Abstract
Understanding forest carbon cycling responses to atmospheric N deposition is critical to evaluating ecosystem N dynamics. The natural abundance of 15N (δ15N) has been suggested as an efficient and non-invasive tool to monitor N pools and fluxes. In this study, three successional forests in southern China were treated with four levels of N addition. In each treatment, we measured rates of soil N mineralization, nitrification, N2O emission and inorganic N leaching as well as N concentration and δ 15N of leaves, litters and soils. We found that foliar N concentration and δ15N were higher in the mature broadleaf forest than in the successional pine or mixed forests. Three-year continuous N addition did not change foliar N concentration, but significantly increased foliar δ 15N (p < 0.05). Also, N addition decreased the δ 15N of top soil in the N-poor pine and mixed forests and significantly increased that of organic and mineral soils in N-rich broadleaf forests (p < 0.05). In addition, the soil N2O emission flux and inorganic N leaching rate increased with increasing N addition and were positively correlated with the 15N enrichment factor (ε p/s) of forest ecosystems. Our study indicates that δ 15N of leaf, litter and soil integrates various information on plant species, forest stand age, exogenous N input and soil N transformation and loss, which can be used to monitor N availability and N dynamics in forest ecosystems caused by increasing N deposition in the future.
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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
Adams M, Ineson P, Binkley D, Cadisch G, Scholes M, Hicks K, Tokuchi N (2004) Soil functional responses to excess nitrogen inputs at global scale. Ambio 33:530–536
Aoyama M, Kumakura N (2001) Quantitative and qualitative changes of organic matter in an Ando soil induced by mineral fertilizer and cattle manure applications for 20 years. Soil Sci Plant Nutr 47:241–252
Arunachalam A, Maithani K, Pandey HN, Tripathi RS (1998) Leaf litter decomposition and nutrient mineralization patterns in regrowing stands of a humid subtropical forest after tree cutting. For Ecol Manage 109:151–161
Boeckx P, Paulino L, Oyarzun C, van Cleemput O, Godoy R (2005) Soil δ15N patterns in old-growth forests of southern Chile as integrator for N-cycling. Isotopes Environ Health Stud 41:249–259
Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497
Chen Y, Högberg P (2006) Gross nitrogen mineralization rates still high 14 years after suspension of N input to a N-saturated forest. Soil Biol Biochem 38:2001–2003
Choi WJ, Lee SM, Ro HM, Kim KC, Yoo SH (2002) Natural 15N abundances of maize and soil amended with urea and composted pig manure. Plant Soil 245:223–232
Choi WJ, Chang SX, Allen HL, Kelting DL, Ro HM (2005) Irrigation and fertilization effects on foliar and soil carbon and nitrogen isotope ratios in a loblolly pine stand. For Ecol Manage 213:90–101
Davidson EA, Chorover J, Dail DB (2003) A mechanism of abiotic immobilization of nitrate in forest ecosystems: the ferrous wheel hypothesis. Glob Chang Biol 9:228–236
Davidson EA, de Carvalho CJR, Vieira ICG, Figueiredo RD, Moutinho P, Ishida FY, dos Santos MTP, Guerrero JB, Kalif K, Saba RT (2004) Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol Appl 14:S150–S163
Dijkstra P, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA (2008) 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11:389–397
Emmett BA, Kjonaas OJ, Gundersen P, Koopmans C, Tietema A, Sleep D (1998) Natural abundance of 15N in forests across a nitrogen deposition gradient. For Ecol Manage 101:9–18
Eshetu Z (2004) Natural N-15 abundance in soils under young-growth forests in Ethiopia. For Ecol Manage 187:139–147
Fang YT, Mo JM, Zhou GY, Gundersen P, Li DJ, Jiang YQ (2004) The short-term responses of soil available nitrogen of Dinghushan forests to simulated N deposition in subtropical China. Acta Ecologica Sinica 21:2353–2359
Fang YT, Gundersen P, Mo JM, Zhu WX (2008) Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5:339–352
Fang HJ, Yu GR, Cheng SL, Mo JM, Yan JH, Li SG (2009a) 13C abundance, water-soluble and microbial biomass carbon as potential indicators of soil organic carbon dynamics in subtropical forests at different successional stages and subject to different nitrogen loads. Plant Soil 320:243–254
Fang YT, Gundersen P, Mo JM, Zhu WX (2009b) Nitrogen leaching in response to increased nitrogen inputs in subtropical monsoon forests in southern China. For Ecol Manage 257:332–342
Fang YT, Zhu WX, Gundersen P, Mo JM, Zhou GY, Yoh M (2009c) Large loss of dissolved organic nitrogen from nitrogen-saturated forests in subtropical China. Ecosystems 12:33–45
Fenn ME, Poth MA, Aber JD, Baron JS, Bormann BT, Johnson DW, Lemly AD, McNulty SG, Ryan DE, Stottlemyer R (1998) Nitrogen excess in North American ecosystems: predisposing factors, ecosystem responses, and management strategies. Ecol Appl 8:706–733
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 Manage 196:159–171
Gundersen P, Emmett BA, Kjonaas OJ, Koopmans CJ, Tietema A (1998) Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. For Ecol Manage 101:37–55
He C, Chen S, Liang Y (1982) The soils of Dinghushan biosphere reserve tropical and subtropical forest. Ecosystem 1:25–38
Högberg P (1997) Tansley review No 95—15N natural abundance in soil-plant systems. New Phytol 137:179–203
Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA 104:8902–8906
Huygens D, Ruetting T, Boeckx P, Van Cleemput O, Godoy R, Mueller C (2007) Soil nitrogen conservation mechanisms in a pristine south Chilean Nothofagus forest ecosystem. Soil Biol Biochem 39:2448–2458
Koopmans CJ, van Dam D, Tietema A, Verstraten JM (1997) Natural N-15 abundance in two nitrogen saturated forest ecosystems. Oecologia 111:470–480
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498
Lohse KA, Matson P (2005) Consequences of nitrogen additions for soil processes and solution losses from wet tropical forests. Ecol Appl 15:2209
Luyssaert S, Schulze ED, Borner A, Knohl A, Hessenmoller D, Law BE, Ciais P, Grace J (2008) Old-growth forests as global carbon sinks. Nature 455:213–215
MacDonald JA, Dise NB, Matzner E, Armbruster M, Gundersen P, Forsius M (2002) Nitrogen input together with ecosystem nitrogen enrichment predict nitrate leaching from European forests. Glob Chang Biol 8:1028–1033
Magill AH, Aber JD, Berntson GM, McDowell WH, Nadelhoffer KJ, Melillo JM, Steudler P (2000) Long-term nitrogen additions and nitrogen saturation in two temperate forests. Ecosystems 3:238–253
Malhi SS, Nyborg M, Harapiak JT, Heier K, Flore NA (1997) Increasing organic C and N in soil under bromegrass with long-term N fertilization. Nutr Cycl Agroecosyst 49:255–260
Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K (1999) Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry 46:45–65
McDowell WH, Magill AH, Aitkenhead-Peterson JA, Aber JD, Merriam JL, Kaushal SS (2004) Effects of chronic nitrogen amendment on dissolved organic matter and inorganic nitrogen in soil solution. For Ecol Manage 196:29–41
Merino A, Perez-Batallon P, Macias F (2004) Responses of soil organic matter and greenhouse gas fluxes to soil management and land use changes in a humid temperate region of southern Europe. Soil Biol Biochem 36:917–925
Mo HM, Brown S, Peng SL, Kong G (2003) Nitrogen availability in disturbed, rehabilitated and mature forests of tropical China. For Ecol Manage 175:573–583
Mo JM, Brown S, Xue J, Fang Y, Li Z (2006) Response of litter decomposition to simulated N deposition in disturbed, rehabilitated and mature forests in subtropical China. Plant Soil 282:135–151
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 J, Zhang W, Zhu W, Gundersen P, Fang Y, Li D, Wang H (2008) Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Glob Chang Biol 14:403–412
Nadelhoffer K, Shaver G, Fry B, Giblin A, Johnson L, McKane R (1996) 15N natural abundances and N use by tundra plants. Oecologia 107:386–394
Nadelhoffer KJ, Emmett BA, Gundersen P, Kjonaas OJ, Koopmans CJ, Schleppi P, Tietema A, Wright RF (1999) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148
Pardo LH, Hemond HF, Montoya JP, Fahey TJ, Siccama TG (2002) Response of the natural abundance of 15N in forest soils and foliage to high nitrate loss following clear-cutting. Can J For Res 32:1126–1136
Pardo LH, Templer PH, Goodale CL, Duke S, Groffman PM, Adams MB, Boeckx P, Boggs J, Campbell J, Colman B, Compton J, Emmett B, Gundersen P, Kjonaas J, Lovett G, Mack M, Magill A, Mbila M, Mitchell MJ, McGee G, McNulty S, Nadelhoffer K, Ollinger S, Ross D, Rueth H, Rustad L, Schaberg P, Schiff S, Schleppi P, Spoelstra J, Wessel W (2006) Regional assessment of N saturation using foliar and root delta N-15. Biogeochemistry 80:143–171
Peng SL, Wang BS (1995) Forest succession at Dinghushan, Guangdong, China. Chin J Bot 7:75–80
Perakis SS, Hedin LO (2002) Nitrogen loss from unpolluted South American forests mainly via dissolved organic compounds. Nature 418:665
Pörtl K, Zechmeister-Boltenstern S, Wanek W, Ambus P, Berger TW (2007) Natural 15N abundance of soil N pools and N2O reflect the nitrogen dynamics of forest soils. Plant Soil 295:79–94
Sah SP, Rita H, Ilvesniemi H (2006) 15N natural abundance of foliage and soil across boreal forests of Finland. Biogeochemistry 80:277–288
Selmants PC, Hart SC (2008) Substrate age and tree islands influence carbon and nitrogen dynamics across a retrogressive semiarid chronosequence. Global Biogeochem Cycles 22:GB1021. doi:10.1029/2007GB003062
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
Venterea RT, Groffman PM, Verchot LV, Magill AH, Aber JD, Steudler PA (2003) Nitrogen oxide gas emissions from temperate forest soils receiving long-term nitrogen inputs. Glob Chang Biol 9:346–357
Venterea RT, Groffman PM, Verchot LV, Magill AH, Aber JD (2004) Gross nitrogen process rates in temperate forest soils exhibiting symptoms of nitrogen saturation. For Ecol Manage 196:129–142
Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention—hypothesis. Bioscience 25:376–381
Watzka M, Buchgraber K, Wanek W (2006) Natural 15N abundance of plants and soils under different management practices in a montane grassland. Soil Biol Biochem 38:1564–1576
Yun SI, Ro HM (2009) Natural 15N abundance of plant and soil inorganic-N as evidence for over-fertilization with compost. Soil Biol Biochem 41:1541–1547
Zhang W, Mo JM, Yu GR, Fang YT, Li DJ, Lu XK, Wang H (2008a) Emissions of nitrous oxide from three tropical forests in Southern China in response to simulated nitrogen deposition. Plant Soil 306:221–236
Zhang W, Mo JM, Zhou GY, Gundersen P, Fang YT, Lu XK, Zhang T, Dong SF (2008b) Methane uptake responses to nitrogen deposition in three tropical forests in southern China. J Geophys Res-Atmospheres 113:D1116. doi:10.1029/2007JD009195
Zhao BZ, Maeda M, Ozaki Y (2002) Natural 15N and 13C abundance in Andisols influenced by long-term fertilization management in Japan. Soil Sci Plant Nutr 48:555–562
Zheng XH, Fu CB, Xu XK, Yan XD, Huang Y, Han SH, Hu F, Chen GX (2002) The Asian nitrogen cycle case study. Ambio 31:79–87
Zhou GY, Liu SG, Li Z, Zhang DQ, Tang XL, Zhou CY, Yan JH, Mo JM (2006) Old-growth forests can accumulate carbon in soils. Science 314:1417
Acknowledgements
This research was funded by National Key Research and Development Program (2010CB833502), National Natural Science Foundation of China (30600071, 40601097, 30590381), Knowledge Innovation Project of the Chinese Academy of Sciences (KZCX2-YW-432, O7V70080SZ, LENOM07LS-01) and the President Fund of GUCAS (O85101PM03). We gratefully acknowledge Dr. Sherry Becky, Dr. Xuhui Zhou, and Dr. Yuanhe Yang for revising the English writing of the manuscript. We appreciate the two anonymous reviewers for their valuable suggestions and effort on this paper.
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Fang, H., Yu, G., Cheng, S. et al. Nitrogen-15 signals of leaf-litter-soil continuum as a possible indicator of ecosystem nitrogen saturation by forest succession and N loads. Biogeochemistry 102, 251–263 (2011). https://doi.org/10.1007/s10533-010-9438-1
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DOI: https://doi.org/10.1007/s10533-010-9438-1