Abstract
Background and aims
Increasing global atmospheric nitrogen (N) deposition has a considerable impact on soil respiration. Due to different carbon dioxide (CO2) resources of different components of soil respiration, there may be different mechanisms by which soils respond to N additions. The aims of this study are to investigate the effects of N additions on total soil respiration (RST), rhizospheric respiration (RSR) and heterotrophic respiration (RSH), and to elucidate the potential causal mechanisms.
Methods
An artificial N addition experiment was conducted in an evergreen broad-leaved forest at the western edge of the Sichuan Basin in China. The effects of three N treatment levels (+0, +50, +150 kg N ha−1 yr.−1) were measured, with the N application initiated in April 2013. Trenching method was used for partitioning RST into RST and RSR. The values of RST and its components were measured monthly from May 2015 to April 2016.
Results
The mean annual RST was 1.92 ± 0.18 μmol CO2 m−2 s−1, with RSH and RSR contributing 75 ± 1% and 25 ± 1% to RST, respectively. Nitrogen addition significantly reduced RST and its two components, as well as the contribution of RSR to RST. Microbial biomass carbon (C) and pH in bulk soil decreased significantly after N application. Nitrogen addition had no effect on rhizospheric soil biochemical properties. RSR was significantly positively correlated with root biomass of Castanopsis platyacantha, while RSH was significantly positively correlated with the concentrations of microbial biomass C (MBC) and microbial biomass N (MBN) for bulk soil.
Conclusions
The positive correlation between RSR and root biomass indicates that N application reduced RSR by reducing belowground C allocation and thus C inputs to the rhizosphere. The value of RSH decreased primarily due to a reduction in microbial activity and soil organic matter decomposition in root-free soil after N was added. The presence of plant roots may mitigate the effect of N inputs to the rhizosphere via alteration of root morphology and exudates.
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References
Agnelli A, Massaccesi L, De Feudis M, Cocco S, Courchesne F, Corti G (2016) Holm oak (Quercus ilex L.) rhizosphere affects limestone-derived soil under a multi-centennial forest. Plant Soil 400:297–314
Allison SD, Czimczik CI, Tresedek KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1156–1168
Baldos AP, Corre MD, Veldkamp E (2015) Response of N cycling to nutrient inputs in forest soils across a 1000–3000 m elevation gradient in the Ecuadorian Andes. Ecology 96:749–761
Batjes NH (2016) Harmonized soil property values for broad-scale modelling (WISE30sec) with estimates of global soil carbon stocks. Geoderma 269:61–68
Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59
Bond-Lamberty B, Thomson A (2010) Temperature-associated increases in the global soil respiration record. Nature 464:579–582
Bowden RD, Nadelhoffer KJ, Boone RD, Melillo JM, Garrison JB (1993) Contributions of above ground litter, below ground litter, and root respiration to total soil respiration in a temperate mixed hardwood forest. Can J For Res 23:1402–1407
Bowden RD, Davidson E, Savage K, Arabia C, Steudler P (2004) Chronic N additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. For Ecol Manage 196:43–56
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842
Chen H, Tian HQ (2005) Does a general temperature-dependent Q10 model of soil respiration exist at biome and global scale? J Integr Plant Biol 47:1288–1302
Chen GT, Peng Y, Zheng J, Li S, Peng TC, Qiu XR, Tu LH (2017a) Effects of short-time nitrogen addition on fine root biomass, lifespan and morphology of Castanopsis platyacantha in a subtropical secondary evergreen broad-leaved forest. Chin J Plant Ecol 41:1041–1050 (in Chinese)
Chen GT, Tu LH, Peng Y, Hu HL, Hu TX, Xu ZF, Liu L, Tang Y (2017b) Effect of nitrogen additions on root morphology and chemistry in a subtropical bamboo forest. Plant Soil 412:441–451
Chen GT, Li S, Peng TC, Qiu XR, Chen YQ, Ma HY, Tu LH (2018) Effect of root isolation and nitrogen addition on soil carbon and nitrogen fractions in a moist evergreen broad-leaved forest. Chin J App Environ Biol 24:1135–1141 (in Chinese)
Cocco S, Agnelli A, Gobran GR, Corti G (2013) Modifications induced by the roots of Erica arborea L. to create a suitable environment in soils developed from alkaline and fine-textured marine sediments. Plant Soil 368:297–313
Comeau LP, Hergoualc'h K, Hartill J, Smith J, Verchot LV, Peak D, Salim AM (2016) How do the heterotrophic and the total soil respiration of an oil palm plantation on peat respond to nitrogen fertilizer application? Geoderma 268:41–51
Corre MD, Veldkamp E, Arnold J, Wright SJ (2010) Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama. Ecology 91:1715–1729
Cusack DF, Silver WL, Torn MS, McDowell WH (2011) Effects of nitrogen additions on above- and belowground carbon dynamics in two tropical forests. Biogeochemistry 104:203–225
Dentener F, Drevet J, Lamarque JF, Bey I, Eickhout B, Fiore AM, Hauglustaine D, Horowitz LW, Krol M, Kulshrestha UC, Lawrence M, Galy-Lacaux C, Rast S, Shindell D, Stevenson D, Van Noije T, Atherton C, Bell N, Bergman D, Butler T, Cofala J, Collins B, Doherty R, Ellingsen K, Galloway J, Gauss M, Montanaro V, Müller JF, Pitari G, Rodriguez J, Sanderson M, Solmon F, Strahan S, Schultz M, Sudo K, Szopa S, Wild O (2006) Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Global Biogeochem Cycles 20:16615–16615
Devaraju N, Bala G, Caldeira K, Nemani R (2016) A model based investigation of the relative importance of CO2-fertilization, climate warming, nitrogen deposition and land use change on the global terrestrial carbon uptake in the historical period. Clim Dyn 47:173–190
Fan HB, Wu JP, Liu WF, Yuan YH, Huang RZ, Liao YC, Li YY (2014) Nitrogen deposition promotes ecosystem carbon accumulation by reducing soil carbon emission in a subtropical forest. Plant Soil 379:361–337
Feudis MD, Cardelli V, Massaccesi L, Hofmann D, Berns AE, Bol R, Cocco S, Corti G, Agnelli A (2017) Altitude affects the quality of the water-extractable organic matter (WEOM) from rhizosphere and bulk soil in European beech forests. Geoderma 302:6–13
Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. Bioscience 53:341–356
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892
Haichar FEZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80
Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146
Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257
Jackson LE, Bowles TM, Hodson AK, Lazcano C (2012) Soil microbial-root and microbial-rhizosphere processes to increase nitrogen availability and retention in agroecosystems. Curr Opin Environ Sustain 4:517–522
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. Nat Geosci 3:315–322
Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448
Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199
Kuzyakov Y, Siniakina SV, Ruehlmann J, Domanski G, Stahr K (2002) Effect of nitrogen fertilisation on below-ground carbon allocation in lettuce. J Sci Food Agr 82:1432–1441
Law B (2013) Nitrogen deposition and forest carbon. Nature 496:307–308
Lebauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
Li RH, Tu LH, Hu TX, Zhang J, Lu Y, Liu WT, Luo SH, Xiang YB (2010) Effects of simulated nitrogen deposition on soil respiration in a Neosinocalamus affinis plantation in rainy area of West China. Chin J Appl Ecol 21:1649–1655 (in Chinese)
Li XG, Jia B, Lv JT, Ma QJ, Kuzyakov Y, Li FM (2017) Nitrogen fertilization decreases the decomposition of soil organic matter and plant residues in planted soils. Soil Biol Biochem 112:47–55
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) Enhanced nitrogen deposition over China. Nature 494:459–462
Liu T, Xu ZZ, Hou YH, Zhou GS (2016) Effects of warming and changing precipitation rates on soil respiration over two years in a desert steppe of northern China. Plant Soil 400:15–27
Lloyd J, Taylor JA (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–323
Luo SH, Hu TX, Zhang J, Dai HZ, Tu LH, Li RH, Huang LH (2010) Responses of soil respiration to nitrogen fertilization in Betulah luminifera forest, rainy area of West China. J Agro-Environ Sci 29:1834–1839 (in Chinese)
Mande HK, Abdullah AM, Aris AZ, Ainuddin AN (2015) Factors responsible for spatial and temporal variation of soil CO2 efflux in a 50 year recovering tropical forest, peninsular Malaysia. Environ Earth Sci 73:5559–5569
Mo JM, Zhang W, Zhu WX, Gundersen P, Fang YT, Li DJ, Wang H (2008) Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Glob Chang Biol 14:403–412
Moran KK, Six J, Horwath WR, van Kessel C (2005) Role of mineral-nitrogen in residue decomposition and stable soil organic matter formation. Soil Sci Soc Am J 69:1730–1736
Ochoa-Hueso R, Arróniz-Crespo M, Bowker MA, Maestre FT, Pérez-Corona ME, Theobald MR, Vivanco MG, Manrique E (2014) Biogeochemical indicators of elevated nitrogen deposition in semiarid Mediterranean ecosystems. Environ Monit Assess 186:5831–5842
Olsson P, Linder S, Giesler R, Högberg P (2005) Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Glob Chang Biol 11:1745–1753
Peng Y, Chen GS, Chen GT, Li S, Peng TC, Qiu XR, Luo J, Yang SS, Hu TX, Hu HL, Xu ZF, Liu L, Tang Y, Tu LH (2017) Soil biochemical responses to nitrogen addition in a secondary evergreen broad-leaved forest ecosystem. Sci Rep 7:2783. https://doi.org/10.1038/s41598-017-03044-w
Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168:305–312
Riggs CE, Hobbie SE, Bach EM, Hofmockel KS, Kazanski CE (2015) Nitrogen addition changes grassland soil organic matter decomposition. Biogeochemistry 125:203–219
Samuelson L, Mathew R, Stokes T, Feng YC, Aubrey D, Coleman M (2009) Soil and microbial respiration in a loblolly pine plantation in response to seven years of irrigation and fertilization. For Ecol Manage 258:2431–2438
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
Scott-Denton LE, Rosenstiel TN, Monson RK (2006) Differential controls by climate and substrate over the heterotrophic and rhizospheric components of soil respiration. Glob Chang Biol 12:205–216
Shcherbak I, Millar N, Robertson GP (2014) Global metaanalysis of the nonlinear response of soil nitrous oxide (N2O) emissions to fertilizer nitrogen. Proc Natl Acad Sci U S A 111:9199–9204
Shrestha RK, Strahm BD, Sucre EB (2015) Greenhouse gas emissions in response to nitrogen fertilization in managed forest ecosystems. New For 46:167–193
Subbarao GV, Nakahara K, Hurtado MP, Ono H, Moreta DE, Salcedo AF, Yoshihashi AT, Ishikawa T, Ishitani M, Ohnishi-Kameyama M, Yoshida M, Rondon M, Rao IM, Lascano CE, Berry WL, Ito O (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. Proc Natl Acad Sci U S A 106:17302–17307
Subke J, Inglima I, Cotrufo M (2006) Trends and methodological impacts in soil CO2 efflux partitioning: a metaanalytical review. Glob Chang Biol 12:921–943
Sun ZZ, Liu LL, Ma YC, Yin GD, Zhao C, Zhang Y, Piao SL (2014) The effect of nitrogen addition on soil respiration from a nitrogen-limited forest soil. Agric For Meteorol 197:103–110
Thorn KA, Mikita MA (1992) Ammonia fixation by humic substances: a nitrogen-15 and carbon-13 NMR study. Sci Total Environ 113:67–87
Tian DS, Niu SL (2015) A global analysis of soil acidifcation caused by nitrogen addition. Environ Res Lett 10:24019–24028
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120
Tu LH, Dai HZ, Hu TX, Zhang J, Luo SH (2011a) Effects of simulated nitrogen deposition on soil respiration in a Bambusa pervariabilis × Dendrocala mopsi plantation in rainy area of West China. Chin J Appl Ecol 22:829–839 (in Chinese)
Tu LH, Hu TX, Zhang J, Li RH, Dai HZ, Luo SH (2011b) Short-term simulated nitrogen deposition increases carbon sequestration in a Pleioblastus amarus plantation. Plant Soil 340:383–396
Tu LH, Hu TX, Zhang J, Li XW, Hu HL, Liu L, Xiao YL (2013) Nitrogen addition stimulates different components of soil respiration in a subtropical bamboo ecosystem. Soil Biol Biochem 58:255–264
Wang CK, Yang JY (2007) Rhizospheric and heterotrophic components of soil respiration in six Chinese temperate forests. Glob Chang Biol 13:123–131
Wang QK, Zhang WD, Sun T, Chen LC, Pang XY, Wang YP, Xiao FM (2017a) N and P fertilization reduced soil autotrophic and heterotrophic respiration in a young Cunninghamia lanceolata forest. Agric For Meteorol 232:66–73
Wang GL, Liu F, Xue S (2017b) Nitrogen addition enhanced water uptake by affecting fine root morphology and coarse root anatomy of Chinese pine seedlings. Plant Soil 418:177–189
Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation-extraction-an automated procedure. Soil Biol Biochem 22:1167–1169
Wurzburger N, Wright SJ (2015) Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96:2137–2146
Xiang YB, Huang CD, Hu TX, Tu LH, Yang WQ, Li RH, Hu C (2014) Response of soil respiration to simulated nitrogen deposition in a Eucalyptus grandis plantation in the Rainy Area of Western China. Sci Silvae Sin 50:21–26 (in Chinese)
Xiao YL, Tu LH, Chen G, Peng Y, Hu HL, Hu TX, Liu L (2015) Soil-nitrogen net mineralization increased after nearly six years of continuous nitrogen additions in a subtropical bamboo ecosystem. J For Res 26:949–956
Xiao SH, You HM, You WB, Liu JS, Cai CT, Wu JQ, Ji ZR, Zhan SH, Hu ZS, Zhang ZR, He DJ (2017) Rhizosphere and bulk soil enzyme activities in a Nothotsuga longibracteata forest in the Tianbaoyan National Nature Reserve, Fujian Province, China. J For Res 28:521–528
Xu ZF, Tu LH, Hu TX, Schädler M (2013) Implications of greater than average increases in nitrogen deposition on the western edge of the Szechwan Basin, China. Environ Pollut 177:201–202
Yan JH, Zhang DQ, Liu JX, Zhou GY (2014) Interactions between CO2 enhancement and N addition on net primary productivity and water-use efficiency in a mesocosm with multiple subtropical tree species. Glob Chang Biol 20:2230–2239
Zang HD, Wang JY, Kuzyakov Y (2016) N fertilization decreases soil organic matter decomposition in the rhizosphere. Appl Soil Ecol 108:47–53
Zhao CZ, Liu Q (2009) Growth and photosynthetic responses of two coniferous species to experimental warming and nitrogen fertilization. Can J For Res 39:1–11
Zhao ZY, Peng CH, Yang Q, Meng FR, Song XZ, Chen ST, Epule TE, Li P, Zhu Q (2017) Model prediction of biome-specific global soil respiration from 1960 to 2012. Earths Future 5:715–729
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This project was supported by the National Natural Science Foundation of China (No. 31300522).
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Peng, Y., Chen, Gt., Li, S. et al. Nitrogen additions reduce rhizospheric and heterotrophic respiration in a subtropical evergreen broad-leaved forest. Plant Soil 431, 449–463 (2018). https://doi.org/10.1007/s11104-018-3751-1
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DOI: https://doi.org/10.1007/s11104-018-3751-1