Abstract
Purpose
Forest recovery from disturbance can alter soil nitrogen (N) status as a result of complex interactions in plant-soil system. The δ15N and δ18O are indicators that integrate complex soil N processes and can help elucidate changes in soil N status. Our objectives were to evaluate differences in soil N status among different forest recovery stages in karst plateau in southwestern China.
Methods
We established a forest recovery gradient with sites in cropland, abandoned cropland, shrub land, and early- and late-successional forests. We measured concentrations and isotopic compositions of soil total N, ammonium (NH4+), and nitrate (NO3−), and δ15N of plant tissue.
Results
With increased levels of recovery, concentrations of soil total N increased, and δ15N of soil total N (δ15NSTN) decreased at 0 ~ 10 cm depth. A positive relationship between δ15NSTN in surface soil and δ15N of plant (P < 0.05) suggested that recovery of plant biomass was the main contributor to soil N recovery. A large difference between δ15N of litter and δ15NSTN demonstrated an important dependence of plants on mycorrhizal fungi for N acquisition. δ15N of NH4+ was lower than δ15NSTN, and a significant correlation between δ15N and δ18O of NO3− was observed only in late-successional forest (slope = l.4), indicating that gas N emission had a minor contribution to N loss. Ratio of ammonium N to nitrate N was < 1 (except in cropland), suggesting low risk of leaching.
Conclusions
Forest recovery promoted soil N recovery, and reduced soil N loss in karst plateau. However, N limitation persisted throughout forest recovery stages.
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Data availability
All data generated during this study are included in this published article.
References
Amundson R, Austin AT, Schuur EAG, Yoo K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cycle 17:11. https://doi.org/10.1029/2002gb001903
Boutton TW and Liao JD (2010) Changes in soil nitrogen storage and δ15N with woody plant encroachment in a subtropical savanna parkland landscape. J Geophys Res 115. https://doi.org/10.1029/2009jg001184
Cao L, Wang SJ, Peng Tao, Cheng QY, Zhang L, Zhang ZC, Yue FJ, Alan EF (2020) Monitoring of suspended sediment load and transport in an agroforestry watershed on a karst plateau, Southwest China. Agric Ecosyst Environ 299:106976. https://doi.org/10.1016/j.agee.2020.106976
Cao J, Yuan D, Pei J (2005) Karst Ecosystem of Southwest China Constrained by Geological Setting. Geology Press, Beijing
Casciotti KL, Sigman DM, Hastings MG, Bohlke JK, Hilkert A (2002) Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal Chem 74:4905–4912. https://doi.org/10.1021/ac020113w
Craine JM et al (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992. https://doi.org/10.1111/j.1469-8137.2009.02917.x
Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Penuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980-992. doi:10.1111/j.1469-8137.2009.02917.x
Davidson E, Carvalho CuRd, Figueira AM, Ishida FY, Ometto JP, Nardoto G, Saba RT (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–999. https://doi.org/10.1038/nature05900
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559. https://doi.org/10.1146/annurev.ecolsys.33.020602.095451
Denk T, Mohn J, Decock C, Lewicka-Szczebak D, Harris E, Butterbach-Bahl K, Kiese R, Wolf B (2017) The nitrogen cycle: A review of isotope effects and isotope modeling approaches. Soil Biol Biochem 105: 121-137. https://doi.org/10.1016/j.soilbio.2016.11.015.
Evans RD, Bloom AJ, Sukrapanna SS, Ehleringer JR (1996) Nitrogen isotope composition of tomato {Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition. Plant Cell Physiol 19: 1317-1323. https://doi.org/10.1111/j.1365-3040.1996.tb00010.x
Fanelli KN and Rothstein DE (2017) Replacement of wildfire by whole-tree harvesting increases nitrification and nitrate movement in jack pine forest soils. Forest Ecol Manag 402:115–121. https://doi.org/10.1016/j.foreco.2017.07.030
Fang YT, Koba K, Makabe A, Takahashi C, Zhu WX, Hayashi T, Hokari AA, Urakawa R, Bai E, Houlton BZ, Xi D, Zhang SS, Matsushita K, Tu Y, Liu DW, Zhu FF, Wang ZY, Zhou GY, Chen DX, Makita T, Toda H, Liu XY, Chen QS, Zhang DQ, Li YD, Yoh M (2015) Microbial denitrification dominates nitrate losses from forest ecosystems. Proc Natl Acad Sci USA 112:1470-1474. https://doi.org/10.1073/pnas.1416776112
Ford D and Williams P (2007) Karst hydrogeology and geomorphology, 2nd edn. Wiley, West Sussex
Gessler AM, Kreuzwieser J, Dopatka T, Rennenberg H (2002) Stomatal uptake and cuticular adsorption contribute to dry deposition of NH3 and NO2 to needles of adult spruce (Picea abies) trees. New Phytol 156(2):179–194. https://doi.org/10.1023/a:1015831304911
Granger J and Wankel SD (2016) Isotopic overprinting of nitrification on denitrification as a ubiquitous and unifying feature of environmental nitrogen cycling. Proc Natl Acad Sci U S A 113:E6391-E6400. https://doi.org/10.1073/pnas.1601383113
Granger J, Sigman DM, Rohde MM, Maldonado MT, Tortell PD (2010) N and O isotope effects during nitrate assimilation by unicellular prokaryotic and eukaryotic plankton cultures. Geochim Cosmochim Acta 74:1030–1040. https://doi.org/10.1016/j.gca.2009.10.044
Guillaume T, Damris M, Kuzyakov Y (2015) Losses of soil carbon by converting tropical forest to plantations: erosion and decomposition estimated by delta C-13. Glob Change Biol 21:3548–3560. https://doi.org/10.1111/gcb.12907
Guo ZM, hang XY, Green SM, Dungait JAJ, Wen XF, Quine TA (2019) Soil enzyme activity and stoichiometry along a gradient of vegetation restoration at the Karst Critical Zone Observatory in Southwest China. Land Degrad Dev 30(16): 1916-1927. https://doi.org/10.1002/ldr.3389
He NP, Liu CC, Piao SL, Sack L, Xu L, Luo YQ, He JS, Han XG, Zhou GS, Zhou XH, Lin Y, Yu Q, Liu SR, Sun W, Niu SL, Li SG, Zhang JH, Yu GR (2019) Ecosystem Traits Linking Functional Traits to Macroecology. Trends Ecol Evol 34(3): 200-210. https://doi.org/10.1016/j.tree.2018.11.004
Heaton TH, Spiro EB, Madeline S, Robertson C (1997) Potential canopy influences on the isotopic composition of nitrogen and sulphur in atmospheric deposition. Oecologia 109(4):600–607. https://doi.org/10.1007/s004420050122
Hobbie E, Hogberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196(2):367–382. https://doi.org/10.1111/j.1469-8137.2012.04300.x
Hogberg P (1997) 15N natural abundance in soil-plant systems. New Phytol 137:515–525
Hogberg P, Johannisson C, Yarwood S, Callesen I, Nasholm T, Myrold DD, Hogberg MN (2011) Recovery of ectomycorrhiza after ‘nitrogen saturation’ of a conifer forest. New Phytol 189:515–525. https://doi.org/10.1111/j.1469-8137.2010.03485.x
Holloway JM, Dahlgren RA (2002) Nitrogen in rock: occurrences and biogeochemical implications. Glob Biogeochem Cycles 16(4):17. https://doi.org/10.1007/s004420050122
Houlton B and Bai E (2009) Imprint of denitrifying bacteria on the global terrestrial biosphere. Proc Natl Acad Sci U S A 106:21713–21716. https://doi.org/10.1073/pnas.0912111106
Houlton BZ, Sigman DM, Hedin LO (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci U S A 103:8745–8750. https://doi.org/10.1073/pnas.0510185103
Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211. https://doi.org/10.2307/1942661
Jiang ZC, Lian YQ, Qin XQ (2014) Rocky desertification in Southwest China: Impacts, causes, and restoration. Earth-Sci Rev 132:1–12. https://doi.org/10.1016/j.earscirev.2014.01.005
Jones AR and Dalal RC (2017) Enrichment of natural N-15 abundance during soil N losses under 20 years of continuous cereal cropping. Sci Total Environ 574:282–287. https://doi.org/10.1016/j.scitotenv.2016.08.192
Kelley CJ, Keller CK, Evans RD, Orr CH, Smith JL, Harlow BA (2013) Nitrate-nitrogen and oxygen isotope ratios for identification of nitrate sources and dominant nitrogen cycle processes in a tile-drained dryland agricultural field. Soil Biol Biochem 57:731–738. https://doi.org/10.1016/j.soilbio.2012.10.017
Kendall C, Elliott EM, Wankel SD (2007) Tracing anthropogenic inputs of nitrogen to ecosystems. In Robert M and Kate L (ed) Stable isotopes in ecology and environmental science, 2rd edn. Blackwell Pub, PP 375-449.
Kreyling J, Schweiger AH, Bahn M, Ineson P, Migliavacca M, Morel-Journel T, Christiansen JR, Schtickzelle N, Larsen KS (2018) To replicate, or not to replicate - that is the question: how to tackle nonlinear responses in ecological experiments. Ecol Lett 21:1629-1638. https://doi.org/10.1111/ele.13134
Li DD, Zhang XY, Sophie G, Jennifer D, Wen XF, Tang YQ, Guo ZM, Yang Y, Sun XM, Timothy Q (2018) Nitrogen functional gene activity in soil profiles under progressive vegetative recovery after abandonment of agriculture at the Puding Karst Critical Zone Observatory, SW China. Soil Biol Biochem 125:93-102. https://doi.org/10.1016/j.soilbio.2018.07.004
Liu CC, Liu YG, Guo K, Wang SJ, Liu HM, Zhao HW, Qiao XG, Hou DJ, Li SB (2016) Aboveground carbon stock, allocation and sequestration potential during vegetation recovery in the karst region of southwestern China: A case study at a watershed scale. Agric Ecosyst Environ 235:91-100. https://doi.org/10.1016/j.agee.2016.10.003
Liu DW, Zhu WX, Wang XB, Pan YP, Wang C, Xi D, Bai E, Wang YS, Han XG, and Fang YT (2017) Abiotic versus biotic controls on soil nitrogen cycling in drylands along a 3200km transect. Biogeoscie 14:989-1001. https://doi.org/10.5194/bg-14-989-2017
Liu DW, Fang YT, Tu Y, Pan YP (2014) Chemical method for nitrogen isotopic analysis of ammonium at natural abundance. Anal Chem 86:3787–3792. https://doi.org/10.1021/ac403756u
Luo H, Pu T, Chen Z, Liu F (2010) Effect of different vegetation community on soil nutrients of microhabitat in Southern karst areas of Guizhou province. Guizhou Agricultural Sciences 38(6):112–115. (In Chinese)
Niu SL, Classen AT, Dukes JS, Kardol P, Liu LL, Luo YQ, Rustad L, Sun J, Tang JW, Templer PH, Thomas RQ, Tian DS, Vicca S, Wang YP, Xia JY, Zaehle S (2016) Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecol Lett 19:697-709. https://doi.org/10.1111/ele.12591
Pan FJ, Liang YM, Zhang W, Zhao J, Wang KL (2016) Enhanced nitrogen availability in karst ecosystems by oxalic acid release in the rhizosphere. Front Plant Sci 7:9. https://doi.org/10.3389/fpls.2016.00687
Pellegrini AFA, Hoffmann WA, Franco AC (2014) Carbon accumulation and nitrogen pool recovery during transitions from savanna to forest in central Brazil. Ecology 95:342–352. https://doi.org/10.1890/13-0290.1
Peng T and Wang SJ (2012) Effects of land use, land cover and rainfall regimes on the surface runoff and soil loss on karst slopes in southwest China. Catena 90:53–62. https://doi.org/10.1016/j.catena.2011.11.001
Reich PB and Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. P Natl Acad Sci USA 101:11001–11006. https://doi.org/10.1073/pnas.0403588101
Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153-162. https://doi.org/10.1016/s0169-5347(00)02098-x
Rutting T, Clough TJ, Muller C, Lieffering M, Newton PCD (2010) Ten years of elevated atmospheric carbon dioxide alters soil nitrogen transformations in a sheep-grazed pasture. Global Change Biol 16(9): 2530-2542. https://doi.org/10.1111/j.1365-2486.2009.02089.x
Ruiz-Navarro A, Barbera GG, Albaladejo J, Querejeta JI (2016) Plant delta(15) N reflects the high landscape-scale heterogeneity of soil fertility and vegetation productivity in a Mediterranean semiarid ecosystem. New Phytol 212:1030–1043. https://doi.org/10.1111/nph.14091
Schimel JP and Bennett J (2004) Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85:591–602. https://doi.org/10.1890/03-8002
Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Bohlke JK (2001) A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73:4145–4153. https://doi.org/10.1021/ac010088e
Song M, He TG, Chen H, Wang KL, Li DJ (2019) Dynamics of soil gross nitrogen transformations during post-agricultural succession in a subtropical karst region. Geoderma 341: 1-9. https://doi.org/10.1016/j.geoderma.2019.01.034
Sun XB, Zhang QS, Xiao KC, Li DJ (2020) Variation of asymbiotic nitrogen fixation with post-agricultural succession in a karst region of Northwest Guangxi. Research of agricultural modernization 41(4):709–717. (In Chinese)
Tong XW, Brandt M, Yue YM, Horion S, Wang KL, Keersmaecker WD, Tian F, Schurgers G, Xiao XM, Luo YQ, Chen C, Myneni R, Shi Z, Chen HS, Fensholt R (2018) Increased vegetation growth and carbon stock in China karst via ecological engineering. Nat Sustain 1:44-50. https://doi.org/10.1038/s41893-017-0004-x
Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc B-Biol Sci 368:9. https://doi.org/10.1098/rstb.2013.0119
Wang SJ, Liu QM, Zhang DF (2004) Karst rocky desertification in southwestern China: Geomorphology, landuse, impact and rehabilitation. Land Degrad Dev 15:115–121. https://doi.org/10.1002/ldr.592
Wang J, Wen X, Zhang X, Li S, Zhang D (2018) Co-regulation of photosynthetic capacity by nitrogen, phosphorus and magnesium in a subtropical Karst forest in China. Sci Rep 8:7406. https://doi.org/10.1038/s41598-018-25839-1
Wen L, Li DJ, Yang LQ, Luo P, Chen H, Xiao KC, Song TQ, Zhang W, He XY, Chen HS, Wang KL (2016) Rapid recuperation of soil nitrogen following agricultural abandonment in a karst area, southwest China. Biogeochem 129:341-354. https://doi.org/10.1007/s10533-016-0235-3
Xiao HW, Xiao HY, Long AM, Wang YL (2012) Who controls the monthly variations of NH4+ nitrogen isotope composition in precipitation? Atmos Environ 54:201–206. https://doi.org/10.1016/j.atmosenv.2012.02.035
Xiao KC, Li DJ, Wen L, Yang LQ, Luo P, Chen H, Wang KL (2018) Dynamics of soil nitrogen availability during post-agricultural succession in a karst region, southwest China. Geoderma 314:184–189. https://doi.org/10.1016/j.geoderma.2017.11.018
Yue FJ, Li SL, Liu C, Lang Y, Ding H (2015) Sources and transport of nitrate constrained by the isotopic technique in a karst catchment: an example from Southwest China. Hydrol Process 29:1883–1893. https://doi.org/10.1002/hyp.10302
Zeng J, Yue FJ, Li SL, Wang ZJ, Qin CQ, Wu QX, Xu S (2020) Agriculture driven nitrogen wet deposition in a karst catchment in southwest China. Agric Ecosyst Environ 294:10. https://doi.org/10.13872/j.1000-0275.2020.0057
Zhang SS, Fang Y, and Xi D (2015) Adaptation of micro-diffusion method for the analysis of 15N natural abundance of ammonium in samples with small volume. RCM 29(14):1297–1306. https://doi.org/10.1002/rcm.7224
Zhou XB, Tao Y, Yin BF, Tucker C, Zhang YM (2020) Nitrogen pools in soil covered by biological soil crusts of different successional stages in a temperate desert in Central Asia. Geoderma 366:9. https://doi.org/10.1016/j.geoderma.2019.114166
Acknowledgements
All auxiliary datasets were shared from “Functional Trait database of terrestrial ecosystems in China (China_Trait)”. Special thanks to Puding Karst Ecosystem Observation and Research Station, Chinese Ecosystem Research Network (CERN) of Chinese Academy of Sciences for providing the study with convenient conditions.
Funding
This study was supported by the National Key Research and Development Program of China (2017YFC0503904), and the National Natural Science Foundation of China (41830860 and 41571130043).
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J.W., X.F.W. and S.D.L. planed and designed the research. J.W. performed experiments and analyzed data. All authors jointly wrote the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Wang, J., Wen, X., Lyu, S. et al. Vegetation recovery alters soil N status in subtropical karst plateau area: Evidence from natural abundance δ15N and δ18O. Plant Soil 460, 609–623 (2021). https://doi.org/10.1007/s11104-020-04797-6
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DOI: https://doi.org/10.1007/s11104-020-04797-6