A review on the effects of nitrogen and phosphorus addition on tree growth and productivity in forest ecosystems

doi:10.17521/cjpe.2019.0176

Abstract

Abstract:

Nitrogen (N) and phosphorus (P) inputs induced by anthropogenic activities and atmospheric N and P deposition have largely increased the availability of soil N and P in terrestrial ecosystems, which have considerably affected terrestrial carbon cycling processes. Tree growth and productivity in forest ecosystems play an important role in global carbon cycling, and determine the magnitude and direction of terrestrial carbon sequestration. Currently, a large number of field manipulation experiments have been conducted to investigate the effects of N and/or P addition on tree growth and forest productivity, but the results from these studies were inconsistent. Such inconsistent results might be affected by multiple factors, including biological, environmental and experimental variables. Here, we reviewed the present research status of the effects of N and P addition on tree growth and forest productivity in forest ecosystems based on three aspects, including the number of publications and experiments with field N and P addition, and the global distributions of these experiments. Then, we summarized the methods for assessing tree growth and forest productivity at ecosystem level in forest ecosystems, including relative growth rate and absolute increment. According to the related results, we reviewed the regulating factors that affect tree growth and productivity, and the potential mechanisms for such factors, including climate, tree size and stand age, plant functional traits (including type of tree-associated mycorrhizal fungi, N-fixation property of trees, and conservative and acquisitive functional traits), plant-microbe interaction, ambient nutrient (i.e., N and P) deposition rate, and experimental variables. Finally, we summarized the current studies, and pointed out five aspects that are urgently needed to provide further insights in future studies, including the physiological mechanism of how tree growth responds to N and P addition, the tradeoff and allocation among growth of various parts of tree under N and P addition, the role of plant functional traits in regulating and predicting the responses of tree growth to N and P addition, how the competition among trees regulates the responses of tree growth to N and P addition, and conducting long-term and coordinated distributed field experiments investigating the effects of N and P addition on tree growth and forest productivity at the global scale.

Key words: nutrient limitation, tree growth, ecosystem productivity, plant functional traits, plant-microbe interaction, nitrogen deposition, phosphorus deposition

FENG Ji-Guang, ZHU Biao. A review on the effects of nitrogen and phosphorus addition on tree growth and productivity in forest ecosystems[J]. Chin J Plant Ecol, 2020, 44(6): 583-597.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2019.0176

https://www.plant-ecology.com/EN/Y2020/V44/I6/583

Figures/Tables 5

Fig. 1 Number of papers and experiments investigating the effects of nitrogen (N) and/or phosphorus (P) addition on tree growth and productivity in forest ecosystems. A, The number of papers in each year and the accumulated number of papers between the year 1970 and 2019. B, The number of experiments with different treatment of nitrogen and phosphorus addition. N represents only N addition in the case study; P represents only P addition in the case study; N, P represent only N and only P addition in the case study; N, P, NP represents only N, only P and N plus P addition in the case study.

Fig. 2 Global distribution of case studies investigating the effects of nitrogen (N) and/or phosphorus (P) addition on tree growth and productivity in forest ecosystems. The horizontal lines in the figure indicate the distribution boundaries of forests in different climatic regions based on latitude, including tropical forest (23.5° S-23.5° N), boreal forest (46°-66° N), and temperate forest (between the tropical and boreal latitudes). N represents only N addition in the case study; P represents only P addition in the case study; N, P represent only N and only P addition in the case study; N, P, NP represents only N, only P and N plus P addition in the case study. This map was drawn using the software ArcGIS 10.2.2.

Table 1 Methods for assessing the effects of nitrogen and/or phosphorus addition on plant growth and productivity

衡量方法 Method	计算公式 Calculation equation	单位 Unit	参考文献 Reference
相对生长速率 Relative growth rate (RGR)	$RGR=\frac{\text{ln}DB{{H}_{{{t}_{2}}}}-\text{ln}DB{{H}_{{{t}_{1}}}}}{{{t}_{2}}-{{t}_{1}}}$	mm·mm^-1·a^-1	Carlson et al., 2008; Alvarez-Clare et al., 2013; Li et al., 2018
	$RGR=\frac{\text{ln}B{{A}_{{{t}_{2}}}}-\text{ln}B{{A}_{{{t}_{1}}}}}{{{t}_{2}}-{{t}_{1}}}$	mm²·mm^-2·a^-1	Tian et al., 2017
	$RGR=\frac{\text{ln}B{{P}_{{{t}_{2}}}}-\text{ln}B{{P}_{{{t}_{1}}}}}{{{t}_{2}}-{{t}_{1}}}$	kg·kg^-1·a^-1	Markewitz et al., 2012
	$RGR=\frac{B{{A}_{{{t}_{2}}}}-B{{A}_{{{t}_{1}}}}\text{ }\!\!~\!\!\text{ }}{\text{B}{{\text{A}}_{{{t}_{1}}}}}$	%	Jiang et al., 2018
绝对增长量 Absolute increment (Δ)	$\Delta =DB{{H}_{{{t}_{2}}}}-DB{{H}_{{{t}_{1}}}}$	mm·a^-1	Noguchi et al., 2013
	$\text{ }\!\!\Delta\!\!\text{ }\!\!~\!\!\text{ }=B{{A}_{{{t}_{2}}}}-B{{A}_{{{t}_{1}}}}$	m²·a^-1	Saarsalmi et al., 2012; Tian et al., 2017
	$\text{ }\!\!\Delta\!\!\text{ }\!\!~\!\!\text{ }=B{{P}_{{{t}_{2}}}}-B{{P}_{{{t}_{1}}}}$	kg·hm^-2·a^-1	Markewitz et al., 2012; Du & Fang, 2014

Table 2 Methods for assessing the effects of nitrogen and/or phosphorus addition on plant growth and productivity

胸径等级 Classes for diameter at breast height (cm)			参考文献 Reference
小树 Small tree	中树 Medium tree	大树 Large tree	参考文献 Reference
3-10	10-20	>20	Fisher et al., 2013; Jiang et al., 2018; Zou et al., 2019
5-10	10-30	>30	Alvarez-Clare et al., 2013; Tian et al., 2017
5-15		>15	Li et al., 2018
10-25		>25	Wright et al., 2018

Fig. 3 Summary diagram for studying the effects of nitrogen and/or phosphorus addition on tree growth and productivity in forest ecosystems. AM, arbuscular mycorrhizal; ECM, ectomycorrhizal.

References 96

[1]	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. DOI URL
[2]	Andersen KM, Corre MD, Turner BL, Dalling JW (2010). Plant-soil associations in a lower montane tropical forest: physiological acclimation and herbivore-mediated responses to nitrogen addition. Functional Ecology, 24, 1171-1180. DOI URL
[3]	Aragão LEOC, Malhi Y, Metcalfe DB, Silva-Espejo JE, Jiménez E, Navarrete D, Almeida S, Costa ACL, Salinas N, Phillips OL, Anderson LO, Alvarez E, Baker TR, Goncalvez PH, Huamán-Ovalle J, Mamani-Solórzano M, Meir P, Monteagudo A, Patiño S, Peñuela MC, Prieto A, Quesada CA, Rozas-Dávila A, Rudas A, Silva Jr JA, Vásquez R (2009). Above- and below-ground net primary productivity across ten Amazonian forests on contrasting soils. Biogeosciences, 6, 2759-2778. DOI URL
[4]	Averill C, Dietze MC, Bhatnagar JM (2018). Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks. Global Change Biology, 24, 4544-4553. DOI URL PMID
[5]	Báez S, Homeier J (2018). Functional traits determine tree growth and ecosystem productivity of a tropical montane forest: insights from a long-term nutrient manipulation experiment. Global Change Biology, 24, 399-409. DOI URL PMID
[6]	Bardgett RD, Mommer L, de Vries FT (2014). Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution, 29, 692-699. DOI URL PMID
[7]	BassiriRad H, Lussenhop JF, Sehtiya HL, Borden KK (2015). Nitrogen deposition potentially contributes to oak regeneration failure in the Midwestern temperate forests of the USA. Oecologia, 177, 53-63. DOI URL PMID
[8]	Borer ET, Harpole WS, Adler PB, Lind EM, Orrock JL, Seabloom EW, Smith MD (2014). Finding generality in ecology: a model for globally distributed experiments. Methods in Ecology and Evolution, 5, 65-73. DOI URL
[9]	Braun S, Schindler C, Rihm B (2017). Growth trends of beech and Norway spruce in Switzerland: the role of nitrogen deposition, ozone, mineral nutrition and climate. Science of the Total Environment, 599-600, 637-646.
[10]	Camarero JJ, Carrer M (2017). Bridging long-term wood functioning and nitrogen deposition to better understand changes in tree growth and forest productivity. Tree Physiology, 37, 1-3. DOI URL PMID
[11]	Čapek P, Manzoni S, Kaštovská E, Wild B, Diáková K, Bárta J, Schnecker J, Biasi C, Martikainen PJ, Alves RJE, Guggenberger G, Gentsch N, Hugelius G, Palmtag J, Mikutta R, Shibistova O, Urich T, Schleper C, Richter A, Šantrůčková H (2018). A plant-microbe interaction framework explaining nutrient effects on primary production. Nature Ecology & Evolution, 2, 1588-1596. DOI URL PMID
[12]	Carlson CA, Burkhart HE, Lee Allen H, Fox TR (2008). Absolute and relative changes in tree growth rates and changes to the stand diameter distribution of Pinus taeda as a result of midrotation fertilizer applications. Canadian Journal of Forest Research, 38, 2063-2071. DOI URL
[13]	Chalot M, Brun A (1998). Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiology Reviews, 22, 21-44. DOI URL PMID
[14]	Chapin III FS, Vitousek PM, van Cleve K (1986). The nature of nutrient limitation in plant communities. The American Naturalist, 127, 48-58. DOI URL
[15]	Chen D, Li J, Lan Z, Hu S, Bai Y (2016). Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment. Functional Ecology, 30, 658-669. DOI URL
[16]	Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, von Fischer JC, Elseroad A, Wasson MF (1999). Global patterns of terrestrial biological nitrogen (N₂) fixation in natural ecosystems. Global Biogeochemical Cycles, 13, 623-645. DOI URL
[17]	Coley PD, Bryant JP, Chapin III FS (1985). Resource availability and plant antiherbivore defense. Science, 230, 895-899. DOI URL PMID
[18]	Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003). A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany, 51, 335-380. DOI URL
[19]	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. DOI URL
[20]	Dai Z, Su W, Chen H, Barberán A, Zhao H, Yu M, Yu L, Brookes PC, Schadt CW, Chang SX, Xu J (2018). Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro-ecosystems across the globe. Global Change Biology, 24, 3452-3461. DOI URL PMID
[21]	DeForest JL, Snell RS (2020). Tree growth response to shifting soil nutrient economy depends on mycorrhizal associations. New Phytologist, 225, 2557-2566. DOI URL PMID
[22]	Deng M, Liu L, Jiang L, Liu W, Wang X, Li S, Yang S, Wang B (2018). Ecosystem scale trade-off in nitrogen acquisition pathways. Nature Ecology & Evolution, 2, 1724-1734. DOI URL PMID
[23]	Du E, Fang J (2014). Weak growth response to nitrogen deposition in an old-growth boreal forest. Ecosphere, 5, 109. DOI: 10.1890/es14-00109.1.
[24]	Du EZ, Terrer C, Pellegrini AFA, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu XH, Jackson RB (2020). Global patterns of terrestrial nitrogen and phosphorus limitation. Nature Geoscience, 13, 221-226. DOI URL
[25]	Dynarski KA, Houlton BZ (2018). Nutrient limitation of terrestrial free-living nitrogen fixation. New Phytologist, 217, 1050-1061. DOI URL PMID
[26]	Elser JJ, Bracken MES, 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. DOI URL PMID
[27]	Feng JG, Zhu B (2019). A global meta-analysis of soil respiration and its components in response to phosphorus addition. Soil Biology & Biochemistry, 135, 38-47. DOI URL
[28]	Fisher JB, Malhi Y, Torres IC, Metcalfe DB, van de Weg MJ, Meir P, Silva-Espejo JE, Huasco WH (2013). Nutrient limitation in rainforests and cloud forests along a 3000-m elevation gradient in the Peruvian Andes. Oecologia, 172, 889-902. DOI URL
[29]	Fleischer K, Rebel KT, van der Molen MK, Erisman JW, Wassen MJ, van Loon EE, Montagnani L, Gough CM, Herbst M, Janssens IA, Gianelle D, Dolman AJ (2013). The contribution of nitrogen deposition to the photosynthetic capacity of forests. Global Biogeochemical Cycles, 27, 187-199. DOI URL
[30]	Goswami S, Fisk MC, Vadeboncoeur MA, Garrison-Johnston M, Yanai RD, Fahey TJ (2018). Phosphorus limitation of aboveground production in northern hardwood forests. Ecology, 99, 438-449. DOI URL PMID
[31]	Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011). Nutrient co-limitation of primary producer communities. Ecology Letters, 14, 852-862. DOI URL
[32]	He NP, Zhang JH, Liu CC, Xu L, Chen Z, Liu Y, Wang RL, Zhao N, Xu ZW, Tian J, Wang Q, Zhu JX, Li Y, Hou JH, Yu GR (2018). Patterns and influencing factors of traits in forest ecosystems: synthesis and perspectives on the synthetic investigation from the north-east transect of eastern China (NETEC). Acta Ecologica Sinica, 38, 6359-6382.
	[ 何念鹏, 张佳慧, 刘聪聪, 徐丽, 陈智, 刘远, 王瑞丽, 赵宁, 徐志伟, 田静, 王情, 朱剑兴, 李颖, 侯继华, 于贵瑞 (2018). 森林生态系统性状的空间格局与影响因素研究进展——基于中国东部样带的整合分析. 生态学报, 38, 6359-6382.]
[33]	Hedin LO (2004). Global organization of terrestrial plant- nutrient interactions. Proceedings of the National Academy of Sciences of the United States of America, 101, 10849-10850. DOI URL PMID
[34]	Herbert DA, Fownes JH (1995). Phosphorus limitation of forest leaf-area and net primary production on a highly weathered soil. Biogeochemistry, 29, 223-235.
[35]	Högberg P, Fan H, Quist M, Binkley D, Tamm CO (2006). Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Global Change Biology, 12, 489-499.
[36]	Hopmans P, Elms SR (2013). Impact of defoliation by Essigella californica on the growth of mature Pinus radiata and response to N, P and S fertilizer. Forest Ecology and Management, 289, 190-200.
[37]	Hou EQ, Luo YQ, Kuang YW, Chen CR, Lu XK, Jiang LF, Luo XZ, Wen DZ (2020). Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. Nature Communications, 11, 637. DOI: 10.1038/s41467-020-14492-w. URL PMID
[38]	Houlton BZ, Wang YP, Vitousek PM, Field CB (2008). A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature, 454, 327-334. DOI URL PMID
[39]	Ibáñez I, Zak DR, Burton AJ, Pregitzer KS (2016). Chronic nitrogen deposition alters tree allometric relationships: implications for biomass production and carbon storage. Ecological Applications, 26, 913-925. DOI URL PMID
[40]	Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G, Papale D, Piao SL, Schulze ED, Tang J, Law BE (2010). Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience, 3, 315-322.
[41]	Jiang J, Wang Y, Yang Y, Yu M, Wang C, Yan J (2019) Interactive effects of nitrogen and phosphorus additions on plant growth vary with ecosystem type. Plant and Soil, 440, 523-537.
[42]	Jiang L, Tian D, Ma S, Zhou X, Xu L, Zhu J, Jing X, Zheng C, Shen H, Zhou Z, Li Y, Zhu B, Fang J (2018). The response of tree growth to nitrogen and phosphorus additions in a tropical montane rainforest. Science of the Total Environment, 618, 1064-1070.
[43]	LeBauer DS, Treseder KK (2008). Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology, 89, 371-379. DOI URL PMID
[44]	Li Y, Niu S, Yu G (2016). Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis. Global Change Biology, 22, 934-943. DOI URL PMID
[45]	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, 95-105.
[46]	Liu XY, Du EZ, Xu LC, Shen HH, Fang JY, Hu HF (2015). Response of tree growth to nitrogen addition in aLarix gmelinii primitive forest. Chinese Journal of Plant Ecology, 39, 433-441.
	[ 刘修元, 杜恩在, 徐龙超, 沈海花, 方精云, 胡会峰 (2015). 落叶松原始林树木生长对氮添加的响应. 植物生态学报, 39, 433-441.]
[47]	Lu M, Yang Y, Luo Y, Fang C, Zhou X, Chen J, Yang X, Li B (2011a). Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis. New Phytologist, 189, 1040-1050. DOI URL PMID
[48]	Lu M, Zhou X, Luo Y, Yang Y, Fang C, Chen J, Li B (2011b). Minor stimulation of soil carbon storage by nitrogen addition: a meta-analysis. Agriculture, Ecosystems & Environment, 140, 234-244.
[49]	Lu X, Vitousek PM, Mao Q, Gilliam FS, Luo Y, Zhou G, Zou X, Bai E, Scanlon TM, Hou E, Mo J (2018). Plant acclimation to long-term high nitrogen deposition in an N-rich tropical forest. Proceedings of the National Academy of Sciences of the United States of America, 115, 5187-5192. DOI URL PMID
[50]	Lu XK, Mo JM, Zhang W, Mao QG, Liu RZ, Wang C, Wang SH, Zheng MH, Mori T, Mao JH, Zhang YQ, Wang YF, Huang J (2019). Effects of simulated atmospheric nitrogen deposition on forest ecosystems in China: an overview. Journal of Tropical and Subtropical Botany, 27, 500-522.
	[ 鲁显楷, 莫江明, 张炜, 毛庆功, 刘荣臻, 王聪, 王森浩, 郑棉海, Mori T, 毛晋花, 张勇群, 王玉芳, 黄娟 (2019). 模拟大气氮沉降对中国森林生态系统影响的研究进展. 热带亚热带植物学报, 27, 500-522.]
[51]	Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004). Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience, 54, 731-739. DOI URL
[52]	Magnani F, Mencuccini M, Borghetti M, Berbigier P, Berninger F, Delzon S, Grelle A, Hari P, Jarvis PG, Kolari P, Kowalski AS, Lankreijer H, Law BE, Lindroth A, Loustau D, Manca G, Moncrieff JB, Rayment M, Tedeschi V, Valentini R, Grace J (2007). The human footprint in the carbon cycle of temperate and boreal forests. Nature, 447, 848-850. DOI URL PMID
[53]	Mainwaring DB, Maguire DA, Perakis SS (2014). Three-year growth response of young Douglas-fir to nitrogen, calcium, phosphorus, and blended fertilizers in Oregon and Washington. Forest Ecology and Management, 327, 178-188.
[54]	Mao HR, Jin GZ (2017). Impacts of nitrogen addition on net primary productivity in the typical mixed broadleaved-‌Korean pine forest. Journal of Beijing Forestry University, 39(8), 42-49.
	[ 毛宏蕊, 金光泽 (2017). 氮添加对典型阔叶红松林净初级生产力的影响. 北京林业大学学报, 39(8), 42-49.]
[55]	Markewitz D, Figueiredo RdO, de Carvalho CJR, Davidson EA (2012). Soil and tree response to P fertilization in a secondary tropical forest supported by an Oxisol. Biology and Fertility of Soils, 48, 665-678.
[56]	Marklein AR, Houlton BZ (2012). Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytologist, 193, 696-704. DOI URL PMID
[57]	McGrath JF, Copeland B, Dumbrell IC (2003). Magnitude and duration of growth and wood quality responses to phosphorus and nitrogen in thinned Pinus radiata in southern Western Australia. Australian Forestry, 66, 223-230.
[58]	Nasto MK, Alvarez-Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC (2014). Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecology Letters, 17, 1282-1289. URL PMID
[59]	Nasto MK, Winter K, Turner BL, Cleveland CC (2019). Nutrient acquisition strategies augment growth in tropical N₂-fixing trees in nutrient-poor soil and under elevated CO₂. Ecology, 100, e02646. DOI: 10.1002/ecy.2646. DOI URL PMID
[60]	Noguchi K, Nagakura J, Konôpka B, Sakata T, Kaneko S, Takahashi M (2013). Fine-root dynamics in sugi (Cryptomeria japonica) under manipulated soil nitrogen conditions. Plant and Soil, 364, 159-169.
[61]	Norby RJ, de Kauwe MG, Domingues TF, Duursma RA, Ellsworth DS, Goll DS, Lapola DM, Luus KA, MacKenzie AR, Medlyn BE, Pavlick R, Rammig A, Smith B, Thomas R, Thonicke K, Walker AP, Yang X, Zaehle S (2016). Model-data synthesis for the next generation of forest free-air CO₂ enrichment (FACE) experiments. New Phytologist, 209, 17-28. DOI URL PMID
[62]	Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG, Ciais P, Jackson RB, Pacala SW, McGuire AD, Piao S, Rautiainen A, Sitch S, Hayes D (2011). A large and persistent carbon sink in the worldʼs forests. Science, 333, 988-993. DOI URL PMID
[63]	Peng YF, Guo DL, Yang YH (2017). Global patterns of root dynamics under nitrogen enrichment. Global Ecology and Biogeography, 26, 102-114.
[64]	Peng YF, Yang YH (2016). Allometric biomass partitioning under nitrogen enrichment: evidence from manipulative experiments around the world. Scientific Reports, 6, 28918. DOI: 10.1038/srep28918. DOI URL PMID
[65]	Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013). Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4, 2934. DOI: 10.1038/ncomms3934. DOI URL PMID
[66]	Rappe-George MO, Gärdenäs AI, Kleja DB (2013). The impact of four decades of annual nitrogen addition on dissolved organic matter in a boreal forest soil. Biogeosciences, 10, 1365-1377.
[67]	Reich PB, Hungate BA, Luo Y (2006). Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annual Review of Ecology, Evolution, and Systematics, 37, 611-636.
[68]	Rosling A, Midgley MG, Cheeke T, Urbina H, Fransson P, Phillips RP (2016). Phosphorus cycling in deciduous forest soil differs between stands dominated by ecto- and arbuscular mycorrhizal trees. New Phytologist, 209, 1184-1195. DOI URL PMID
[69]	Saarsalmi A, Smolander A, Kukkola M, Moilanen M, Saramäki J (2012). 30-year effects of wood ash and nitrogen fertilization on soil chemical properties, soil microbial processes and stand growth in a Scots pine stand. Forest Ecology and Management, 278, 63-70.
[70]	Schulte-Uebbing L, de Vries W (2018). Global-scale impacts of nitrogen deposition on tree carbon sequestration in tropical, temperate, and boreal forests: a meta-analysis. Global Change Biology, 24, 416-431.
[71]	Talbot JM, Allison SD, Treseder KK (2008). Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Functional Ecology, 22, 955-963.
[72]	Taylor BN, Menge DNL (2018). Light regulates tropical symbiotic nitrogen fixation more strongly than soil nitrogen. Nature Plants, 4, 655-661. DOI URL PMID
[73]	Thomas RQ, Canham CD, Weathers KC, Goodale CL (2010). Increased tree carbon storage in response to nitrogen deposition in the US. Nature Geoscience, 3, 13-17.
[74]	Tian D, Li P, Fang W, Xu J, Luo Y, Yan Z, Zhu B, Wang J, Xu X, Fang J (2017). Growth responses of trees and understory plants to nitrogen fertilization in a subtropical forest in China. Biogeosciences, 14, 3461-3469.
[75]	Tian D, Niu S (2015). A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters, 10, 024019. DOI: 10.1088/1748-9326/10/2/024019.
[76]	Tian D, Wang H, Sun J, Niu S (2016). Global evidence on nitrogen saturation of terrestrial ecosystem net primary productivity. Environmental Research Letters, 11, 024012. DOI: 10.1088/1748-9326/11/2/024012.
[77]	Vadeboncoeur MA (2010). Meta-analysis of fertilization experiments indicates multiple limiting nutrients in northeastern deciduous forests. Canadian Journal of Forest Research, 40, 1766-1780.
[78]	Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007). Let the concept of trait be functional! Oikos, 116, 882-892. DOI URL
[79]	Vitousek PM (1984). Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology, 65, 285-298. DOI URL
[80]	Vitousek PM, Farrington H (1997). Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry, 37, 63-75.
[81]	Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010). Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications, 20, 5-15. DOI URL PMID
[82]	Vitousek PM, Walker LR, Whiteaker LD, Matson PA (1993). Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry, 23, 197-215.
[83]	Walker TW, Syers JK (1976). The fate of phosphorus during pedogenesis. Geoderma, 15, 1-19.
[84]	Waring BG, Pérez-Aviles D, Murray JG, Powers JS (2019). Plant community responses to stand-level nutrient fertilization in a secondary tropical dry forest. Ecology, 100, e02691. DOI: 10.1002/ecy.2691. DOI URL PMID
[85]	Wieder WR, Cleveland CC, Kolby Smith W, Todd-Brown K (2015). Future productivity and carbon storage limited by terrestrial nutrient availability. Nature Geoscience, 8, 441-444.
[86]	Wooliver RC, Marion ZH, Peterson CR, Potts BM, Senior JK, Bailey JK, Schweitzer JA (2017). Phylogeny is a powerful tool for predicting plant biomass responses to nitrogen enrichment. Ecology, 98, 2120-2132. DOI URL PMID
[87]	Wright SJ (2019). Plant responses to nutrient addition experiments conducted in tropical forests. Ecological Monographs, 89, e01382. DOI: 10.1002/ecm.1382.
[88]	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, 1129-1138. DOI URL PMID
[89]	Xu XF, Thornton PE, Post WM (2013). A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Global Ecology and Biogeography, 22, 737-749.
[90]	Yuan ZY, Chen HYH (2012). A global analysis of fine root production as affected by soil nitrogen and phosphorus. Proceedings of the Royal Society B, 279, 3796-3802. DOI URL PMID
[91]	Yue K, Fornara DA, Yang W, Peng Y, Peng C, Liu Z, Wu F (2017). Influence of multiple global change drivers on terrestrial carbon storage: additive effects are common. Ecology Letters, 20, 663-672. DOI URL PMID
[92]	Zhao Q, Zeng DH (2019). Nitrogen addition effects on tree growth and soil properties mediated by soil phosphorus availability and tree species identity. Forest Ecology and Management, 449, 117478. DOI: 10.1016/j.foreco.2019.117478.
[93]	Zheng M, Zhou Z, Luo Y, Zhao P, Mo J (2019). Global pattern and controls of biological nitrogen fixation under nutrient enrichment: a meta-analysis. Global Change Biology, 25, 3018-3030. DOI URL PMID
[94]	Zhou XL, Cai Q, Xiong XY, Fang WJ, Zhu JX, Zhu JL, Fang JY, Ji CJ (2018). Ecosystem carbon stock and within-‌system distribution in successionalFagus lucida forests in Mt. Yueliang, Guizhou, China. Chinese Journal of Plant Ecology, 42, 703-712.
	[ 周序力, 蔡琼, 熊心雨, 方文静, 朱剑霄, 朱江玲, 方精云, 吉成均 (2018). 贵州月亮山不同演替阶段亮叶水青冈林碳储量及其分配格局. 植物生态学报, 42, 703-712.]
[95]	Zhu F, Lu X, Mo J (2014). Phosphorus limitation on photosynthesis of two dominant understory species in a lowland tropical forest. Journal of Plant Ecology, 7, 526-534.
[96]	Zou AL, Li XP, Ni XF, Ji CJ (2019). Responses of tree growth to nitrogen addition inQuercus wutaishanica forests in Mt. Dongling, Beijing, China. Chinese Journal of Plant Ecology, 43, 783-792.
	[ 邹安龙, 李修平, 倪晓凤, 吉成均 (2019). 模拟氮沉降对北京东灵山辽东栎林树木生长的影响. 植物生态学报, 43, 783-792.]