Abstract
Elevated atmospheric N deposition has been well documented to enhance fine root production in N-limited temperate forests, but how fine roots respond to N deposition in N-rich tropical and subtropical forests remains poorly understood. The sequential coring and minirhizotron methods were applied to quantify fine root biomass, production, and turnover of a N-rich but P-limited subtropical forest in southern China and to assess the responses of these root variables to a gradient of N additions (control (0), low-N (35), medium-N (70), and high-N (105 kg N ha−1 year−1)) during the first 3 years of experimentation. The high- and medium-N additions significantly reduced fine root diameter by about 30% but increased the specific root length by 20–105%, i.e., fine roots became thinner and longer under the experimental N addition. Both low- and medium-N additions generally stimulated fine root production (10–88%) and turnover (3–40%), whereas high-N suppressed them by 32–70% and 8–54%, respectively, varying with sampling season and estimation method. The stimulatory effects were presumably ascribed to the increased fine root growth for P acquisition, the suppressive effect, to the deleterious damage to the root health and micronutrient availability. Overall, the N effects were more pronounced in the surface (0–10 cm) than in the deeper (10–40 cm) soil layers and for the first-order than the higher-order fine roots. Our results indicate that lower-order absorptive fine roots are responsive to elevated N deposition, and complex responses could emerge due to the interactive influences of the N deposition rate, seasonality, and soil depth.
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References
Addo-Danso SD, Prescott CE, Smith AR (2016) Methods for estimating root biomass and production in forest and woodland ecosystem carbon studies: a review. For Ecol Manag 359:332–351. https://doi.org/10.1016/j.foreco.2015.08.015
Burton AJ, Pregitzer KS, Hendrick RL (2000) Relationships between fine root dynamics and nitrogen availability in Michigan northern hardwood forests. Oecologia 125:389–399. https://doi.org/10.1007/s004420000455
Chen HYH, Brassard BW (2013) Intrinsic and extrinsic controls of fine root life span. Crit Rev Plant Sci 32:151–161. https://doi.org/10.1080/07352689.2012.734742
Cusack DF, Silver WL, Torn MS, McDowell WH (2011) Effects of nitrogen additions on above- and below-ground carbon dynamics in two tropical forests. Biogeochemistry 104:203–225. https://doi.org/10.1007/s10533-010-9496-4
Eissenstat DM, Wells CE, Yanai RD, Whitbecks JL (2000) Building roots in a changing environment implications for root longevity. New Phytol 147:33–42. https://doi.org/10.1046/j.1469-8137.2000.00686.x
Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60. https://doi.org/10.1016/S0065-2504(08)60005-7
Espeleta JF, Clark DA (2007) Multi-scale variation in fine-root biomass in a tropical rain forest: a seven-year study. Ecol Monogr 77:377–404. https://doi.org/10.1890/06-1257.1
Fang Y, Gundersen P, Mo J, Zhu.W. (2008) Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5:339–352. https://doi.org/10.5194/bg-5-339-2008
Finér L, Ohashi M, Noguchi K, Hirano Y (2011) Fine root production and turnover in forest ecosystems in relation to stand and environmental characteristics. For Ecol Manag 262:2008–2023. https://doi.org/10.1016/j.foreco.2011.08.042
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. Science 320:889–892. https://doi.org/10.1126/science.1136674
Gill RA, Jackson RB (2000) Global patterns of root turnover for terrestrial ecosystems. New Phytol 147:13–31. https://doi.org/10.1046/j.1469-8137.2000.00681.x
Goebel M, Hobbie SE, Bulaj B, Zadworny M, Archibald DD, Oleksyn J, Reich PB, Eissenstat DM (2011) Decomposition of the finest root branching orders: linking belowground dynamics to fine-root function and structure. Ecol Monogr 81:89–102. https://doi.org/10.1890/09-2390.1
Grandy AS, Sinsabaugh RL, Neff JC, Stursova M, Zak DR (2008) Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91:37–49. https://doi.org/10.1007/s10533-008-9257-9
Green JJ, Dawson LA, Proctor J, Duff EI, Elston DA (2005) Fine root dynamics in a tropical rain forest is influenced by rainfall. Plant Soil 276:23–32. https://doi.org/10.1007/s11104-004-0331-3
Han X, Shen W, Zhang J, Muller C (2018) Microbial adaptation to long-term N supply prevents large responses in N dynamics and N losses of a subtropical forest. Sci Total Environ 626:1175–1187. https://doi.org/10.1016/j.scitotenv.2018.01.132
Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD, Guo D (2006) Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. J Ecol 94:40–57. https://doi.org/10.1111/j.1365-2745.2005.01067.x
Hogberg P, Nordgren A, Buchmann N, Taylor A, Ekblad A, Hogberg M, Nyberg G, Ottosson-Lofvenius M, Readk D (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792. https://doi.org/10.1038/35081058
Homeier J, Hertel D, Camenzind T, Cumbicus NL, Maraun M, Martinson GO, Poma LN, Rillig MC, Sandmann D, Scheu S, Veldkamp E, Wilcke W, Wullaert H, Leuschner C (2012) Tropical Andean forests are highly susceptible to nutrient inputs—rapid effects of experimental N and P addition to an Ecuadorian montane forest. PLoS One 7:e47128. https://doi.org/10.1371/journal.pone.0047128
Jackson RB, Mooney HA, Schulze E-D (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci U S A 94:7362–7366. https://doi.org/10.1073/pnas.94.14.7362
Jourdan C, Silva EV, Gonçalves JLM, Ranger J, Moreira RM, Laclau JP (2008) Fine root production and turnover in Brazilian Eucalyptus plantations under contrasting nitrogen fertilization regimes. For Ecol Manag 256:396–404. https://doi.org/10.1016/j.foreco.2008.04.034
Kou L, Guo D, Yang H, Gao W, Li S (2015) Growth, morphological traits and mycorrhizal colonization of fine roots respond differently to nitrogen addition in a slash pine plantation in subtroical China. Plant Soil 391:207–218. https://doi.org/10.1007/s11104-015-2420-x
Kou L, Jiang L, Fu X, Dai X, Wang H, Li S (2018) Nitrogen deposition increases root production and turnover but slows root decomposition in Pinus elliottii plantations. New Phytol 218:1450–1461. https://doi.org/10.1111/nph.15066
Li X, Lange H (2015) A modified soil coring method for measuring fine root production, mortality and decomposition in forests. Soil Biol Biochem 91:192–199. https://doi.org/10.1016/j.soilbio.2015.08.015
Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462. https://doi.org/10.1038/nature11917
Lu X, Gilliam FS, Yu G, Li L, Mao Q, Chen H, Mo J (2013) Long-term nitrogen addition decreases carbon leaching in a nitrogen-rich forest ecosystem. Biogeosciences 10:3931–3941. https://doi.org/10.5194/bg-10-3931-2013
Lu X, Mo J, Gilliam FS, Zhou G, Fang Y (2010) Effects of experimental nitrogen additions on plant diversity in an old-growth tropical forest. Glob Change Biol 16:2688–2700. https://doi.org/10.1111/j.1365-2486.2010.02174.x
Lu X, Vitousek PM, Mao Q, Gilliam FS, Luo Y, Zhou G, Zou X, Bai E, Scanlon TM, Hou E, Mo J (2018) Plant acclimation to long-term high nitrogen deposition in an N-rich tropical forest. Proc Natl Acad Sci USA 115:5187–5192.https://doi.org/10.1073/pnas.1720777115
Majdi H, Andersson P (2005) Fine root production and turnover in a Norway spruce stand in northern Sweden: effects of nitrogen and water manipulation. Ecosystems 8:191–199. https://doi.org/10.1007/s10021-004-0246-0
Mao Q, Lu X, Zhou K, Chen H, Zhu X, Mori T, Mo J (2017) Effects of long-term nitrogen and phosphorus additions on soil acidification in an N-rich tropical forest. Geoderma 285:57–63. https://doi.org/10.1016/j.geoderma.2016.09.017
Marschner P (2012) Marschner's mineral nutrition of higher plants. Academic press, New York
McCormack ML, Adams TS, Smithwick EA, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–831. https://doi.org/10.1111/j.1469-8137.2012.04198.x
McCormack ML, Eissenstat DM, Prasad AM, Smithwick EA (2013) Regional scale patterns of fine root lifespan and turnover under current and future climate. Glob Change Biol 19:1697–1708. https://doi.org/10.1111/gcb.12163
McCormack ML, Guo D (2014) Impacts of environmental factors on fine root lifespan. Front Plant Sci 5:205. https://doi.org/10.3389/fpls.2014.00205
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518. https://doi.org/10.1111/nph.13363
Metcalfe DB, Meir P, Aragão LEOC, da Costa ACL, Braga AP, Gonçalves PHL, de Athaydes Silva Junior J, de Almeida SS, Dawson LA, Malhi Y, Williams M (2008) The effects of water availability on root growth and morphology in an Amazon rainforest. Plant Soil 311:189–199. https://doi.org/10.1007/s11104-008-9670-9
Milchunas DG (2009) Estimating root production: comparison of 11 methods in shortgrass steppe and review of biases. Ecosystems 12:1381–1402. https://doi.org/10.1007/s10021-009-9295-8
Mo J, 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. https://doi.org/10.1007/s11104-005-5446-7
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 Change Biol 14:403–412. https://doi.org/10.1111/j.1365-2486.2007.01503.x
Nadelhoffe KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147:131–139. https://doi.org/10.1046/j.1469-8137.2000.00677.x
Nie Y, Wang M, Zhang W, Ni Z, Hashidoko Y, Shen W (2018) Ammonium nitrogen content is a dominant predictor of bacterial community composition in an acidic forest soil with exogenous nitrogen enrichment. Sci Total Environ 624:407–415. https://doi.org/10.1016/j.scitotenv.2017.12.142
Norby RJ, Jackson RB (2000) Root dynamics and global change seeking an ecosystem perspective. New Phytol 147:3–12. https://doi.org/10.1046/j.1469-8137.2000.00676.x
Osawa A, Aizawa R (2012) A new approach to estimate fine root production, mortality, and decomposition using litter bag experiments and soil core techniques. Plant Soil 355:167–181. https://doi.org/10.1007/s11104-011-1090-6
Ostertag R (2001) Effects of nitrogen and phosphorus availability on fine-root dynamics in Hawaiian montane forests. Ecology 82:485–499. https://doi.org/10.1890/0012-9658(2001)082[0485:EONAPA]2.0.CO;2
Ostonen I, Lõhmus K, Pajuste K (2005) Fine root biomass, production and its proportion of NPP in a fertile middle-aged Norway spruce forest: comparison of soil core and ingrowth core methods. For Ecol Manag 212:264–277. https://doi.org/10.1016/j.foreco.2005.03.064
Peng Y, Guo D, Yang Y (2017) Global patterns of root dynamics under nitrogen enrichment. Glob Ecol Biogeogr 26:102–114. https://doi.org/10.1111/geb.12508
Piao S, Fang J, Ciais P, Peylin P, Huang Y, Sitch S, Wang T (2009) The carbon balance of terrestrial ecosystems in China. Nature 458:1009–1013. https://doi.org/10.1038/nature07944
Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north American trees. Ecol Monogr 72:293–309. https://doi.org/10.2307/3100029
Raich JW, Nadelhoffer KJ (1989) Belowground carbon allocation in forest ecosystems: global trends. Ecology 70:1346–1354. https://doi.org/10.2307/1938194
Reay DS, Dentener F, Smith P, Grace J, Feely RA (2008) Global nitrogen deposition and carbon sinks. Nat Geosci 1:430–437. https://doi.org/10.1038/ngeo230
Ruess RW, Cleve KV, Yarie J, Viereck LA (1996) Contributions of fine root production and turnover to the carbon and nitrogen cycling in taiga forests of the Alaskan interior. Can J For Res 26:1326–1336. https://doi.org/10.1139/x26-148
Schenk HJ, Jackson RB (2002) The global biogeography of roots. Ecol Monogr 72:311–328. https://doi.org/10.1890/0012-9615(2002)072[0311:TGBOR]2.0.CO;2
Smithwick EAH, Eissenstat DM, Lovett GM, Bowden RD, Rustad LE, Driscoll CT (2013) Root stress and nitrogen deposition: consequences and research priorities. New Phytol 197:712–719. https://doi.org/10.1111/nph.12081
Tateno R, Hishi T, Takeda H (2004) Above- and below-ground biomass and net primary production in a cool-temperate deciduous forest in relation to topographical changes in soil nitrogen. For Ecol Manag 193:297–306. https://doi.org/10.1016/j.foreco.2003.11.011
Tonitto C, Goodale CL, Weiss MS, Frey SD, Ollinger SV (2013) The effect of nitrogen addition on soil organic matter dynamics: a model analysis of the Harvard Forest chronic nitrogen amendment study and soil carbon response to anthropogenic N deposition. Biogeochemistry 117:431–454. https://doi.org/10.1007/s10533-013-9887-4
Wells CE, Eissenstat DM (2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82:882–892. https://doi.org/10.2307/2680206
Wells CE, Glenn DM, Eissenstat DM (2002) Changes in the risk of fine-root mortality with age: a case study in peach, Prunus persica (Rosaceae). Am J Bot 89:79–87. https://doi.org/10.3732/ajb.89.1.79
Yu G, Chen Z, Piao S, Peng C, Ciais P, Wang Q, Li X, Zhu X (2014) High carbon dioxide uptake by subtropical forest ecosystems in the East Asian monsoon region. Proc Natl Acad Sci USA 111:4910–4915. https://doi.org/10.1073/pnas.1317065111
Yuan Z, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutrient contents in boreal forest ecosystems in relation to species, climate, fertility, and stand age: literature review and meta-analyses. Crit Rev Plant Sci 29:204–221. https://doi.org/10.1080/07352689.2010.483579
Yuan Z, Chen HYH (2012) A global analysis of fine root production as affected by soil nitrogen and phosphorus. Proc Biol Sci 279:3796–3802. https://doi.org/10.1098/rspb.2012.0955
Yuan Z, Chen HYH, Ostle N (2012) Fine root dynamics with stand development in the boreal forest. Funct Ecol 26:991–998. https://doi.org/10.1111/j.1365-2435.2012.02007.x
Zhu F, Lu X, Liu L, Mo J (2015) Phosphate addition enhanced soil inorganic nutrients to a large extent in three tropical forests. Sci Rep 5:7923. https://doi.org/10.1038/srep07923
Zhu F, Yoh M, Gilliam FS, Lu X, Mo J (2013) Nutrient limitation in three lowland tropical forests in southern China receiving high nitrogen deposition: insights from fine root responses to nutrient additions. PLoS One 8:e82661. https://doi.org/10.1371/journal.pone.0082661
Acknowledgments
We thank the Dinghushan forest ecosystem research station, CAS, for platform support, and we thank Yanxia Nie, Shengnan Ouyang and Weiren Wang for their helps with the field sampling. Three anonymous reviewers provided constructive comments that helped the revision of the manuscript.
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This work was supported by the National Natural Science Foundation of China (31425005, 31290222), and the National Ten Thousand Talents Program.
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WS and WW conceived the ideas and designed the study; WW, QM, and XH collected the samples and analyzed the data; DH took part in writing and data analysis; all authors contributed to the writing and revision of the manuscript.
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Wang, W., Mo, Q., Han, X. et al. Fine root dynamics responses to nitrogen addition depend on root order, soil layer, and experimental duration in a subtropical forest. Biol Fertil Soils 55, 723–736 (2019). https://doi.org/10.1007/s00374-019-01386-3
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DOI: https://doi.org/10.1007/s00374-019-01386-3