Abstract
Aims
As an important contributor to carbon (C) flux in the global C cycle, fine root litter in forests has the potential to be affected by the elevated nitrogen (N) deposition observed globally. However, the direct effects (on current fine root decomposition) and indirect effects (on root quality and subsequent decomposition) of N deposition on fine root decomposition are poorly understood.
Methods
We conducted a 5-year field experiment in a Pleioblastus amarus bamboo forest in southwestern China. In the first 3 years of the experiment, N-treated sites (0, 50, 150, and 300 kg N ha−1 year−1, respectively) and fine roots under two N regimes (0 and 150 kg N ha−1 year−1; 0 N-Root/+N-Root, respectively) were prepared. Next, these two fine root treatments were applied to a 2-year decomposition experiment in the N-treated sites under continuous N treatment.
Results
Nitrogen additions increased fine root density, concentrations of N, P, and lignin in fine roots, and concentrations of TOC, TN, NH4 +-N and NO3 −-N in the soil, and decreased the soil pH. The decomposition constant k decreased under N addition treatments, and the decomposition rate of + N-Root was lower than that of 0 N-Root, suggesting that both the direct and indirect effects of N additions on fine root decomposition rates were negative. Both N addition and root substrate changes led to an increase in the residual lignin content during decomposition. Nitrogen additions significantly decreased the loss of C, N, P, K, Ca and Mg during decomposition.
Conclusions
The changes in the soil environment and increased root lignin concentration as a result of N additions may be the mechanism underlying the negative direct and indirect effects observed. Elevated fine root biomass input and slower degradation rates may be a potential mechanism explaining the increase in soil TOC and TN under N treatment.
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Aber JD, 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. Biosci 48(11):921–934
Baron JS, Hall EK, Nolan BT, Finlay JC, Bernhardt ES, Harrison JA, Chan F, Boyer EW (2013) The interactive effects of excess reactive nitrogen and climate change on aquatic ecosystems and water resources of the United States. Biogeochemistry 114:71–92. doi:10.1007/s10533-012-9788-y
Berg B (1986) Nutrient release from litter and humus in coniferous forest soils – a mini review. Scand J Forest Res 1(1–4):359–369
Berg B, Laskowski R (2006) Litter decomposition: A guide to carbon and nutrient turnover. Elsevier Ltd., Burlington
Berg B, Matzner E (1997) Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environ Rev 5:1–25
Berg B, McClaugherty C (2008) Plant litter: Decomposition, humus formation, carbon sequestration, 2nd edn. Springer, Heidelberg
Berg B, Staaf H (1980) Decomposition rate and chemical changes of scots pine needle litter II. Influence of chemical composition. Ecol Bull 32:373–390
Birouste M, Kazakou E, Blanchard A, Roumet C (2011) Plant traits and decomposition: are the relationships for roots comparable to those for leaves? Ann Bot. doi:10.1093/aob/mcr297
Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-M, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition on plant diversity : a synthesis. Ecol Appl 20:30–59. doi:10.1890/08-1140.1
Boddy E, Hill PW, Farrar J, Jones DL (2007) Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field soils. Soil Biol Biochem 39:827–835. doi:10.1016/j.soilbio.2006.09.030
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. Forest Ecol Manag 196:43–56. doi:10.1016/j.foreco.2004.03.011
Burton AJ, Pregitzer KS, Reuss RW, Hendrick RL, Allen MF (2002) Root respiration in North American forests: effects of nitrogen concentration and temperature across biomes. Oecologia 131:559–568. doi:10.1007/s00442-002-0931-7
Cairns MA, Brown S, Helmer EH, Baumgardner GA (1997) Root biomass allocation in the world’s upland forests. Oecologia 111:1–11. doi:10.1007/s004420050201
Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecol 81:2359–2365. doi:10.1890/0012-9658(2000)081[2359:MESELD]2.0.CO;2
Chen X, Zhang X, Zhang Y, Booth T, He X (2009) Changes of carbon stocks in bamboo stands in China during 100 years. Forest Ecol Manag 258:1489–1496. doi:10.1016/j.foreco.2009.06.051
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. doi:10.1073/pnas.0600989103
Cui J, Zhou J, Peng Y, He Y, Yang H, Mao J, Zhang M, Wang Y, Wang S (2014) Atmospheric wet deposition of nitrogen and sulfur in the agroecosystem in developing and developed areas of Southeastern China. Atmosph Envrion 89:102–108. doi:10.1016/j.atmosenv.2014.02.007
Denman KL, Brasseur G, Chidthaisong A, Ciais P, Cox PM, Dickinson RE, Hauglustaine D, Heinze C, Holland E, Jacob D, Lohmann U, Ramachandran S, da Silva Dias PL, Wofsy SC, Zhang X (2007) Couplings between changes in the climate system and biogeochemistry. In: Solomon S, Qin D, Manning M, Marquis M, Averyt K, Tignor MMB, Miller HLR, Chen Z (eds) Climate change 2007, the physical science basis. Contribution of working group i to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 499–587
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 Cy 20(4). doi:10.1029/2005GB002672
Falconer GJ, Wright JW, Beall HW (1933) The decomposition of certain types of fresh litter under field conditions. Am J Bot 20:196–203
Fang H, Mo J, Peng S, Li Z, Wang H (2007) Cumulative effects of nitrogen additions on litter decomposition in three tropical forests in southern China. Plant Soil 297:233–242. doi:10.1007/s11104-007-9339-9
Fang YT, Gundersen P, Vogt RD, Koba K, Chen F, Chen X, Yoh M (2011) Atmospheric deposition and leaching of nitrogen in Chinese forest ecosystems. J Forest Res 16:341–350. doi:10.1007/s10310-011-0267-4
FAO (2010) Global forest resources assessment 2010: Main report. Food and Agriculture Organization of the United Nations, Rome
Fitter A (2002) Characteristics and functions of root systems. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: The hidden half. Marcel Dekker, New York
Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–462
Fujii S, Takeda H (2010) Dominant effects of litter substrate quality on the difference between leaf and root decomposition process above- and belowground. Soil Biol Biochem 42:2224–2230. doi:10.1016/j.soilbio.2010.08.022
Fujimaki R, Takeda H, Wiwatiwitaya D (2008) Fine root decomposition in tropical dry evergreen and dry deciduous forests in Thailand. J Forest Res 13:338–346. doi:10.1007/s10310-008-0087-3
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:10.1007/s10533-004-0370-0
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Sci 320:889–892. doi:10.1126/science.1136674
Gan H, Zak DR, Hunter MD (2013) Chronic nitrogen deposition alters the structure and function of detrital food webs in a northern hardwood ecosystem. Ecol Appl 23:1311–1321. doi:10.1890/12-1895.1
Gholz HL, Wedin DA, Smitherman SM, Harmon ME, Parton WJ (2000) Long-term dynamics of pine and hardwood litter in contrasting environments: toward a global model of decomposition. Global Change Biol 6:751–765. doi:10.1046/j.1365-2486. 2000.00349.x
Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31. doi:10.1046/j.1469-8137.2000.00681.x
Grimshaw HM, Allen SE, Parkinson JA (1989) Nutrient elements. In: Allen SE (ed) Chemical analysis of ecological material. Blackwell Scientific, Oxford, pp 81–159
Helmisaari HS, Saarsalmi A, Kukkola M (2009) Effects of wood ash and nitrogen fertilization on fine root biomass and soil and foliage nutrients in a Norway spruce stand in Finland. Plant Soil 314:121–132. doi:10.1007/s11104-008-9711-4
Hendricks JJ, Nadelhoffer KJ, Aber JD (1993) Assessing the role of fine roots in carbon and nutrient cycling. Trends Ecol Evol 8:174–178. doi:10.1016/0169-5347(93)90143-D
Hobbie SE (2008) Nitrogen effects on decomposition: a five-year experiment in eight temperate sites. Ecol 89:2633–2644. doi:10.1890/07-1119.1
Hobbie SH, Vitousek PM (2000) Nutrient limitation of decomposition in Hawaiian forests. Ecol 81:1867–1877. doi:10.1890/0012-9658(2000)081[1867:NLODIH]2.0.CO;2
Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB (2010) Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162:505–513. doi:10.1007/s00442-009-1479-6
Hu ZY, Xu CK, Zhou LN, Sun BH, He YQ, Zhou J, Cao ZH (2007) Contribution of atmospheric nitrogen compounds to N deposition in a broadleaf forest of southern China. Pedosphere 17:360–365. doi:10.1016/S1002-0160(07)60043-5
Huttunen L, Aphalo PJ, Lehto T, Niemela P, Kuokkanen K, Kellomaki S (2009) Effects of elevated temperature, elevated CO2 and fertilization on quality and subsequent decomposition of silver birch leaf litter. Soil Biol Biochem 41:2414–2421. doi:10.1016/j.soilbio.2009.08.014
Jackson ML (1958) Soil chemical analysis. Prantice Hall Inc., Englewood Cliffs
Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci U S A 94:7362–7366
Jia S, Wang Z, Li X, Sun Y, Zhang X, Liang A (2010) N fertilization affects on soil respiration, biomass and root respiration in Larix gmelinii and Fraxinus mandshurica plantations in China. Plant Soil 333:325–336. doi:10.1007/s11104-010-0348-8
Jones JB, Case VW (1990) Sampling, handling, and analyzing plant tissue samples. In: Westerman RL (ed) Soil testing and plant analysis. Soil Science Society of America, Inc., Madison, pp 390–428
Jourdan C, Silva EV, Goncalves JLM, Ranger J, Moreira RM, Laclau JP (2008) Fine root production and turnover in Brazilian Eucalyptus plantations under contrasting nitrogen fertilization regimes. Forest Ecol Manag 256:396–404. doi:10.1016/j.foreco.2008.04.034
Kalembasa SJ, Jenkinson DSA (1973) comparative study of titrimetric and gravimetric methods for determination of organic carbon in soil. J Sci Food Agr 24:1085–1090
Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43. doi:10.1111/j.1461-0248.2007.01124.x
Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosyst 12:1–15. doi:10.1007/s10021-008-9199-z
Keyser P, Kirk TK, Zeikus IG (1978) Ligninolytic enzyme of phanerochaete chrysosporium: synthesized in the absence of lignin in response to nitrogen starvation. J Bacteriol 135:790–797
Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecol 86:3252–3257. doi:10.1890/05-0150
Lee KH, Jose S (2003) Soil respiration, fine root production, and microbial biomass in cottonwood and loblolly pine plantations along a nitrogen fertilization gradient. Forest Ecol Manag 185:263–273. doi:10.1016/S0378-1127(03)00164-6
Lin CF, Yang YS, Guo JF, Chen G, Xie J (2011) Fine root decomposition of evergreen broadleaved and coniferous tree species in mid-subtropical China: dynamics of dry mass, nutrient and organic fractions. Plant Soil 338:311–327. doi:10.1007/s11104-010-0547-3
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. Nat 494:459–462. doi:10.1038/nature11917
Ludovici KH, Kress LW (2006) Decomposition and nutrient release from fresh and dried pine roots under two fertilizer regimes. Can J Forest Res 36:105–111
Magill AH, Aber JD (1998) Long-term effects of experimental nitrogen additions on foliar litter decay and humus formation in forest ecosystems. Plant Soil 203:301–311. doi:10.1023/A:1004367000041
Matson P, Lohse K, Jall SJ (2002) The globalization of nitrogen: consequences for terrestrial ecosystems. Ambio 31:113–119. doi:10.1579/0044-7447-31.2.113
Mo J, Zhang W, Zhu W, Gundersen P, Fang Y, Li D, Wang H (2007) Nitrogen addition reduces soil respiration in a mature tropical forest in southern. Global Chang Biol 14:1–10. doi:10.1111/j.1365-2486.2007.01503.x
Nadelhoffer KJ, Raich JW (1992) Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecol 73:1139–1147
Nambiar EKS, Fife DF (1991) Nutrient retranslocation in temperate conifers. Tree Physiol 9:185–207. doi:10.1093/treephys/9.1-2.185
Nelson DW, Sommers LE (1982) Total carbon, OC, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2. Agronomy Society of America and Soil Science Society of America, Madison, pp 539–577
Nikula S, Vapaavuori E, Manninen S (2010) Urbanization-related changes in European aspen (Populus tremula L.): Leaf traits and litter decomposition. Environ Poll 158:2132–2142. doi:10.1016/j.envpol.2010.02.025
Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates the response of a deciduous forest to atmospheric CO2 enrichment. Proc Natl Acad Sci 101:9689–9693. doi:10.1073/pnas.0403491101
NRC (National Research Council (1996) Understanding marine biodiversity. National Academy Press, Washington
Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2. Agronomy Society of America and Soil Science Society of America, Madison, pp 403–430
Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecol 44:322–331
Ostertag R, Hobbie SE (1999) Early stages of root and leaf decomposition in Hawaiian forests: effects of nutrient availability. Oecologia 121:564–573. doi:10.1007/s0044 20050963
Powers JS, Treseder KK, Lerdau MT (2005) Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distances. New Phytol 165:913–921. doi:10.1111/j.1469-8137.2004.01279.x
Pregitzer KS, Burton A (1992) Foliar sulfur and nitrogen along an 800-km pollution gradient. Can J Forest Res 22:1761–1769
Rabalais NN (2002) Nitrogen in aquatic ecosystems. Ambio 31:102–112. doi:10.1579/ 0044-7447-31.2.102
Reay DS, Dentener F, Smith P, Grace J, Feely RA (2008) Global nitrogen deposition and carbon sinks. Nat Geosci 1:430–437. doi:10.1038/ngeo230
Ring E, Jacobson S, Högbom L (2011) Long-term effects of nitrogen fertilization on soil chemistry in three Scots pine stands in Sweden. Can J Forest Res 41:279–288. doi:10.1139/X10-208
Rowland AP, Roberts JD (1994) Lignin and cellulose fractionation in decomposition studies using acid-detergent fiber methods. Commun Soil Sci Plan 25:26–277
SFAPRC (2010) Statistics of forest resources in China (2004–2008). State Forestry Administration, People’s Republic of China, Available: http://cfdb.forestry.gov.cn:443/showpdf.action. Accessed 2014 Aug 16
Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419. doi:10.1007/s004420100740
Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404. doi:10.1016/j.soilbio.2009.10.014
Song X, Jiang H, Zhang Z, Zhou G, Zhang S, Peng C (2013) Interactive effects of elevated UV-B radiation and N deposition on decomposition of Moso bamboo litter. Soil Biol Biochem 69:11–16. doi:10.1016/j.soilbio.2013.10.036
Sun T, Mao Z, Han Y (2013) Slow decomposition of very fine roots and some factors controlling the process: a 4-year experiment in four temperate tree species. Plant Soil 372:445–458. doi:10.1007/s11104-013-1755-4
Tateno R, Hishi T, Takeda H (2004) Above- and belowground biomass and net primary production in a cool-temperate deciduous forest in relation to topographical changes in soil nitrogen. Forest Ecol Manag 193:297–306. doi:10.1016/j.foreco.2003.11.011
Tu LH, Hu TX, Zhang J, Li RH, Dai HZ, Luo SH (2011) Short-term simulated nitrogen deposition increases carbon sequestration in a Pleioblastus amarus plantation. Plant Soil 340:383–396. doi:10.1007/s11104-010-0610-0
Tu LH, Hu TX, Zhang J, Huang LH, Xiao YL, Chen G, Hu HL, Liu L, Zheng JK, Xu ZF, Chen LH (2013a) Nitrogen distribution and cycling through water flows in a subtropical bamboo forest under high level of atmospheric deposition. PLoS One 8:e75862. doi:10.1371/journal.pone.0075862
Tu LH, Hu TX, Zhang J, Li XW, Hu HL, Liu L, Xiao YL (2013b) Nitrogen addition stimulates different components of soil respiration in a subtropical bamboo ecosystem. Soil Biol Biochem 58:255–264. doi:10.1016/j.soilbio.2012.12.005
Tu LH, Chen G, Peng Y, Hu HL, Hu TX, Zhang J, Li XW, Liu L, Tang Y (2014a) Soil biochemical responses to nitrogen addition in a bamboo forest. PLoS One 9:e102315. doi:10.1371/journal.pone.0102315
Tu LH, Hu HL, Chen G, Peng Y, Xiao YL, Hu TX, Zhang J, Li XW, Liu L, Tang Y (2014b) Nitrogen addition significantly affects forest litter decomposition under high levels of ambient nitrogen deposition. PLoS One 9:e88752. doi:10.1371/journal.pone.0088752
Van Groenigen KJ, Six J, Hungate BA, de Graaff MA, van Breemen N, van Kessel C (2006) Element interactions limit soil carbon storage. Proc Natl Acad Sci U S A 103:6571–6574. doi:10.1073/pnas.0509038103
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. doi:10.1890/1051-0761(1997)007[0737:HAOTGN]2.0.CO;2
Waldrop MP, Zak DR, Sinsabaugh RL, Gallo M, Lauber C (2004) Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–1177. doi:10.1890/03-5120
Wang C, Han S, Zhou Y, Yan C, Cheng X, Zheng X, Li M (2012) Responses of fine roots and soil N availability to short-term nitrogen fertilization in a broad-leaved Korean pine mixed forest in northeastern China. PLoS One 7:e31042. doi:10.1371/journal.pone. 0031042
Xiao YL, Tu LH, Hu TX, Zhang J, Li XW, Hu HL (2013) Early effects of simulated nitrogen deposition on annual nutrient input from litterfall in a Pleioblastus amarus plantation in rainy area of West China. Acta Ecol Sin 33:7355–7363. doi:10.5846/stxb201208301224, in Chinese with English abstract
Xu ZF, Tu LH, Hu TX, Zhang J, Li XW, Hu HL (2013) Implications of greater than average increases in nitrogen deposition on the western edge of the Szechwan Basin, China. Environ Poll 177:201–202. doi:10.1016/j.envpol.2012.12.031
Yang YS, Chen GS, Guo JF, Lin P (2004) Decomposition dynamic of fine roots in a mixed forest of Cunninghamia lanceolata and Tsoongiodendron odonum in mid-subtropics. Ann Forest Sci 61:65–72. doi:10.1051/forest:2003085
Zhang DQ, Hui DF, Luo YQ, Zhou GY (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85–93. doi:10.1093/jpe/rtn002
Zhao X, Yan X, Xiong Z, Xie Y, Xing G, Shi S, Zhu Z (2009) Spatial and temporal variation of inorganic nitrogen wet deposition to the Yangtze River Delta region, China. Water Air Soil Poll 203:277–289. doi:10.1007/s11270-009-0011-2
Zogg GP, Zak DR, Burton AJ, Pregitzer KS (1996) Fine root respiration in northern hardwood forests in relation to temperature and nitrogen availability. Tree Physiol 16:719–725. doi:10.1093/treephys/16.8.719
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This project was supported by the National Natural Science Foundation of China (No. 31300522), the Specialized Research Fund for the Doctoral Program of Higher Education of China (No. 20125103120018) and the Scientific Research Fund of Sichuan Provincial Education Department of China (No. 12ZA118).
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Tu, Lh., Peng, Y., Chen, G. et al. Direct and indirect effects of nitrogen additions on fine root decomposition in a subtropical bamboo forest. Plant Soil 389, 273–288 (2015). https://doi.org/10.1007/s11104-014-2353-9
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DOI: https://doi.org/10.1007/s11104-014-2353-9