Abstract
Increased nitrogen (N) deposition has been found controversial affecting soil CO2 emission in terrestrial ecosystems, which leads to serious debate on the efficiency of estimated C sequestration induced by N enrichment. The forms of input N might be responsible for this controversy. This study aims to explore the effects of NH4 + (reduced N) and NO3 − (oxidized N) on soil CO2 flux and the underlying microbial mechanisms. An N addition experiment, two N fertilizers (NH4Cl and NaNO3) and two rates (40 and 120 kg N ha−1 year−1), was carried out in a slash pine plantation of southern China. Soil-atmospheric CO2 exchange, soil microbial biomass, and community composition were measured using static chamber-gas chromatography and phospholipid fatty acid (PLFA) analyses in the active growing and nonactive growing seasons, respectively. Low level of NaNO3 addition significantly increased soil CO2 flux in the active growing season, whereas other N treatments did not change soil CO2 flux. High level of NH4Cl addition significantly reduced soil fungal biomass (fungal PLFA) and changed microbial community composition (ratio of fungal to bacterial (F/B) PLFAs). The positive relationships between the change in soil CO2 flux and the change in fungal biomass, as well as between the change in soil CO2 flux and the change in community composition, were observed in the nonactive growing season. The N forms as NO3 − or NH4 + are important factors affecting C cycles in the subtropical coniferous plantation. These results suggested that the variations of soil CO2 emission and microbial biomass and community composition in the subtropical plantation depended on the seasons and the levels and forms of N addition.
Similar content being viewed by others
References
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
Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1156–1168
Bastviken D, Thomsen F, Svensson T, Karlsson S, Sanden P, Shaw G, Matucha M, Oberg G (2007) Chloride retention in forest soil by microbial uptake and by natural chlorination of organic matter. Geochim Cosmochim Acta 71:3182–3192
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
Bowden RD, Davidson E, Savage K, Arabia C, Steudler P (2004) Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard Forest. For Ecol Manag 196:43–56
Chapin FS, Matso PA, Vitousek PM (2011) Principles of terrestrial ecosystem ecology, 2nd edn. Springer, New York
Chen FS, Feng X, Liang C (2012) Endogenous versus exogenous nutrient affects C, N, and P dynamics in decomposing litters in mid-subtropical forests of China. Ecol Res 27:923–932
Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci U S A 103:10316–10321
Contosta AR, Frey SD, Cooper AB (2011) Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils. Ecosphere 2: art36. doi: 10.1890/ES10-00133.1
Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621–632
DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci Soc Am J 68:132–138
Department of Forest Resources Management S (2010) The 7th National forest inventory and status of forest resources. For Resour Manag 1:3–10
Entwistle EM, Zak DR, Edwards IP (2013) Long-term experimental nitrogen deposition alters the composition of the active fungal community in the forest floor. Soil Sci Soc Am J 77:1648–1658
Fang HJ, Yu GR, Cheng SL, Zhu TH, Wang YS, Yan JH, Wang M, Cao M, Zhou M (2010) Effects of multiple environmental factors on CO2 emission and CH4 uptake from old-growth forest soils. Biogeosciences 7:395–407
Fang HJ, Cheng SL, Yu GR, Zheng JJ, Zhang PL, Xu MJ, Li YN, Yang XM (2012) Responses of CO2 efflux from an alpine meadow soil on the Qinghai Tibetan Plateau to multi-form and low-level N addition. Plant Soil 351:177–190
Fang HJ, Cheng SL, Wang YS, Yu GR, Xu MJ, Dang XS, Li LS, Wang L (2014a) Changes in soil heterotrophic respiration, carbon availability, and microbial function in seven forests along a climate gradient. Ecol Res 29:1077–1086
Fang HJ, Cheng SL, Yu GR, Xu MJ, Wang YS, Li LS, Dang XS, Wang L, Li YN (2014b) Experimental nitrogen deposition alters the quantity and quality of soil dissolved organic carbon in an alpine meadow on the Qinghai-Tibetan Plateau. Appl Soil Ecol 81:1–11
Fang HJ, Cheng SL, Yu GR, Yang XM, Xu MJ, Wang YS, Li LS, Dang XS, Wang L, Li YN (2014c) Nitrogen deposition impacts on the amount and stability of soil organic matter in an alpine meadow ecosystem depend on the form and rate of applied nitrogen. Eur J Soil Sci 65:510–519
Fanin N, Hattenschwiler S, Schimann H, Fromin N (2015) Interactive effects of C, N and P fertilization on soil microbial community structure and function in an Amazonian rain forest. Funct Ecol 29:140–150
Ferre C, Zechmeister-Boltenstern S, Comolli R, Andersson M, Seufert G (2012) Soil microbial community structure in a rice paddy field and its relationships to CH4 and N2O fluxes. Nutr Cycl Agroecosyst 93:35–50
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171
Frostegard A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fert Soils 22:59–65
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
Gavrichkova O, Kuzyakov Y (2008) Ammonium versus nitrate nutrition of Zea mays and Lupinus albus: effect on root-derived CO2 efflux. Soil Biol Biochem 40:2835–2842
Gilliam FS, McCulley RL, Nelson JA (2011) Spatial variability in soil microbial communities in a nitrogen-saturated hardwood forest watershed. Soil Sci Soc Am J 75:280–286
Hasselquist NJ, Högberg P (2014) Dosage and duration effects of nitrogen additions on ectomycorrhizal sporocarp production and functioning: an example from two N-limited boreal forests. Ecol Evol 4:3015–3026
Hassett JE, Zak DR, Blackwood CB, Pregitzer KS (2009) Are basidiomycete laccase gene abundance and composition related to reduced lignolytic activity under elevated atmospheric NO3 - deposition in a northern hardwood forest? Microb Ecol 57:728–739
Högberg P (2007) Environmental science—nitrogen impacts on forest carbon. Nature 447:781–782
Högberg MN, Hogbom L, Kleja DB (2013) Soil microbial community indices as predictors of soil solution chemistry and N leaching in Picea abies (L.) Karst. forests in S. Sweden. Plant Soil 372:507–522
Inselsbacher E, Hinko-Najera Umana N, Stange FC, Gorfer M, Schuller E, Ripka K, Zechmeister-Boltenstern S, Hood-Novotny R, Strauss J, Wanek W (2010) Short-term competition between crop plants and soil microbes for inorganic N fertilizer. Soil Biol Biochem 42:360–372
IUSS Working Group W (2006) World reference base for soil resources. World Soil Resources Report 103
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
Jia YL, Yu GR, He NP, Zhan XY, Fang HJ, Sheng WP, Zuo Y, Zhang DY, Wang QF (2014) Spatial and decadal variations in inorganic nitrogen wet deposition in China induced by human activity. Sci Rep-Uk 4:3673. doi:10.1038/Srep03763
Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143
Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257
Koba K, Hirobe M, Koyama L, Kohzu A, Tokuchi N, Nadelhoffer KJ, Wada E, Takeda H (2003) Natural N-15 abundance of plants and soil N in a temperate coniferous forest. Ecosystems 6:457–469
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 Soil. doi:10.1007/s11104-015-2420-x
Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38:425–448
Kuzyakov Y, Xu XL (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669
Lu XK, Mo JM, Gilliam FS, Zhou GY, Fang YT (2010) Effects of experimental nitrogen additions on plant diversity in an old-growth tropical forest. Glob Chang Biol 16:2688–2700
Lu M, Yang YH, Luo YQ, Fang CM, Zhou XH, Chen JK, Yang X, Li B (2011a) Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis. New Phytol 189:1040–1050
Lu M, Zhou XH, Luo YQ, Yang YH, Fang CM, Chen JK, Li B (2011b) Minor stimulation of soil carbon storage by nitrogen addition: a meta-analysis. Agr Ecosyst Environ 140:234–244
Ma ZQ, Hartmann H, Wang HM, Li QK, Wang YD, Li SG (2014) Carbon dynamics and stability between native Masson pine and exotic slash pine plantations in subtropical China. Eur J For Res 133:307–321
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
Månsson K, Bengtson P, Falkengren-Grerup U, Bengtsson G (2009) Plant-microbial competition for nitrogen uncoupled from soil C:N ratios. Oikos 118:1908–1916
Mo JM, Zhang W, Zhu WX, Fang YT, Li DJ, Zhao P (2007) Response of soil respiration to simulated N deposition in a disturbed and a rehabilitated tropical forest in southern China. Plant Soil 296:125–135
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
Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–62
Nelson DR, Mele PM (2007) Subtle changes in rhizosphere microbial community structure in response to increased boron and sodium chloride concentrations. Soil Biol Biochem 39:340–351
Ochoa-Hueso R, Rocha I, Stevens CJ, Manrique E, Lucianez MJ (2014) Simulated nitrogen deposition affects soil fauna from a semiarid Mediterranean ecosystem in central Spain. Biol Fertil Soils 50:191–196
Phillips RL, Podrebarac F (2009) Net fluxes of CO2, but not N2O or CH4, are affected following agronomic-scale additions of urea to prairie and arable soils. Soil Biol Biochem 41:2011–2013
Pietri JCA, Brookes PC (2009) Substrate inputs and pH as factors controlling microbial biomass, activity and community structure in an arable soil. Soil Biol Biochem 41:1396–1405
Roslev P, Iversen N, Henriksen K (1998) Direct fingerprinting of metabolically active bacteria in environmental samples by substrate specific radiolabelling and lipid analysis. J Microbiol Meth 31:99–111
Sheng WP, Yu GR, Fang HJ, Jiang CM, Yan JH, Zhou M (2014) Sinks for inorganic nitrogen deposition in forest ecosystems with low and high nitrogen deposition in China. Plos One 9:e89322. doi:10.1371/journal.pone.0089322
Spitzer V (1996) Structure analysis of fatty acids by gas chromatography low resolution electron impact mass spectrometry of their 4,4-dimethyloxazoline derivatives—a review. Prog Lipid Res 35:387–408
Stark S, Mannisto MK, Eskelinen A (2014) Nutrient availability and pH jointly constrain microbial extracellular enzyme activities in nutrient-poor tundra soils. Plant Soil 383:373–385
Sutton MA, Howard C, Erisman JW, Billen G, Bleeker A, Grenfelt P, van Grinsven H, Grizzetti B (2011) The European Nitrogen Assessment (Eds.) Cambridge University Press, Cambridge, pp 612
Tang XL, Liu SG, Zhou GY, Zhang DQ, Zhou CY (2006) Soil-atmospheric exchange of CO2, CH4, and N2O in three subtropical forest ecosystems in southern China. Glob Chang Biol 12:546–560
Thornton PE, Rosenbloom NA (2005) Ecosystem model spin-up: estimating steady state conditions in a coupled terrestrial carbon and nitrogen cycle model. Ecol Model 189:25–48
Tischner R (2000) Nitrate uptake and reduction in higher and lower plants. Plant Cell Environ 23:1005–1024
van Diepen LTA, Lilleskov EA, Pregitzer KS, Miller RM (2010) Simulated nitrogen deposition causes a decline of intra- and extraradical abundance of arbuscular mycorrhizal fungi and changes in microbial community structure in northern hardwood forests. Ecosystems 13:683–695
Vestal JR, White DC (1989) Lipid analysis in microbial ecology—quantitative approaches to the study of microbial communities. Bioscience 39:535–541
Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284
Wang SQ, Liu JY, Yu GR, Pan YY, Chen QM, Li KR, Li JY (2004) Effects of land use change on the storage of soil organic carbon: a case study of the Qianyanzhou Forest Experimental Station in China. Clim Chang 67:247–255
Wang YD, Li QK, Wang HM, Wen XF, Yang FT, Ma ZQ, Liu YF, Sun XM, Yu GR (2011) Precipitation frequency controls interannual variation of soil respiration by affecting soil moisture in a subtropical forest plantation. Can J For Res 41:1897–1906
Wang YD, Wang ZL, Wang HM, Guo CC, Bao WK (2012) Rainfall pulse primarily drives litterfall respiration and its contribution to soil respiration in a young exotic pine plantation in subtropical China. Can J Forest Res 42:657–666
Wang H, Liu SR, Wang JX, Shi ZM, Lu LH, Zeng J, Ming AG, Tang JX, Yu HL (2013) Effects of tree species mixture on soil organic carbon stocks and greenhouse gas fluxes in subtropical plantations in China. For Ecol Manag 300:4–13
Wang YS, Cheng SL, Fang HJ, Yu GR, Xu MJ, Dang XS, Li LS, Wang L (2014) Simulated nitrogen deposition reduces CH4 uptake and increases N2O emission from a subtropical plantation forest soil in southern China. Plos One 9:e93571. doi:10.1371/journal.pone.0093571
Whittinghill KA, Currie WS, Zak DR, Burton AJ, Pregitzer KS (2012) Anthropogenic N deposition increases soil C storage by decreasing the extent of litter decay: analysis of field observations with an ecosystem model. Ecosystems 15:450–461
Winjum JK, Schroeder PE (1997) Forest plantations of the world: their extent, ecological attributes, and carbon storage. Agric For Meteorol 84:153–167
Yu GR, Song X, Wang QF, Liu YF, Guan DX, Yan JH, Sun XM, Zhang LM, Wen XF (2008) Water-use efficiency of forest ecosystems in eastern China and its relations to climatic variables. New Phytol 177:927–937
Zak DR, Holmes WE, Burton AJ, Pregitzer KS, Talhelm AF (2008) Simulated atmospheric NO3 - deposition increases soil organic matter by slowing decomposition. Ecol Appl 18:2016–2027
Zak DR, Pregitzer KS, Burton AJ, Edwards IP, Kellner H (2011) Microbial responses to a changing environment: implications for the future functioning of terrestrial ecosystems. Fungal Ecol 4:386–395
Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129
Zhang B, Liang C, He HB, Zhang XD (2013a) Variations in soil microbial communities and residues along an altitude gradient on the northern slope of Changbai Mountain, China. Plos One 8:e66184. doi:10.1371/journal.pone.0066184
Zhang YC, Zhang JB, Meng TZ, Zhu TB, Muller C, Cai ZC (2013b) Heterotrophic nitrification is the predominant NO3 - production pathway in acid coniferous forest soil in subtropical China. Biol Fertil Soils 49:955–957
Zheng XH, Mei BL, Wang YH, Xie BH, Wang YS, Dong HB, Xu H, Chen GX, Cai ZC, Yue J, Gu JX, Su F, Zou JW, Zhu JG (2008) Quantification of N2O fluxes from soil-plant systems may be biased by the applied gas chromatograph methodology. Plant Soil 311:211–234
Acknowledgments
This project was supported by Development Plan Program of State Key Basic Research (No. 2012CB41710), National Natural Science Foundation of China (No. 31130009, 31290222, 41471212, 31470558, and 31290221), Bingwei’s Funds for Young Talents from Institute of Geographical Sciences and Natural Resources Research, CAS (No. 2011RC202), and CAS Strategic Priority Program (No. XDA 05050600).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Wang, Y., Cheng, S., Fang, H. et al. Contrasting effects of ammonium and nitrate inputs on soil CO2 emission in a subtropical coniferous plantation of southern China. Biol Fertil Soils 51, 815–825 (2015). https://doi.org/10.1007/s00374-015-1028-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-015-1028-x