Applications of nitrogen stable isotope techniques in the study of nitrogen cycling in terrestrial ecosystems

doi:10.17521/cjpe.2019.0249

Abstract

Abstract:

In the past several decades, the development of nitrogen (N) stable isotope techniques has improved the understanding of N cycling in terrestrial ecosystems. This review briefly introduced the history of N stable isotope techniques in studying N cycling in terrestrial ecosystems and summarized typical studies focusing on different aspects of ecosystem N cycling in recent years, including using 1) ¹⁵N natural abundance to identify plant N sources, indicate N status of ecosystems, and quantify N transformation rates; 2) ¹⁵N enriched tracers to study N fates, redistribution and gaseous loss from ecosystems. In the end, this review points out challenges and future applications of N stable isotope techniques on studying N cycling in terrestrial ecosystems.

Key words: nitrogen stable isotope technique, natural abundance technique, ¹⁵N labelling technique

FANG Yun-Ting, LIU Dong-Wei, ZHU Fei-Fei, TU Ying, LI Shan-Long, HUANG Shao-Nan, QUAN Zhi, WANG Ang. Applications of nitrogen stable isotope techniques in the study of nitrogen cycling in terrestrial ecosystems[J]. Chin J Plant Ecol, 2020, 44(4): 373-383.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2019.0249

https://www.plant-ecology.com/EN/Y2020/V44/I4/373

Figures/Tables 1

References 96

[1]	Ackerman D, Millet DB, Chen X (2019). Global estimates of inorganic nitrogen deposition across four decades. Global Biogeochemical Cycles, 33, 100-107. DOI URL
[2]	Bai E, Houlton BZ (2009). Coupled isotopic and process-based modeling of gaseous nitrogen losses from tropical rain forests. Global Biogeochemical Cycles, 23, GB2011. DOI: 10.1029/2008gb003361.
[3]	Bai E, Houlton BZ, Wang YP (2012). Isotopic identification of nitrogen hotspots across natural terrestrial ecosystems. BiogeoSciences, 9, 3287-3304. DOI URL
[4]	Blesh J, Drinkwater LE (2014). Retention of ¹⁵N-labeled fertilizer in an Illinois prairie soil with winter rye . Soil Science Society of America Journal, 78, 496-508. DOI URL
[5]	Brunner B, Contreras S, Lehmann MF, Matantseva O, Rollog M, Kalvelage T, Klockgether G, Lavik G, Jetten MSM, Kartal B, Kuypers MMM (2013). Nitrogen isotope effects induced by anammox bacteria. Proceedings of the National Academy of Sciences of the United States of America, 110, 18994-18999. URL PMID
[6]	Burke IC, O’Deen LA, Mosier AR, Porter LK (1990). Diffusion of soil extracts for nitrogen and nitrogen-15 analyses by automated combustion/mass spectrometry. Soil Science Society of America Journal, 54, 1190-1192. DOI URL
[7]	Chalk PM, Craswell ET, Polidoro JC, Chen DL (2015). Fate and efficiency of ¹⁵N-labelled slow- and controlled-release fertilizers . Nutrient Cycling in Agroecosystems, 102, 167-178. DOI URL
[8]	Chen ZM, Wang HY, Liu XW, Lu DJ, Zhou JM (2016). The fates of ¹⁵N-labeled fertilizer in a wheat-soil system as influenced by fertilization practice in a loamy soil . Scientific Reports, 6, 34754. DOI: 10.1038/srep34754. URL PMID
[9]	Coyle JS, Dijkstra P, Doucett RR, Schwartz E, Hart SC, Hungate BA (2009). Relationships between C and N availability, substrate age, and natural abundance ¹³C and ¹⁵N signatures of soil microbial biomass in a semiarid climate . Soil Biology & Biochemistry, 41, 1605-1611.
[10]	Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Peñuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009). Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytologist, 183, 980-992. URL PMID
[11]	Craine JM, Elmore AJ, Wang LX, Aranibar J, Bauters M, Boeckx P, Crowley BE, Dawes MA, Delzon S, Fajardo A, Fang YT, Fujiyoshi L, Gray A, Guerrieri R, Gundale MJ, Hawke DJ, Hietz P, Jonard M, Kearsley E, Kenzo T, Makarov M, Marañón-Jiménez S, McGlynn TP, McNeil BE, Mosher SG, Nelson DM, Peri PL, Roggy JC, Sanders- Demott R, Song MH, Szpak P, Templer PH, van der Colff D, Werner C, Xu XL, Yang Y, Yu GR, Zmudczyńska- Skarbek K (2018). Isotopic evidence for oligotrophication of terrestrial ecosystems. Nature Ecology & Evolution, 2, 1735-1744. URL PMID
[12]	Craine JM, Elmore AJ, Wang LX, Augusto L, Baisden WT, Brookshire ENJ, Cramer MD, Hasselquist NJ, Hobbie EA, Kahmen A, Koba K, Kranabetter JM, Mack MC, Marin-Spiotta E, Mayor JR, McLauchlan KK, Michelsen A, Nardoto GB, Oliveira RS, Perakis SS, Peri PL, Quesada CA, Richter A, Schipper LA, Stevenson BA, Turner BL, Viani RAG, Wanek W, Zeller B (2015). Convergence of soil nitrogen isotopes across global climate gradients. Scientific Reports, 5, 8280. DOI: 10.1038/srep08280. DOI URL PMID
[13]	de Oliveira SM, de Almeida REM, Ciampitti IA, Pierozan Junior C, Lago BC, Trivelin PCO, Favarin JL (2018). Understanding N timing in corn yield and fertilizer N recovery: an insight from an isotopic labeled-N determination. PLOS ONE, 13, e0192776. DOI: 10.1371/journal.pone.0192776. URL PMID
[14]	Denk TRA, Mohn J, Decock C, Lewicka-Szczebak D, Harris E, Butterbach-Bahl K, Kiese R, Wolf B (2017). The nitrogen cycle: a review of isotope effects and isotope modeling approaches. Soil Biology & Biochemistry, 105, 121-137. DOI URL
[15]	Dijkstra P, Ishizu A, Doucett R, Hart SC, Schwartz E, Menyailo OV, Hungate BA (2006). ¹³C and ¹⁵N natural abundance of the soil microbial biomass . Soil Biology & Biochemistry, 38, 3257-3266. DOI URL
[16]	Ding LJ, An XL, Li S, Zhang GL, Zhu YG (2014). Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environmental Science & Technology, 48, 10641-10647. DOI URL PMID
[17]	Fang YT, Koba K, Makabe A, Takahashi C, Zhu WX, Hayashi T, Hokari AA, Urakawa R, Bai E, Houlton BZ, Xi D, Zhang SS, Matsushita K, Tu Y, Liu DW, Zhu FF, Wang ZY, Zhou GY, Chen DX, Makita T, Toda H, Liu XY, Chen QS, Zhang DQ, Li YD, Yoh M (2015). Microbial denitrification dominates nitrate losses from forest ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 112, 1470-1474. URL PMID
[18]	Feng Z, Brumme R, Xu YJ, Lamersdorf N (2008). Tracing the fate of mineral N compounds under high ambient N deposition in a Norway spruce forest at Solling/Germany. Forest Ecology and Management, 255, 2061-2073. DOI URL
[19]	Fry B (2006). Stable Isotope Ecology. Springer, New York.
[20]	Gabriel JL, Alonso-Ayuso M, García-González I, Hontoria C, Quemada M (2016). Nitrogen use efficiency and fertiliser fate in a long-term experiment with winter cover crops. European Journal of Agronomy, 79, 14-22.
[21]	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, Vörösmarty CJ (2004). Nitrogen cycles: past, present, and future. Biogeochemistry, 70, 153-226. DOI URL
[22]	Gardner JB, Drinkwater LE (2009). The fate of nitrogen in grain cropping systems: a meta-analysis of ¹⁵N field experiments . Ecological Applications, 19, 2167-2184. DOI URL PMID
[23]	Goodale CL (2017). Multiyear fate of a ¹⁵N tracer in a mixed deciduous forest: retention, redistribution, and differences by mycorrhizal association . Global Change Biology, 23, 867-880. DOI URL PMID
[24]	Groffman PM, Altabet MA, Böhlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP, Voytek MA (2006). Methods for measuring denitrification: diverse approaches to a difficult problem. Ecological Applications, 16, 2091-2122. DOI URL PMID
[25]	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 . Global Change Biology, 22, 3608-3620. URL PMID
[26]	Hastings MG (2010). Evaluating source, chemistry and climate change based upon the isotopic composition of nitrate in ice cores. IOP Conference Series: Earth and Environmental Science, 9, 012002. DOI: 10.1088/1755-1315/9/1/012002. DOI URL
[27]	He HB, Lü H, Zhang W, Hou SM, Zhang XD (2011). A liquid chromatographic/mass spectrometric method to evaluate ¹³C and ¹⁵N incorporation into soil amino acids . Journal of Soils and Sediments, 11, 731-740. DOI URL
[28]	He HB, Xie HT, Zhang XD (2006). A novel GC/MS technique to assess ¹⁵N and ¹³C incorporation into soil amino sugars . Soil Biology & Biochemistry, 38, 1083-1091. DOI URL
[29]	Hietz P, Turner BL, Wanek W, Richter A, Nock CA, Wright SJ (2011). Long-term change in the nitrogen cycle of tropical forests. Science, 334, 664-666. DOI URL PMID
[30]	Hoering T (1955). Variations of nitrogen-15 abundance in naturally occurring substances. Science, 122, 1233-1234. URL PMID
[31]	Houlton BZ, Bai E (2009). Imprint of denitrifying bacteria on the global terrestrial biosphere. Proceedings of the National Academy of Sciences of the United States of America, 106, 21713-21716. URL PMID
[32]	Houlton BZ, Marklein AR, Bai E (2015). Representation of nitrogen in climate change forecasts. Nature Climate Change, 5, 398-401. DOI URL
[33]	Houlton BZ, Sigman DM, Hedin LO (2006). Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proceedings of the National Academy of Sciences of the United States of America, 103, 8745-8750. URL PMID
[34]	Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007). A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proceedings of the National Academy of Sciences of the United States of America, 104, 8902-8906. URL PMID
[35]	Huang SN, Elliott EM, Felix JD, Pan YP, Liu DW, Li SL, Li ZJ, Zhu FF, Zhang N, Fu PQ, Fang YT (2019). Seasonal pattern of ammonium ¹⁵N natural abundance in precipitation at a rural forested site and implications for NH₃ source partitioning . Environmental Pollutant, 247, 541-549.
[36]	Ju XT (2014). The concept and meanings of nitrogen fertilizer availability ratio—Discussing misunderstanding of traditional nitrogen use efficiency. Acta Pedologica Sinica, 51, 921-933.
	[ 巨晓棠 (2014). 氮肥有效性的概念和意义——兼论对传统氮肥利用率的理解误区. 土壤学报, 51, 921-933.]
[37]	Ju XT, Christie P (2011). Calculation of theoretical nitrogen rate for simple nitrogen recommendations in intensive cropping systems: a case study on the North China Plain. Field Crops Research, 124, 450-458. DOI URL
[38]	Koba K, Inagaki K, Sasaki Y, Takebayashi Y, Yoh M (2010). Nitrogen isotopic analysis of dissolved inorganic and organic nitrogen in soil extracts//Ohkouchi N, Tayasu I, Koba K. Earth, Life and Isotopes. Kyoto University Press, Kyoto, Japan. 17-36.
[39]	Kool DM, Dolfing J, Wrage N, van Groenigen JW (2011). Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biology & Biochemistry, 43, 174-178. DOI URL
[40]	Krause K, Providoli I, Currie WS, Bugmann H, Schleppi P (2012). Long-term tracing of whole catchment ¹⁵N additions in a mountain spruce forest: measurements and simulations with the TRACE model . Trees, 26, 1683-1702. DOI URL
[41]	Ladha JK, Pathak H, Krupnik TJ, Six J, van Kessel C (2005). Efficiency of fertilizer nitrogen in cereal production: retrospects and prospects. Advances in Agronomy, 87, 85-156.
[42]	LeBauer DS, Treseder KK (2008). Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology, 89, 371-379. URL PMID
[43]	Li SL, Gurmesa GA, Zhu WX, Gundersen P, Zhang SS, Xi D, Huang SN, Wang A, Zhu FF, Jiang Y, Zhu JJ, Fang YT (2019). Fate of atmospherically deposited NH₄⁺ and NO₃^- in two temperate forests in China: temporal pattern and redistribution. Ecological Applications, 29, e01920. DOI: 10.1002/eap.1920. DOI URL PMID
[44]	Liang B, Zhao W, Yang XY, Zhou JB (2013). Fate of nitrogen- 15 as influenced by soil and nutrient management history in a 19-year wheat-maize experiment. Field Crops Research, 144, 126-134. DOI URL
[45]	Lin GH (2013). Stable Isotope Ecology. Higher Education Press, Beijing. 71.
	[ 林光辉 (2013). 稳定同位素生态学. 高等教育出版社, 北京. 71.]
[46]	Liu DW, Tu Y, Fang YT (2017). Isotope analysis of ammonium and nitrate: a review on measured methods and their application. Chinese Journal of Applied Ecology, 28, 2353-2360. URL PMID
	[ 刘冬伟, 图影, 方运霆 (2017). 铵盐和硝酸盐稳定同位素丰度测定方法及其应用案例. 应用生态学报, 28, 2353-2360.] URL PMID
[47]	Liu DW, Zhu WX, Wang XB, Pan YP, Wang C, Xi D, Bai E, Wang YS, Han XG, Fang YT (2017a). Abiotic versus biotic controls on soil nitrogen cycling in drylands along a 3200 km transect. Biogeosciences, 14, 989-1001. DOI URL
[48]	Liu J, Peng B, Xia ZW, Sun JF, Gao DC, Dai WW, Jiang P, Bai E (2017b). Different fates of deposited NH₄⁺and NO₃^- in a temperate forest in northeast China: a ¹⁵N tracer study. Global Change Biology, 23, 2441-2449. DOI URL PMID
[49]	Liu WJ, Yu LF, Zhang T, Kang RH, Zhu J, Mulder J, Huang YM, Duan L (2017c). In situ ¹⁵N labeling experiment reveals different long-term responses to ammonium and nitrate inputs in N-saturated subtropical forest. Journal of Geophysical Research, 122, 2251-2264.
[50]	Liu XE, Li XG, Guo RY, Kuzyakov Y, Li FM (2015). The effect of plastic mulch on the fate of urea-N in rain-fed maize production in a semiarid environment as assessed by ¹⁵N-labeling . European Journal of Agronomy, 70, 71-77. DOI URL
[51]	Liu XY, Koba K, Koyama LA, Hobbie SE, Weiss MS, Inagaki Y, Shaver GR, Giblin AE, Hobara S, Nadelhoffer KJ, Sommerkorn M, Rastetter EB, Kling GW, Laundre JA, Yano Y, Makabe A, Yano M, Liu CQ (2018). Nitrate is an important nitrogen source for Arctic tundra plants. Proceedings of the National Academy of Sciences of the United States of America, 115, 3398-3403. DOI URL PMID
[52]	Mary B, Recous S, Robin D (1998). A model for calculating nitrogen fluxes in soil using ¹⁵N tracing . Soil Biology & Biochemistry, 30, 1963-1979. DOI URL
[53]	Mayor JR, Schuur EAG, Mack MC, Hollingsworth TN, Bååth E (2012). Nitrogen isotope patterns in Alaskan black spruce reflect organic nitrogen sources and the activity of ectomycorrhizal fungi. Ecosystems, 15, 819-831. DOI URL
[54]	McIlvin MR, Altabet MA (2005). Chemical conversion of nitrate and nitrite to nitrous oxide for nitrogen and oxygen isotopic analysis in freshwater and seawater. Analytical Chemistry, 77, 5589-5595. DOI URL PMID
[55]	McLauchlan KK, Craine JM, Oswald WW, Leavitt PR, Likens GE (2007). Changes in nitrogen cycling during the past century in a northern hardwood forest. Proceedings of the National Academy of Sciences of the United States of America, 104, 7466-7470. DOI URL PMID
[56]	McLauchlan KK, Ferguson CJ, Wilson IE, Ocheltree TW, Craine JM (2010). Thirteen decades of foliar isotopes indicate declining nitrogen availability in central North American grasslands. New Phytologist, 187, 1135-1145. URL PMID
[57]	McLauchlan KK, Gerhart LM, Battles JJ, Craine JM, Elmore AJ, Higuera PE, Mack MC, McNeil BE, Nelson DM, Pederson N, Perakis SS (2017). Centennial-scale reductions in nitrogen availability in temperate forests of the United States. Scientific Report, 7, 7856. DOI: 10.1038/s41598-017-08170-z.
[58]	Michener R, Lajtha AK (2007). Stable Isotopes in Ecology and Environmental Science. Blackwell Publications, Oxford.
[59]	Möbius J (2013). Isotope fractionation during nitrogen remineralization (ammonification): implications for nitrogen isotope biogeochemistry. Geochimica et Cosmochimica Acta, 105, 422-432. DOI URL
[60]	Müller C, Laughlin RJ, Spott O, Rütting T (2014). Quantification of N₂O emission pathways via a ¹⁵N tracing model . Soil Biology & Biochemistry, 72, 44-54. DOI URL
[61]	Müller C, Rütting T, Kattge J, Laughlin RJ, Stevens RJ (2007). Estimation of parameters in complex ¹⁵N tracing models by Monte Carlo sampling . Soil Biology & Biochemistry, 39, 715-726. DOI URL
[62]	Murphy RP, Montes-Molina JA, Govaerts B, Six J, van Kessel C, Fonte SJ (2016). Crop residue retention enhances soil properties and nitrogen cycling in smallholder maize systems of Chiapas, Mexico. Applied Soil Ecology, 103, 110-116. DOI URL
[63]	Nadelhoffer KJ, Colman BP, Currie WS, Magill A, Aber JD (2004). Decadal-scale fates of ¹⁵N tracers added to oak and pine stands under ambient and elevated N inputs at the Harvard Forest (USA) . Forest Ecology and Management, 196, 89-107. DOI URL
[64]	Nadelhoffer KJ, Downs MR, Fry B (1999). Sinks for ¹⁵N-enriched additions to an oak forest and a red pine plantation . Ecological Applications, 9, 72-86. DOI URL
[65]	Nie SA, Li H, Yang XR, Zhang ZJ, Weng BS, Huang FY, Zhu GB, Zhu YG (2015). Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. The ISME Journal, 9, 2059-2067. DOI URL PMID
[66]	Niu SL, Classen AT, Dukes JS, Kardol P, Liu LL, Luo YQ, Rustad L, Sun J, Tang JW, Templer PH, Thomas RQ, Tian DS, Vicca S, Wang YP, Xia JY, Zaehle S (2016). Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecology Letters, 19, 697-709. DOI URL PMID
[67]	Pan YP, Tian SL, Liu DW, Fang YT, Zhu XY, Zhang Q, Zheng B, Michalski G, Wang YS (2016). Fossil fuel combustion-related emissions dominate atmospheric ammonia sources during severe haze episodes: evidence from ¹⁵N-stable isotope in size-resolved aerosol ammonium . Environmental Science & Technology, 50, 8049-8056. DOI URL PMID
[68]	Quan Z, Li SL, Zhu FF, Zhang LM, He JZ, Wei WX, Fang YT (2018). Fates of ¹⁵N-labeled fertilizer in a black soil-maize system and the response to straw incorporation in Northeast China . Journal of Soils and Sediments, 18, 1441-1452. DOI URL
[69]	Ren HY, Xu ZW, Isbell F, Huang JH, Han XG, Wan SQ, Chen SP, Wang RZ, Zeng DH, Jiang Y, Fang YT (2017). Exacerbated nitrogen limitation ends transient stimulation of grassland productivity by increased precipitation. Ecological Monographs, 87, 457-469.
[70]	Rimski-Korsakov H, Rubio G, Lavado RS (2012). Fate of the nitrogen from fertilizers in field-grown maize. Nutrient Cycling in Agroecosystems, 93, 253-263.
[71]	Robinson D (2001). δ¹⁵N as an integrator of the nitrogen cycle. Trends in Ecology & Evolution, 16, 153-162. URL PMID
[72]	Ruisi P, Saia S, Badagliacca G, Amato G, Frenda AS, Giambalvo D, di Miceli G (2016). Long-term effects of no tillage treatment on soil N availability, N uptake, and ¹⁵N-fertilizer recovery of durum wheat differ in relation to crop sequence . Field Crops Research, 189, 51-58.
[73]	Sebilo M, Mayer B, Nicolardot B, Pinay G, Mariotti A (2013). Long-term fate of nitrate fertilizer in agricultural soils. Proceedings of the National Academy of Sciences of the United States of America, 110, 18185-18189. URL PMID
[74]	Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Böhlke JK (2001). A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Analytical Chemistry, 73, 4145-4153. URL PMID
[75]	Stevens RJ, Laughlin RJ (1998). Measurement of nitrous oxide and di-nitrogen emissions from agricultural soils. Nutrient Cycling in Agroecosystems, 52, 131-139.
[76]	Takebayashi Y, Koba K, Sasaki Y, Fang YT, Yoh M (2010). The natural abundance of ¹⁵N in plant and soil-available N indicates a shift of main plant N resources to NO₃^- from NH₄⁺ along the N leaching gradient. Rapid Communications in Mass Spectrometry, 24, 1001-1008. URL PMID
[77]	Templer PH, Mack MC, Chapin FS, Christenson LM, Compton JE, Crook HD, Currie WS, Curtis CJ, Dail DB, D’antonio CM, Emmett BA, Epstein HE, Goodale CL, Gundersen P, Hobbie SE, Holland K, Hooper DU, Hungate BA, Lamontagne S, Nadelhoffer KJ, Osenberg CW, Perakis SS, Schleppi P, Schimel J, Schmidt IK, Sommerkorn M, Spoelstra J, Tietema A, Wessel WW, Zak DR (2012). Sinks for nitrogen inputs in terrestrial ecosystems: a meta-analysis of ¹⁵N tracer field studies . Ecology, 93, 1816-1829. DOI URL PMID
[78]	Tietema A, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans CJ (1998). The fate of ¹⁵N-labelled nitrogen deposition in coniferous forest ecosystems. Forest Ecology and Management, 101, 19-27. DOI URL
[79]	Wang A, Zhu WX, Gundersen P, Phillips OL, Chen DX, Fang YT (2018). Fates of atmospheric deposited nitrogen in an Asian tropical primary forest. Forest Ecology and Management, 411, 213-222.
[80]	Wang SJ, Luo SS, Yue SC, Shen YF, Li SQ (2016a). Fate of ¹⁵N fertilizer under different nitrogen split applications to plastic mulched maize in semiarid farmland. Nutrient Cycling in Agroecosystems, 105, 129-140.
[81]	Wang XB, Zhou W, Liang GQ, Pei XX, Li KJ (2016b). The fate of ¹⁵N-labelled urea in an alkaline calcareous soil under different N application rates and N splits. Nutrient Cycling in Agroecosystems, 106, 311-324.
[82]	Wang XT, Suo YY, Feng Y, Shohag MJI, Gao J, Zhang QC, Xie S, Lin XY (2011). Recovery of ¹⁵N-labeled urea and soil nitrogen dynamics as affected by irrigation management and nitrogen application rate in a double rice cropping system. Plant and Soil, 343, 195-208.
[83]	Xi D, Bai R, Zhang LM, Fang YT (2016). Contribution of anammox to nitrogen removal in two temperate forest soils. Applied and Environmental Microbiology, 82, 4602-4612. URL PMID
[84]	Xu HG, Zhong GR, Lin JJ, Ding YF, Li GH, Wang SH, Liu ZH, Tang S, Ding CQ (2015). Effect of nitrogen management during the panicle stage in rice on the nitrogen utilization of rice and succeeding wheat crops. European Journal of Agronomy, 70, 41-47.
[85]	Yang L, Guo S, Chen QW, Chen FJ, Yuan LX, Mi GH (2016). Use of the stable nitrogen isotope to reveal the source-sink regulation of nitrogen uptake and remobilization during grain filling phase in maize. PLOS ONE, 11, e0162201. DOI: 10.1371/journal.pone.0162201. DOI URL PMID
[86]	Yang WH, McDowell AC, Brooks PD, Silver WL (2014). New high precision approach for measuring ¹⁵N-N₂ gas fluxes from terrestrial ecosystems. Soil Biology & Biochemistry, 69, 234-241.
[87]	Yao FY, Zhu B, Du EZ (2012). Use of ¹⁵N natural abundance in nitrogen cycling of terrestrial ecosystems. Chinese Journal of Plant Ecology, 36, 346-352.
	[ 姚凡云, 朱彪, 杜恩在 (2012). ¹⁵N自然丰度法在陆地生态系统氮循环研究中的应用. 植物生态学报, 36, 346-352.]
[88]	Zhang L, Altabet MA, Wu TX, Hadas O (2007a). Sensitive measurement of NH₄⁺¹⁵N/¹⁴N (δ¹⁵NH₄⁺) at natural abundance levels in fresh and saltwaters. Analytical Chemistry, 79, 5297-5303. URL PMID
[89]	Zhang L, Wu Z, Jiang Y, Chen L, Song Y, Wang L, Xie J, Ma X (2010). Fate of applied urea ¹⁵N in a soil-maize system as affected by urease inhibitor and nitrification inhibitor. Plant, Soil & Environment, 56, 8-15.
[90]	Zhang SS, Fang YT, Xi D (2015). Adaptation of microdiffusion method for the analysis of ¹⁵N natural abundance of ammonium in samples with small volume. Rapid Communications in Mass Spectrometry, 29, 1297-1306. URL PMID
[91]	Zhang XD, Amelung W (1996). Gas chromatographic determination of muramic acid, glucosamine, mannosamine, and galactosamine in soils. Soil Biology & Biochemistry, 28, 1201-1206.
[92]	Zhang XD, He HB, Amelung W (2007b). A GC/MS method for the assessment of ¹⁵N and ¹³C incorporation into soil amino acid enantiomers. Soil Biology & Biochemistry, 39, 2785-2796.
[93]	Zhang ZL, Li N, Xiao J, Zhao CZ, Zou TT, Li DD, Liu Q, Yin HJ (2018). Changes in plant nitrogen acquisition strategies during the restoration of spruce plantations on the eastern Tibetan Plateau, China. Soil Biology & Biochemistry, 119, 50-58. DOI URL
[94]	Zhu FF, Dai LM, Hobbie EA, Koba K, Liu XY, Gurmesa GA, Huang SN, Li SL, Li YH, Han SJ, Fang YT (2019). Uptake patterns of glycine, ammonium, and nitrate differ among four common tree species of northeast China. Frontiers in Plant Science, 10, 799. DOI: 10.3389/fpls.2019.00799. URL PMID
[95]	Zhu GB, Wang SY, Wang Y, Wang CX, Risgaard-Petersen N, Jetten MS, Yin CQ (2011). Anaerobic ammonia oxidation in a fertilized paddy soil. The ISME Journal, 5, 1905-1912. URL PMID
[96]	Zong Z, Wang XP, Tian CG, Chen YJ, Fang YT, Zhang F, Li C, Sun JZ, Li J, Zhang G (2017). First assessment of NO_x sources at a regional background site in North China using isotopic analysis linked with modeling. Environmental Science & Technology, 51, 5923-5931. DOI URL PMID