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Does the accelerated soil N cycling sustain N demand of Quercus mongolica after decade-long elevated CO2 treatment?

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Abstract

The stimulation of plant growth and biomass accumulation by elevated CO2 may be limited by soil nitrogen (N) availability. However, our understanding of the response of soil N cycling to elevated CO2 and when progressive N limitation occurs remains limited. Here, we used an open top chamber experiment to examine the effects of 10 years of elevated CO2 on ecosystem carbon (C) and N dynamics in a Quercus mongolica (oak) dominated system in northeastern China. Elevated CO2 increased oak biomass, C and N stocks and C/N by 26.4, 26.2, 16.5 and 8.6% respectively, which suggests increased plant N demand. Soil gross N mineralization, re-mineralization of microbial N and nitrification were accelerated likely due to increased photosynthesis (by 34.9%) and microbial biomass (by 24.2%) under elevated CO2. Thus, the supply of soil available N can sustain the tree growth stimulated by elevated CO2, and to date progressive N limitation has not happened. Nevertheless, both the annual increase of oak biomass, C and N stocks and C/N ratio and the seasonal variations of soil available N and microbial N concentrations, and net N transformation rates indicated that gradual N deficiency may be occurring and the CO2 fertilization effect has weakened with increasing treatment duration.

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References

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165(2):351–372

    Article  Google Scholar 

  • Arnone JA, Bohlen PJ (1998) Stimulated N2O flux from intact grassland monoliths after two growing seasons under elevated atmospheric CO2. Oecologia 116(3):331–335

    Article  Google Scholar 

  • Barnard R, Barthes L, Le Rous X, Leadley PW (2004) Dynamics of nitrifying activities, denitrifying activities and nitrogen in grassland mesocosms as altered by elevated CO2. New Phytol 162(2):365–376

    Article  Google Scholar 

  • Barnard R, Barthes L, Leadley PW (2006) Short-term uptake of 15N by a grass and soil micro-organisms after long-term exposure to elevated CO2. Plant Soil 280(1–2):91–99

    Article  Google Scholar 

  • Bengtson P, Bengtsson G (2005) Bacterial immobilization and remineralization of N at different growth rates and N concentrations. FEMS Microbiol Ecol 54(1):13–19

    Article  Google Scholar 

  • Berntson GM, Bazzaz FA (1997) Regenerating temperate forest mesocosms in elevated CO2: belowground growth and nitrogen cycling. Oecologia 113(1):115–125

    Article  Google Scholar 

  • Björsne AK, Rütting T, Ambus P (2014) Combined climate factors alleviate changes in gross soil nitrogen dynamics in heathlands. Biogeochemistry 120(1–3):191–201

    Article  Google Scholar 

  • Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75(2):139–157

    Article  Google Scholar 

  • Brookes PC, Kragt JF, Powlson DS, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: the effects of fumigation time and temperature. Soil Biol Biochem 17(6):831–835

    Article  Google Scholar 

  • Carrillo Y, Dijkstra FA, Pendall E, Morgan JA, Blumenthal DM (2012) Controls over soil nitrogen pools in a semiarid grassland under elevated CO2 and warming. Ecosystems 15(5):761–774

    Article  Google Scholar 

  • Chapin FS III, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New York

    Google Scholar 

  • Collins JG, Dijkstra P, Hart SC, Hungate BA, Flood NM, Schwartz E (2008) Nitrogen source influences natural abundance 15N of Escherichia coli. FEMS Microbiol Lett 282(2):246–250

    Article  Google Scholar 

  • De Graaff MA, van Groenigen KJ, Six J, Hungate BA, van Kessel C (2006) Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta-analysis. Global Change Biol 12(11):2077–2091

    Article  Google Scholar 

  • Dijkstra P, Menyailo OV, Doucett RR, Hart SC, Schwartz E, Hungate BA (2006) C and N availability affects the 15N natural abundance of the soil microbial biomass across a cattle manure gradient. Eur J Soil Sci 57(4):468–475

    Article  Google Scholar 

  • Dijkstra P, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA (2008a) 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11(4):389–397

    Article  Google Scholar 

  • Dijkstra FA, Pendall E, Mosier AR, King JY, Milchunas DG, Morgan JA (2008b) Long-term enhancement of N availability and plant growth under elevated CO2 in a semi-arid grassland. Funct Ecol 22(6):975–982

    Article  Google Scholar 

  • Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Billings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Phillips RP, Pippen JS, Pritchard SG, Treseder KK, Schlesinger WH, DeLucia EH, Finzi AC (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14(4):349–357

    Article  Google Scholar 

  • Feng ZZ, Rütting T, Pleijel H, Wallin G, Reich PB, Kammann CI, Newton PCD, Kobayashi K, Luo YJ, Uddling J (2015) Constraints to nitrogen acquisition of terrestrial plants under elevated CO2. Glob Change Biol 21(8):3152–3168

    Article  Google Scholar 

  • Finzi AC, Norby RJ, Calfapietra C, Gallet-Budynek A, Gielen B, Holmes WE, Hoosbeek MR, Iversen CM, Jackson RB, Kubiske ME, Ledford J, Liberloo M, Oren R, Polle A, Pritchard S, Zak DR, Schlesinger WH, Ceulemans R (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Natl Acad Sci USA 104(35):14014–14019

    Article  Google Scholar 

  • Gee GM, Bauder JW (1986) Physical and mineralogical methods. Methods of soil analysis. American Society of Agronomy, Madison, pp 383–411

    Google Scholar 

  • Hikosaka K, Terashima I, Katoh S (1994) Effects of leaf age, nitrogen nutrition and photon flux density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia 97(4):451–457

    Article  Google Scholar 

  • Hu S, Tu C, Chen X, Gruver JB (2006) Progressive N limitation of plant response to elevated CO2: a microbiological perspective. Plant Soil 289(1–2):47–58

    Article  Google Scholar 

  • Hungate BA, Chapin FS III, Zhong H, Holland EA, Field CB (1997a) Stimulation of grassland nitrogen cycling under carbon dioxide enrichment. Oecologia 109(1):149–153

    Article  Google Scholar 

  • Hungate BA, Lund CP, Pearson HL, Chapin FS III (1997b) Elevated CO2 and nutrient addition alter soil N cycling and N trace gas fluxes with early season wet-up in a California annual grassland. Biogeochemistry 37(2):89–109

    Article  Google Scholar 

  • Hungate BA, Dijkstra P, Johnson DW, Hinkle CR, Drake BG (1999) Elevated CO2 increases nitrogen fixation and decreases soil nitrogen mineralization in Florida scrub oak. Glob Change Biol 5(7):781–789

    Article  Google Scholar 

  • Huo CF, You WZ, Zhang HD, Yan TW, Wei WJ, Zhao G, Guo JS, Xing ZK (2011) Biomass and net primary productivity of Quecus mongolica plantation in Binglashan Mountains in Liaoning Province. J Liaoning For Sci Technol 4:4–11

    Google Scholar 

  • IPCC (2013) Climate Change 2013: The physical science basis: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 465–470

    Google Scholar 

  • Iversen CM, Hooker TD, Classen AT, Norby RJ (2011) Net mineralization of N at deeper soil depths as a potential mechanism for sustained forest production under elevated CO2. Glob Change Biol 17(2):1130–1139

    Article  Google Scholar 

  • Jaeger CH III, Monson RK, Fisk MC, Schmidt SK (1999) Seasonal partitioning of nitrogen and soil microorganisms in an alpine ecosystem. Ecology 80(6):1883–1891

    Article  Google Scholar 

  • Johnson DW, Hungate BA, Dijkstra P, Hymus G, Drake B (2001) Effects of elevated carbon dioxide on soils in a Florida scrub oak ecosystem. J Environ Qual 30(2):501–507

    Article  Google Scholar 

  • Leuzinger S, Luo YQ, Beier C, Dieleman W, Vicca S, Körner C (2011) Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol Evol 26(5):236–241

    Article  Google Scholar 

  • Li XF, Han SJ, Guo ZL, Shao DK, Xin LH (2010) Changes in soil microbial biomass carbon and enzyme activities under elevated CO2 affect fine root decomposition processes in a Mongolian oak ecosystem. Soil Biol Biochem 42(7):1101–1107

    Article  Google Scholar 

  • Liang JY, Qi X, Souza L, Luo YQ (2016) Processes regulating progressive nitrogen limitation under elevated carbon dioxide: a meta-analysis. Biogeosciences 13(9):2689–2699

    Article  Google Scholar 

  • Liu J, Peng B, Xia ZW, Sun JF, Gao DC, Dai WW, Jiang P, Bai E (2017) Different fates of deposited NH4 + and NO3 − in a temperate forest in northeast China: a 15N tracer study. Glob Change Biol 23(6):2441–2449

    Article  Google Scholar 

  • Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628

    Article  Google Scholar 

  • Lu Y, Chen YM, Cao Y, Song C (2015) C, N and P stoichiometric characteristics of plants and soil in Quercus liaotungensis forest on Ziwuling mountain of Loess Plateau. J Soil Water Conserv 29(3):196–201

    Google Scholar 

  • Luo YQ, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate BA, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Rebecca Shaw M, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54(8):731–739

    Article  Google Scholar 

  • Luo YQ, Hui DF, Zhang DQ (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87(1):53–63

    Article  Google Scholar 

  • Mary B, Recous S, Robin D (1998) A model for calculating nitrogen fluxes in soil using 15N tracing. Soil Biol Biochem 30(14):1963–1979

    Article  Google Scholar 

  • McKinley DC, Romero JC, Hungate BA, Drake BG, Megonigal JP (2009) Does deep soil N availability sustain long-term ecosystem responses to elevated CO2? Glob Change Biol 15(8):2035–2048

    Article  Google Scholar 

  • Müller C, Rütting T, Abbasi MK, Laughlin RJ, Kammann C, Clough TJ, Sherlock RR, Kattge J, Jäger HJ, Watson CJ, Stevens RJ (2009) Effect of elevated CO2 on soil N dynamics in a temperate grassland soil. Soil Biol Biochem 41(9):1996–2001

    Article  Google Scholar 

  • Niklaus PA, Leadley PW, Stöcklin J, Körner C (1998) Nutrient relations in calcareous grassland under elevated CO2. Oecologia 116(1):67–75

    Article  Google Scholar 

  • Niklaus PA, Kandeler E, Leadley PW, Schmid B, Tscherko D, Körner C (2001) A link between plant diversity, elevated CO2 and soil nitrate. Oecologia 127(4):540–548

    Article  Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14(2):187–194

    Article  Google Scholar 

  • Raison RJ, Connell MJ, Khanna PK (1987) Methodology for studying fluxes of soil mineral N in situ. Soil Biol Biochem 19(5):521–530

    Article  Google Scholar 

  • Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440(7086):922–925

    Article  Google Scholar 

  • Richter M, Hartwig UA, Frossard E, Nösberger J, Cadisch G (2003) Gross fluxes of nitrogen in grassland soil exposed to elevated atmospheric CO2 for seven years. Soil Biol Biochem 35(10):1325–1335

    Article  Google Scholar 

  • Rütting T, Andresen LC (2015) Nitrogen cycle responses to elevated CO2 depend on ecosystem nutrient status. Nutr Cycl Agroecosyst 101(3):285–294

    Article  Google Scholar 

  • Rütting T, Clough TJ, Müller C, Lieffering M, Newton PCD (2010) Ten years of elevated atmospheric carbon dioxide alters soil nitrogen transformations in a sheep-grazed pasture. Glob Change Biol 16(9):2530–2542

    Article  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85(3):591–602

    Article  Google Scholar 

  • Schleppi P, Bucher-Wallin I, Hagedorn F, Körner C (2012) Increased nitrate availability in the soil of a mixed mature temperate forest subjected to elevated CO2 concentration (canopy FACE). Glob Change Biol 18(2):757–768

    Article  Google Scholar 

  • Schneider MK, Lüscher A, Richter M, Aeschlimann U, Hartwig U, Blum H, Frossard E, Nösberger J (2004) Ten years of free-air CO2 enrichment altered the mobilization of N from soil. Glob Change Biol 10(8):1377–1388

    Article  Google Scholar 

  • Sebilo M, Mayer B, Grably M, Billiou D, Mariotti A (2004) The use of the ‘ammonium diffusion’ method for δ15N-NH4 + and δ15N-NO3 − measurements: comparison with other techniques. Environ Chem 1(2):99–103

    Article  Google Scholar 

  • Sun JF, Peng B, Li W, Qu GF, Dai WW, Dai GH, Jiang P, Han SJ, Bai E (2016) Effects of nitrogen addition on potential soil nitrogen cycling processes in a temperate forest ecosystem. Soil Sci 181(1):29–38

    Article  Google Scholar 

  • Sun JF, Xia ZW, He TX, Dai WW, Peng B, Liu J, Gao DC, Jiang P, Han SJ, Bai E (2017) Ten years of elevated CO2 affects soil greenhouse gas fluxes in an open top chamber experiment. Plant Soil 420(1–2):435–450

    Article  Google Scholar 

  • Thornley JHM, Cannell MGR (2000) Dynamics of mineral N availability in grassland ecosystems under increased CO2: hypotheses evaluated using the Hurley Pasture Model. Plant Soil 224(1):153–170

    Article  Google Scholar 

  • Van Groenigen KJ, de Graaff MA, Six J, Harris D, Kuikman P, van Kessel C (2006) The impact of elevated atmospheric CO2 on soil C and N dynamics: a meta-analysis. Managed ecosystems and CO2 case studies, processes and perspectives. Springer, Berlin, pp 373–392

    Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) Microbial biomass measurements in forest soils: determination of kC values and tests of hypotheses to explain the failure of the chloroform fumigation-incubation method in acid soils. Soil Biol Biochem 19(6):689–696

    Article  Google Scholar 

  • Williams MA, Rice CW, Owensby CE (2000) Carbon dynamics and microbial activity in tallgrass prairie exposed to elevated CO2 for 8 years. Plant Soil 227(1–2):127–137

    Article  Google Scholar 

  • Xia JY, Wan SQ (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179(2):428–439

    Article  Google Scholar 

  • Yoccoz NG (1991) Use, overuse, and misuse of significance tests in evolutionary biology and ecology. Bull Ecol Soc Am 72(2):106–111

    Google Scholar 

  • Zak DR, Pregitzer KS, Curtis PS, Teeri JA, Fogel R, Randlett DL (1993) Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant Soil 151(1):105–117

    Article  Google Scholar 

  • Zak DR, Pregitzer KS, Kubiske ME, Burton AJ (2011) Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol Lett 14(12):1220–1226

    Article  Google Scholar 

  • Zheng JQ, Han SJ, Wang Y, Zhang CG, Li MH (2010) Composition and function of microbial communities during the early decomposition stages of foliar litter exposed to elevated CO2 concentrations. Eur J Soil Sci 61(6):914–925

    Article  Google Scholar 

  • Zhou YM, Li MH, Cheng XB, Wang CG, Fan AN, Shi LX, Wang XX, Han SJ (2010) Soil respiration in relation to photosynthesis of Quercus mongolica trees at elevated CO2. PLoS ONE 5(12):e15134

    Article  Google Scholar 

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Acknowledgements

This study was supported by National Key R&D Program of China (2016YFA0600804), the National Natural Science Foundation of China (31522010), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15010301), and the Key Research Program of Frontier Sciences, CAS (QYZDB-SSWDQC006). We are very grateful to Dr. B. Mary for kindly providing the FLUAZ model, and Lufu Zhao for maintaining the OTC facility.

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Authors and Affiliations

  1. CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, No. 72 Wenhua Road, Shenyang, 110016, China

    Jianfei Sun, Weiwei Dai, Bo Peng, Jun Liu, Tongxin He, Ping Jiang, Shijie Han & Edith Bai

  2. Key Laboratory of Beibu Gulf Environment Change and Resources Use (Guangxi Teachers Education University), Ministry of Education, No. 175 Mingxiu East Road, Nanning, 530001, China

    Jianfei Sun & Tongxin He

  3. College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China

    Jianfei Sun, Bo Peng, Jun Liu & Tongxin He

  4. School of Geographical Sciences, Northeast Normal University, No. 5268 Renmin Road, Changchun, 130024, China

    Edith Bai

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  1. Jianfei Sun
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Sun, J., Dai, W., Peng, B. et al. Does the accelerated soil N cycling sustain N demand of Quercus mongolica after decade-long elevated CO2 treatment?. Biogeochemistry 139, 197–213 (2018). https://doi.org/10.1007/s10533-018-0463-9

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