Contrasting effects of long-term acid rain simulation on temperature sensitivity of soil respiration and enzymatic activities in a subtropical forest

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The purpose of this study was to investigate the long-term effects of acid rain simulation (ARS) on soil respiration (Rs) components and enzymatic activities.

Materials and methods

An 8-year field ARS experiment was conducted in a subtropical forest. A trenching method was used to partition Rs into heterotrophic respiration (Rh) and autotrophic respiration (Ra). Soil urease, invertase, and catalase activities were measured after long-term ARS application.

Results and discussion

The repeated-measures ANOVA indicated that there was no significant (P > 0.05) difference in annual mean Rs (or Rh) between SAR plots from March 2016 to February 2018. Rs was significantly (P < 0.001) higher than Rh for each specific ARS treatment across the 2 years. There were no significant (P > 0.05) differences in Q10 of Rs (or Rh) between ARS treatments, indicating that the ARS effect on Q10 was not significant. ARS induced a decline in soil urease activity in both untrenched and trenched plots on most measurement dates. The soil invertase and catalase activities were significantly (P < 0.05) reduced by ARS manipulation but had temporal variations. Long-term ARS did not significantly change Rs in the untrenched plots or Rh in the trenched plots in this subtropical forest ecosystem.


Compared with soil respiration, which is a process involving more biological groups, soil enzymes were more vulnerable to the long-term ARS.

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  1. Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic, London

  2. Bond-Lamberty B, Thomson A (2010a) Temperature-associated increases in the global soil respiration record. Nature 464(7288):579–582

  3. Bond-Lamberty B, Thomson A (2010b) A global database of soil respiration data. Biogeosciences 7(6):1915–1926

  4. 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(1):30–59

  5. Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP (1998) Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 396(6711):570–572

  6. Bowman WD, Cleveland CC, Halada L, Hresko J, Baron JS (2008) Negative impact of nitrogen deposition on soil buffering capacity. Nat Geosci 1(11):767–770

  7. Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49(6):637–644

  8. Cao C, Leng Y, Kufe D (2003) Catalase activity is regulated by c-Abl and Arg in the oxidative stress response. J Biol Chem 278(32):29667–29675

  9. Chen D, Wang Y, Lan Z, Li J, Xing W, Hu S, Bai Y (2015) Biotic community shifts explain the contrasting responses of microbial and root respiration to experimental soil acidification. Soil Biol Biochem 90:139–147

  10. Cheng X, Kang F, Han H, Liu H, Zhang Y (2015) Effect of thinning on partitioned soil respiration in a young Pinus tabulaeformis plantation during growing season. Agric For Meteorol 214:473–482

  11. Dai Z, Lice Y, Wang X, Zhao D (1998) Changes in pH, CEC and exchangeable acidity of some forest soils in southern China during the last 32-35 years. Water Air Soil Pollut 108(3–4):377–390

  12. DeForest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biol Biochem 41(6):1180–1186

  13. Dentener F, Drevet J, Lamarque J, Bey I, Eickhout B, Fiore AM, Hauglustaine D, Horowitz L, Krol M, Kulshrestha U (2006) Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Global Biogeochem Cy 20(4):16615–16615

  14. Enowashu E, Poll C, Lamersdorf N, Kanderler E (2009) Microbial biomass and enzyme activities under reduced nitrogen deposition in a spruce forest soil. Appl Soil Ecol 43(3):11–21

  15. Fang C, Li F, Pei J, Ren J, Gong Y, Yuan Z, Ke W, Zheng Y, Bai X, Ye J (2018) Impacts of warming and nitrogen addition on soil autotrophic and heterotrophic respiration in a semi-arid environment. Agric For Meteorol 248:449–457

  16. Frankenberger WT Jr, Johanson JB (1983) Method of measuring invertase activity in soils. Plant Soil 74(3):301–311

  17. Fritze H (1992) Effects of environmental pollution on forest soil microflora—a review. Silva Fenn 26(1):37–47

  18. Giasson M-A, Averill C, Finzi AC (2014) Correction factors for dissolved organic carbon extracted from soil, measured using the Mn (III)-pyrophosphate colorimetric method adapted for a microplate reader. Soil Biol Biochem 78:284–287

  19. Gopal M, Gupta A, Arunachalam V, Magu SP (2007) Impact of azadirachtin, an insecticidal allelochemical from neem on soil microflora, enzyme and respiratory activities. Bioresour Technol 98(16):3154–3158

  20. Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48(1):115–146

  21. Hou Q, Zhao Y (2009) An analysis on characteristics of regional acid rain over China in 2007. Adv Clim Chang Res 5(1):1673–1719 (in Chinese with English abstract)

  22. Kang H, Lee D (1998) Changes of soil enzyme activities by simulated acid and nitrogen deposition. Chem Ecol 14(2):123–131

  23. Kuribayashi M, Ohara T, Morino Y, Uno I, Kurokawa J, Hara H (2012) Long-term trends of sulfur deposition in East Asia during 1981-2005. Atmos Environ 59:461–475

  24. Kuzyakov Y (2002) Separating microbial respiration of exudates from root respiration in non-sterile soils: a comparison of four methods. Soil Biol Biochem 34(11):1621–1631

  25. Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil Biol Biochem 38(3):425–448

  26. Lavigne MB, Boutin R, Foster RJ, Goodine G, Bernier PY, Robitaille G (2003) Soil respiration responses to temperature are controlled more by roots than by decomposition in balsam fir ecosystems. Can J For Res 33(9):1733–1753

  27. Lee N-Y, Koo J-W, Noh NJ, Kim J, Son Y (2010) Autotrophic and heterotrophic respiration in needle fir and Quercus-dominated stands in a cool-temperate forest, central Korea. J Plant Res 123(4):485–495

  28. Liang N, Hirano T, Zheng Z, Tang J, Fujinuma Y (2010) Soil CO2 efflux of a larch forest in northern Japan. Biogeosciences 7(11):3447–3457

  29. Liang Y, Yang Y, Yang C, Shen Q, Zhou J, Yang L (2003) Soil enzymatic activity and growth of rice and barley as influenced by organic manure in an anthropogenic soil. Geoderma 115(1–2):149–160

  30. Liang G, Liu X, Chen X, Qiu Q, Zhang D, Chu G, Liu J, Liu S, Zhou G (2013) Response of soil respiration to acid rain in forests of different maturity in southern China. PLoS One 8(4):e62207.

  31. Ling D, Zhang J, Ouyang Y, Huang Q (2007) Role of simulated acid rain on cations, phosphorus and organic matter dynamics in latosol. Arch Environ Contam Toxicol 52(1):16–21

  32. Ling D, Huang Q, Ouyang Y (2010) Impacts of simulated acid rain on soil enzyme activities in a latosol. Ecotox Environ Safe 73(8):1914–1918

  33. Liu Y, Liu S, Wan S, Wang J, Luan J, Wang H (2016) Differential responses of soil respiration to soil warming and experimental throughfall reduction in a transitional oak forest in central China. Agric For Meteorol 226–227:186–198

  34. Liu G, Zhang X, Wang X, Shao H, Yang J, Wang X (2017) Soil enzymes as indicators of saline soil fertility under various soil amendments. Agric Ecosyst Environ 237:274–279

  35. Luan J, Liu S, Wang J, Zhu X (2013) Factors affecting spatial variation of annual apparent Q(10) of soil respiration in two warm temperate forests. PLoS One 8(5):e64167.

  36. Lv Y, Wang C, Jia Y, Wang W, Ma X, Du J, Pu G, Tian X (2014) Effects of sulfuric, nitric, and mixed acid rain on litter decomposition, soil microbial biomass, and enzyme activities in subtropical forests of China. Appl Soil Ecol 79:1–9

  37. McColl JG, Firestone MK (1991) Soil chemical and microbial effects of simulated acid rain on clover and soft chess. Water Air Soil Pollut 60(3–4):301–313

  38. Moghimian N, Hosseini SM, Kooch Y, Darki BZ (2017) Impacts of changes in land use/cover on soil microbial and enzyme activities. Catena 157:407–414

  39. Mäkiranta P, Riutta T, Penttil T, Minkkinen K (2010) Dynamics of net ecosystem CO2 exchange and heterotrophic soil respiration following clearfelling in a drained peatland forest. Agric For Meteorol 150(12):1585–1596

  40. Noh NJ, Kuribayashi M, Saitoh TM, Muraoka H (2017) Different responses of soil, heterotrophic and autotrophic respirations to a 4-year soil warming experiment in a cool-temperate deciduous broadleaved forest in central Japan. Agric For Meteorol 247:560–570

  41. Peng S, Piao S, Wang T, Sun J, Shen Z (2009) Temperature sensitivity of soil respiration in different ecosystems in China. Soil Biol Biochem 41(5):1008–1014

  42. Raich JW, Potter CS, Bhagawati D (2002) Interannual variability in global soil respiration, 1980–94. Glob Chang Biol 8(8):800–812

  43. Raiesi F, Salek-Gilani S (2018) The potential activity of soil extracellular enzymes as an indicator for ecological restoration of rangeland soils after agricultural abandonment. Appl Soil Ecol 126:140–147

  44. Reddy GB, Reinert RA, Eason G (1991) Enzymatic changes in the biosphere of loblolly pine exposed to ozone and acid rain. Soil Biol Biochem 23(12):1115–l119

  45. Reddy G, Reinert R, Eason G (1995) Loblolly pine needle nutrient and soil enzyme activity as influenced by ozone and acid rain chemistry. Soil Biol Biochem 27(8):1059–1064

  46. Salonius PO (1990) Respiration rates in forest soil organic horizon materials treated with simulated acid rain. Can J For Res 20(7):910–913

  47. Schloter M, Dilly O, Munch JK (2003) Indicators for evaluating soil quality. Agric Ecosyst Environ 98(1–3):255–262

  48. Singh A, Agrawal M (2008) Acid rain and its ecological consequences. J Environ Biol 29(1):15–24

  49. Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics of northern hardwood forest receiving simulated nitrogen deposition. Biogeochemistry 75(2):201–215

  50. Tamm CO, Hallbacken L (1988) Changes in soil acidity in two forest areas with different acid deposition: 1920s to 1980s. Ambio 17(1):56–61

  51. Teramoto M, Liang N, Zeng J, Saigusa N, Takahashi Y (2017) Long-term chamber measurements reveal strong impacts of soil temperature on seasonal and inter-annual variation in understory CO2 fluxes in a Japanese larch (Larix kaempferi Sarg.) forest. Agric For Meteorol 247:194–206

  52. Tian Q, Liu N, Bai W, Li L, Chen J, Reich PB, Yu Q, Guo D, Smith M, Knapp AK, Cheng W, Lu P, Gao Y, Yang A, Wang T, Li X, Wang Z, Ma Y, Han X, Zhang W (2015) A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe. Ecology 97(1):65–74

  53. Tjoelker MG, Oleksyn J, Reich PB (2001) Modelling respiration of vegetation: evidence for a general temperature-dependent Q 10. Glob Chang Biol 7(2):223–230

  54. Turner DP, Tingey DT (1990) Foliar leaching and root uptake of Ca, Mg and K in relation to acid fog effects on Douglas-fir. Water Air Soil Pollut 49(1):205–214

  55. Vanhala P, Fritze H, Neuvonen S (1996) Prolonged simulated acid rain treatment in the subarctic: effect on the soil respiration rate and microbial biomass. Biol Fertil Soils 23(1):7–14

  56. Van Breeman N, Driscoll CT, Mulder J (1984) Acidification and internal proton sources in acidification of soil and water. Nature 307(5952):599–604

  57. Vet R, Artz RS, Carou S, Shaw M, Ro C-U, Aas W, Baker A, Bowersox VC, Dentener F, Galy-Lacaux C, Hou A, Pienaar JJ, Gillett R, Forti MC, Gromov S, Hara H, Khodzher T, Mahowald NM, Nickovic S, Rao PSP, Reid NW (2014) A global assessment of precipitation chemistry and deposition of sulfur, nitrogen, sea salt, base cations, organic acids, acidity and pH, and phosphorus. Atmos Environ 93:3–100

  58. Walna B, Drzymała S, Siepak J (1998) The impact of acid rain on calcium and magnesium status in typical soils of the Wielkopolski National Park. Sci Total Environ 220(2–3):115–120

  59. Watmough SA, Dillon PJ (2003) Base cation and nitrogen budgets for a mixed hardwood catchment’s in south-central Ontario. Ecosystems 6(7):675–693

  60. Will ME, Graetz DA, Roof BS (1986) Effect of simulated acid precipitation on soil microbial activity in a Typic Quartzipsamment. J Environ Qual 15(4):399–403

  61. Wright BC, Lockaby BG, Meldahl R, Thornton F, Chappelka AH (1990) The influence of acid precipitation and ozone on nitrogen nutrition of young loblolly pine. Water Air Soil Pollut 54(1):135–142

  62. Yu H, He N, Wang Q, Zhu J, Gao Y, Zhang Y, Jia Y, Yu G (2017a) Development of atmospheric acid deposition in China from the 1990s to the 2010s. Environ Pollut 231(Pt 1):182–190

  63. Yu S, Chen Y, Zhao J, Fu S, Li Z, Xia H, Zhou L (2017b) Temperature sensitivity of total soil respiration and its heterotrophic and autotrophic components in six vegetation types of subtropical China. Sci Total Environ 607–608:160–167

  64. Yu P, Liu S, Zhang L, Li Q, Zhou D (2018) Selecting the minimum data set and quantitative soil quality indexing of alkaline soils under different land uses in northeastern China. Sci Total Environ 616–617:564–571

  65. Zhang J, Ouyang Y, Ling D (2007) Impacts of simulated acid rain on cation leaching from the latosol in South China. Chemosphere 67(11):2131–2137

  66. Zhang C, Niu D, Hall SJ, Wen H, Li X, Fu H, Wan C, Elser JJ (2014) Effects of simulated nitrogen deposition on soil respiration components and their temperature sensitivities in a semiarid grassland. Soil Biol Biochem 75:113–123

  67. Zelles L, Scheunert I, Kreutzer K (1987) Effect of artificial irrigation, acid precipitation and liming on the microbial activity in soil of a spruce forest. Biol Fertil Soils 4(3):137–143

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Correspondence to Shutao Chen.

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Chen, S., Sun, L., Zhang, X. et al. Contrasting effects of long-term acid rain simulation on temperature sensitivity of soil respiration and enzymatic activities in a subtropical forest. J Soils Sediments 20, 412–424 (2020).

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  • Acid rain simulation (ARS)
  • Catalase
  • Heterotrophic respiration (R h)
  • Invertase
  • Soil respiration (R s)
  • Urease