, Zhang T, Gilliam FS, Gundersen P, Zhang W, Chen H, Mo JM ( 2013 b). Interactive effects of nitrogen and phosphorus on soil microbial communities in a tropical forest. PLOS ONE, 8, e61188. DOI: 10.1371/journal.pone.0061188.
[53] Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS ( 2013 c). Enhanced nitrogen deposition over China. Nature, 494, 459-462.
[54] Lu XK, Mo JM, Gilliam FS, Fang H, Zhu FF, Fang YT, Zhang W, Huang J ( 2012). Nitrogen addition shapes soil phosphorus availability in two reforested tropical forests in southern China. Biotropica, 44, 302-311.
[55] Lussenhop J, Treonis A, Curtis PS, Teeri JA, Vogel CS ( 1998). Response of soil biota to elevated atmospheric CO2 in poplar model systems. Oecologia, 113, 247-251.
[56] Ma YJ ( 2015). Effects of Fertilization on Nutrient Absorption Characteristics and the Law of C, N, P Ecological Stoichiometry of Cunninghamia lanceolata. Master degree dissertation, Northwest A & F University, Yangling, Shaanxi.
[ 马亚娟 ( 2015). 施肥对杉木养分吸收特性及其碳、氮、磷生态化学计量规律的影响. 硕士学位论文, 西北农林科技大学, 陕西杨凌.]
[57] Marklein AR, Houlton BZ ( 2012). Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytologist, 193, 696-704.
[58] Mayor JR, Wright SJ, Turner BL ( 2014). Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. Journal of Ecology, 102, 36-44.
[59] Minden V, Kleyer M ( 2014). Internal and external regulation of plant organ stoichiometry. Plant Biology, 16, 897-907.
[60] Mohren GMJ, Burger FW ( 1986). Phosphorus deficiency induced by nitrogen input in Douglas fir in the Netherlands. Plant and Soil, 95, 191-200.
[61] Mudge SR, Rae AL, Diatloff E, Smith FW ( 2002). Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant Journal, 31, 341-353.
[62] Olsen JK, Bell LC ( 1990). A glasshouse evaluation of “critical” N and P concentrations and N:P ratios in various plant parts of six eucalypt species. Australian Journal of Botany, 38, 669-678.
[63] Pang L, Zhang Y, Zhou ZC, Feng ZP, Chu DY ( 2014). Effects of simulated nitrogen deposition on growth and phosphorus efficiency of Pinus massoniana under low phosphorus stress. Journal of Applied Ecology, 25, 1275-1282.
[ 庞丽, 张一, 周志春, 丰忠平, 储德裕 ( 2014). 模拟氮沉降对低磷胁迫下马尾松生长和磷效率的影响. 应用生态学报, 25, 1275-1282.]
[64] Pang L, Zhou ZC, Zhang Y, Feng ZP ( 2016). Effects of atmospheric N sedimentation on growth and P efficiency of Pinus Massoniana mycorrhizal seedlings under low P stress. Journal of Plant Nutrition and Fertilizer, 22, 225-235.
[ 庞丽, 周志春, 张一, 丰忠平 ( 2016). 大气氮沉降提高低磷土壤条件下马尾松菌根共生和磷效率的原因. 植物营养与肥料学报, 22, 225-235.]
[65] Pant HK, Warman PR ( 2000). Enzymatic hydrolysis of soil organic phosphorus by immobilized phosphatases. Biology and Fertility of Soils, 30, 306-311.
[66] Pasqualini D, Uhlmann A, Stürmer SL ( 2007). Arbuscular mycorrhizal fungal communities influence growth and phosphorus concentration of woody plants species from the Atlantic rain forest in South Brazil. Forest Ecology and Management, 245, 148-155.
[67] Raghothama KG ( 1999). Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 665-693.
[68] Reed SC, Yang X, Thornton PE ( 2015). Incorporating phosphorus cycling into global modeling efforts: A worthwhile, tractable endeavor. New Phytologist, 208, 324-329.
[69] Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL ( 2012). Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. Journal of Ecology, 100, 309-316.
[70] 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.
[71] See CR, Yanai RD, Fisk MC, Vadeboncoeur MA, Quintero BA, Fahey TJ ( 2015). Soil nitrogen affects phosphorus recycling: Foliar resorption and plant-soil feedbacks in a northern hardwood forest. Ecology, 96, 2488-2498.
[72] Silver WL, Thompson AW, Reich A, Ewel JJ, Firestone MK ( 2005). Nitrogen cycling in tropical plantation forests: Potential controls on nitrogen retention. Ecological Applications, 15, 1604-1614.
[73] Song P, Zhang R, Zhang Y, Zhou ZC, Feng ZP ( 2016). Effects of simulated nitrogen deposition on fine root morphology, nitrogen and phosphorus efficiency of Pinus massoniana clone under phosphorus deficiency. Chinese Journal of Plant Ecology, 40, 1136-1144.
[ 宋平, 张蕊, 张一, 周志春, 丰忠平 ( 2016). 模拟氮沉降对低磷胁迫下马尾松无性系细根形态和氮磷效率的影响. 植物生态学报, 40, 1136-1144.]
[74] Sterner RW, Elser JJ ( 2002). Ecological Stoichiometry:The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton, USA.
[75] Sullivan BW, Alvarez-Clare S, Castle SC, Porder S, Reed SC, Schreeg L, Townsend AR, Cleveland CC ( 2014). Assessing nutrient limitation in complex forested ecosystems: Alternatives to large-scale fertilization experiments. Ecology, 95, 668-681.
[76] Tarafdar JC, Claassen N ( 1998). Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms. Biology and Fertility of Soils, 5, 308-312.
[77] Tessier JT, Raynal DJ ( 2003). Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. Journal of Applied Ecology, 40, 523-534.
[78] Tian D ( 2017). Effects of Nutrient Fertilization on the Main Processes of Carbon Cycling in Subtropical Forests. PhD dissertation, Peking University, Beijing.
[ 田地 ( 2017). 养分添加对亚热带常绿阔叶林碳循环主要过程的影响. 博士学位论文, 北京大学, 北京.]
[79] Tian D, Jiang L, Du EZ, Ma SH, Zeng WJ, Zou AL, Feng CY, Xu LC, Xing AJ, Wang W, Zheng CY, Ji CJ, Shen HH, Fang JY ( 2018). Responses of forest ecosystems to increasing nitrogen deposition in China: A critical review. Environmental Pollution, 243, 75-86.
[80] Tian D, Yan ZB, Niklas KJ, Han WX, Kattge J, Reich PB, Luo YK, Chen YH, Tang ZY, Hu HF, Wright LJ, Schmid B, Fang JY ( 2017). Global leaf nitrogen and phosphorus stoichiometry and their scaling exponent. National Science Review, 5, 728-739.
[81] Tibbett M, Sanders FE ( 2002). Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Annals of botany, 89, 783-789.
[82] Treseder KK, Vitousek PM ( 2001). Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian Rain Forests. Ecology, 82, 946-954.
[83] Turner BL ( 2010). Leaf nitrogen to phosphorus ratios of tropical trees: Experimental assessment of physiological and environmental controls. New Phytologist, 185, 770-779.
[84] Turner BL, Brenesarguedas T, Condit R ( 2018). Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature, 555, 367-370.
[85] Vance CP ( 2001). Symbiotic nitrogen fixation and phosphorus acquisition: Plant nutrition in a world of decining renewable resources. Plant Physiology, 127, 390-397.
[86] Vance CP, Uhde-Stone, Claudia, Allan DL ( 2010). Phosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource. New Phytologist, 157, 423-447.
[87] Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB ( 2012). Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecological Monographs, 82, 205-220.
[88] Vitousek P ( 1982). Nutrient cycling and nutrient use efficiency. The American Naturalist, 119, 553-572.
[89] Vitousek PM, Porder S, Houlton BZ, Chadwick OA ( 2010). Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications, 20, 5-15.
[90] Vries WD, Du E, Butterbach-Bahl K ( 2014). Short and long-term impacts of nitrogen deposition on carbon sequestration by forest ecosystems. Current Opinion in Environmental Sustainability, 9-10, 90-104.
[91] Waldner P, Marchetto A, Thimonier A, Schmitt M, Rogora M, Granke O, Mues V, Hansen K, Karlsson GP, Zlindra D, Clarke N, Verstraeten A, Lazdins A, Schimming C, Iacoban C, Lindroos A, Vanguelova E, Benham S, Meesenburg H, Nicolas M, Kowalska A, Apuhtin V, Napa U, Lachmanova Z, Kristoefel F, Bleeker A, Ingerslev M, Vesterdal L, Molina J, Fischer U, Seidling W, Jonard M, O'Dea P, Johnson J, Fischer R, Lorenz M ( 2014). Detection of temporal trends in atmospheric deposition of inorganic nitrogen and sulphate to forests in Europe. Atmospheric Environment, 95, 363-374.
[92] Wang M, Murphy MT, Moore TR ( 2014). Nutrient resorption of two evergreen shrubs in response to long-term fertilization in a bog. Oecologia, 174, 365-377.
[93] Wang QSY, Zheng CY, Zhang XY, Zeng FX, Xing J ( 2016). Impacts of nitrogen addition on foliar nitrogen and phosphorus stoichiometry in a subtropical evergreen broad-leaved forest in Mount Wuyi. Chinese Journal of Plant Ecology, 40, 1124-1135.
[ 王乔姝怡, 郑成洋, 张歆阳, 曾发旭, 邢娟 ( 2016). 氮添加对武夷山亚热带常绿阔叶林植物叶片氮磷化学计量特征的影响. 植物生态学报, 40, 1124-1135.]
[94] Weand MP, Arthur MA, Lovett GM ( 2010). The phosphorus status of northern hardwoods differs by species but is unaffected by nitrogen fertilization. Biogeochemistry, 97, 159-181.
[95] Wurzburger N, Wright SJ ( 2015). Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology, 96, 2137-2146.
[96] Yan T, Qu TT, Song HH, Ciais P, Piao SL, Sun ZZ, Zeng H ( 2018). Contrasting effects of N addition on the N and P status of understory vegetation in plantations of sapling and mature Larix principis-rupprechtii. Journal of Plant Ecology, 11, 843-852.
[97] Yan ZB, Guan HY, Han WX, Han TS, Guo YL, Fang JY ( 2016). Reproductive organ and young tissues show constrained elemental composition in Arabidopsis thaliana. Annals of Botany, 117, 431-439.
[98] Yang H ( 2018). Effects of nitrogen and phosphorus addition on leaf nutrient characteristics in a subtropical forest. Trees, 32, 383-391.
[99] Yang K, Zhu JJ, Gu JC, Yu LZ, Wang ZQ ( 2015). Changes in soil phosphorus fractions after 9 years of continuous nitrogen addition in a Larix gmelinii plantation. Annals of Forest Science, 72, 435-442.
[100] Yang X, Tang ZY, Ji CJ, Liu HY, Ma WH, Mohhamot A, Shi ZY, Sun W, Wang T, Wang XP, Wu X, Yu SL, Yue M, Zheng CY ( 2014). Scaling of nitrogen and phosphorus across plant organs in shrubland biomes across Northern China. Scientific Reports, 4, 5448. DOI: 10.1038/srep05448.
[101] Yuan ZY, Chen HYH ( 2016). Negative effects of fertilization on plant nutrient resorption. Ecology, 96, 373-380.
[102] Zhang QF, Xie JS, Lyu MK, Xiong DC, Wang J, Chen YH, Li YQ, Wang MK, Yang YS ( 2017). Short-term effects of soil warming and nitrogen addition on the N:P stoichiometry of Cunninghamia lanceolata, in subtropical regions. Plant and Soil, 411, 395-407.
[103] Zhang Y, Zhou ZC, Yang Q ( 2013). Genetic variations in root morphology and phosphorus efficiency of Pinus massoniana, under heterogeneous and homogeneous low phosphorus conditions. Plant and Soil, 364, 93-104.
[104] Zhao Y ( 2016). Effects of N Fertilization on C:N:P Ecological Stoichiometry of Chinese fir in Huitong. Master degree dissertation, Central South University of Forestry and Technology, Changsha.
[ 赵月 ( 2016). 施N肥对会同杉木人工林C:N:P生态化学计量特征的影响. 硕士学位论文, 中南林业科技大学, 长沙.]
[105] Zhou LL, Addo-Danso SD, Wu PF, Li SB, Zou XH, Zhang Y, Ma XQ ( 2016). Leaf resorption efficiency in relation to foliar and soil nutrient concentrations and stoichiometry of Cunninghamia lanceolata, with stand development in southern China. Journal of Soils and Sediments, 16, 1448-1459.
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